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",isbn:"978-1-83969-506-3",printIsbn:"978-1-83969-505-6",pdfIsbn:"978-1-83969-507-0",doi:null,price:0,priceEur:0,priceUsd:0,slug:null,numberOfPages:0,isOpenForSubmission:!0,hash:"0e5d67464d929fda6d8c83ec20c4138a",bookSignature:"Dr. Endre Zima",publishedDate:null,coverURL:"https://cdn.intechopen.com/books/images_new/10704.jpg",keywords:"Anatomy, Physiology, Perioperative, Non-Cardiac Causes, Antiarrhythmic Drugs, Development, SARS-CoV2, Infection, Cardiac Arrest, Resuscitation, PPE, Arrhythmias",numberOfDownloads:null,numberOfWosCitations:0,numberOfCrossrefCitations:null,numberOfDimensionsCitations:null,numberOfTotalCitations:null,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"February 11th 2021",dateEndSecondStepPublish:"March 11th 2021",dateEndThirdStepPublish:"May 10th 2021",dateEndFourthStepPublish:"July 29th 2021",dateEndFifthStepPublish:"September 27th 2021",remainingDaysToSecondStep:"2 days",secondStepPassed:!1,currentStepOfPublishingProcess:2,editedByType:null,kuFlag:!1,biosketch:"Prof. Dr. Endre Zima works as the chief of Cardiac ICU at Semmelweis University Heart and Vascular Center. His fields of interest are intensive cardiac care, CPR, post-cardiac arrest care, device therapy of arrhythmias, defibrillator waveform, and AED development.",coeditorOneBiosketch:null,coeditorTwoBiosketch:null,coeditorThreeBiosketch:null,coeditorFourBiosketch:null,coeditorFiveBiosketch:null,editors:[{id:"201263",title:"Dr.",name:"Endre",middleName:null,surname:"Zima",slug:"endre-zima",fullName:"Endre Zima",profilePictureURL:"https://mts.intechopen.com/storage/users/201263/images/system/201263.jpg",biography:"Prof. Dr. Endre Zima works as the chief of Cardiac ICU at Semmelweis University Heart and Vascular Center. Dr. Zima is specialized in anesthesiology-intensive care and cardiology. He has authored 13 book chapters and more than 130 journal papers, achieved a Hirsch-index of 14, g-index of 22, and more than 650 independent citations. \nHe has been holding graduate and postraduate lectures and practices in anesthesiology since 2006, and in cardiology since 2008. He is a PhD Lecturer in Semmelweis University since 2010. He obtains an accreditation of EHRA on Cardiac Pacing and Implantable Cardioverter Defibrillators, he is accredited AALS Instructor of European Resuscitation Council. \nHe is a Fellow of the European Society of Cardiology, member of the European Heart Rhythm Association and Acute Cardiovascular Care Association, board member of the Hungarian Society of Cardiology (HSC), president of Working Group (WG) on Cardiac Pacing of HSC , board member of WG of Heart Failure. Dr. Zima is also a member the Hungarian Society of Resuscitation, Hungarian Society of Anesthesiology. 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Venkateswarlu",coverURL:"https://cdn.intechopen.com/books/images_new/371.jpg",editedByType:"Edited by",editors:[{id:"58592",title:"Dr.",name:"Arun",surname:"Shanker",slug:"arun-shanker",fullName:"Arun Shanker"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"878",title:"Phytochemicals",subtitle:"A Global Perspective of Their Role in Nutrition and Health",isOpenForSubmission:!1,hash:"ec77671f63975ef2d16192897deb6835",slug:"phytochemicals-a-global-perspective-of-their-role-in-nutrition-and-health",bookSignature:"Venketeshwer Rao",coverURL:"https://cdn.intechopen.com/books/images_new/878.jpg",editedByType:"Edited by",editors:[{id:"82663",title:"Dr.",name:"Venketeshwer",surname:"Rao",slug:"venketeshwer-rao",fullName:"Venketeshwer Rao"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"4816",title:"Face Recognition",subtitle:null,isOpenForSubmission:!1,hash:"146063b5359146b7718ea86bad47c8eb",slug:"face_recognition",bookSignature:"Kresimir Delac and Mislav Grgic",coverURL:"https://cdn.intechopen.com/books/images_new/4816.jpg",editedByType:"Edited by",editors:[{id:"528",title:"Dr.",name:"Kresimir",surname:"Delac",slug:"kresimir-delac",fullName:"Kresimir Delac"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}}]},chapter:{item:{type:"chapter",id:"17479",title:"Bioresources for Third-Generation Biofuels",doi:"10.5772/17134",slug:"bioresources-for-third-generation-biofuels",body:'Modern societies’ welfare relies greatly on fossil fuels. The current energy model, based on the extensive utilization of fossil fuels, is affected by economic and environmental problems. The United States Department of Energy 2009 report estimates that, within the next two decades, global energy consumption will double (Conti, 2009). On the other hand, the European Commission 2009 report indicates that the management of climate change problems in Europe, since 2000, has been globally unfavourable. Nevertheless, there are some positive signs, such as the 1.4% reduction in 2007 of CO2 emissions with respect to the figures obtained from 2000 to 2004 in the European Union of Fifteen (E-15). However, considering the 27 European states (E-27), and paying attention to the consumption and production of renewable energy and biofuels, the reduction in emissions has not fulfilled the European Union objectives. Among the motives of this negative evaluation, the fall in the companies’ productivity, increased transport and industry emissions and the reduction in research and development areas can be cited (Radermacher, 2009). First- and second-generation biofuels could ameliorate or solve the associated fossil fuel depletion problems, although their recent implantation has raised some doubts. The main problems associated with biofuels are the food vs. fuel controversy; the agricultural and forestry land usage and the actual sustainability of biofuels’ production. Third-generation biofuels, based on the microbiological processing of agricultural, urban and industrial residues, could be a possible solution. However, several technical problems must be solved to make them economically viable and easily affordable for the industry (Robles-Medina et al., 2009).
The parallel progression in energy demands over depleting oil reserves and rising greenhouse gas emissions entails a high risk of severe impacts on biodiversity, humankind food security and welfare. Thus, a new energy model is needed, based on greener and renewable energy sources, and cleaner as well as more sustainable fuel technology (Fortman et al., 2008; Jegannathan et al., 2009).
The first response of heavy industry to the current energy and environmental problems includes some old systems, such as syngas and Fischer Tropsch liquids. Current advances in technology and engineering could bring new opportunities to these classical chemistry and biochemistry solutions, associated with fuel shortage situations such as the Arab oil embargo of the 1970s, or the Second World War. Some of these will be detailed below.
Biogas is an attractive source of energy primarily because it is renewable and enables the recycling of organic waste. The production of biogas from manure can help to manage the problems associated with this residue, contributing to the reduction of the greenhouse gas methane. Besides, biomethanation is not only useful for energy production, but also for cleaning up solid waste in urban areas. Compared with bioethanol from wheat and biodiesel from rapeseed, biogas production based on energy crops could generate about twice the net energy yield per hectare per year. Furthermore, biogas could be produced from the by-products generated by the current bioethanol and biodiesel industries (Jegannathan et al., 2009).
Biogas production is based on bacterial methanogenesis in the absence of air of organic matter in a water solution. The process occurs in three steps. The first, hydrolysis, is carried out by strict anaerobes such as Bacteroides or Clostridia, and facultative anaerobes such as Streptococci. It involves the enzymatic transformation of insoluble organic material and higher molecular mass compounds such as lipids, polysaccharides, proteins, nucleic acids etc. into soluble organic materials — energy and cell carbon sources such as monosaccharides and amino acids, among others. In the second step, acidogenesis, other types of microorganisms ferment the mentioned products to acetic acid, hydrogen, carbon dioxide and other lower weight simple volatile organic acids, such as propionic and butyric acid, which are converted to acetic acid. Finally, organic acids, hydrogen and carbon dioxide are converted into a mixture of methane and carbon dioxide by the methanogenic bacteria such as Methanosarcina spp. or Methanothrix spp. (consuming acetate), as well as microorganisms such as Methanobacterium sp. and Methanococcus sp., or others that consume hydrogen and formate to yield methane (Jegannathan et al., 2009).
In spite of its attractions, biogas has only been used in rural areas of developing countries and has received investment from governmental and non-profit organizations. The absence of private investment is due to some technical limitations that hamper its economic viability. The process is relatively slow and unstable, and requires large volumes of digester. The decrease in gas generation during the winter season is a serious problem, and can lead to the clogging of the reactor. Other causes for the reduction in gas production are pH and temperature variations, so the loading rate and solid concentration have to be continuously maintained (Jegannathan et al., 2009).
Synthetic gas, known as syngas, is a mixture of H2, CO and CO2 in different proportions. Traditionally, syngas was produced through gasification of coal at high temperatures, but it can also be produced by methane reformation (submitting the methane to a high temperature water steam stream, or hydrocracking) or by gasification of biomass. In the latter case, the obtained gas is called biosyngas. Syngas and biosyngas can be used directly as fuel, but they also can serve as precursors for other fuels, such as hydrogen, obtained by the compression of carbon monoxide and dioxide. Also, by Fischer-Tropsch synthesis (FTS), short and long chain hydrocarbons can be obtained from the aforementioned H2, CO and CO2 mixture (Srinivas et al., 2007). Fischer-Tropsch synthesis was discovered in the first half of the twentieth century and developed for large-scale production during the Second World War. It is based on the polymerization, through successive stages, of H2 with CO and CO2, yielding linear hydrocarbons. Iron, cobalt or ruthenium can be used as catalysts (Huber et al., 2006). FTS can be developed at high or low temperature. The high temperature FTS is performed at 330–350ºC yielding mostly short-chain hydrocarbons (gasolines) and light olefins in a fluidized-bed reactor. On the other hand, low temperature FTS develops at 220–250ºC in a slurry bubble column reactor, and waxes and long-chain hydrocarbons are obtained (Bludowsky & Agar, 2009). As FTS is an extremely exothermic reaction, it can be coupled with biomass gasification. However, FTS has some drawbacks, such as the fact that complex mixtures of different chain lengths are always obtained. Thus, FTS products have to be separated prior to subsequent processes (Huber et al., 2006).
The direct usage of crude or filtered vegetable oils for diesel engine fuel is possible by blending them with conventional diesel fuels in a suitable ratio. These blends are easy to obtain and keep stable for short-term use. But vegetable oils present high viscosity, acid contamination and free fatty acids that lead to gum formation by oxidation, polymerization and carbon deposition (Ranganathan, 2008). Thus, the long-term utilization of vegetable oils for fuel leads to filter clogging, nozzle blockage and deposits in the combustion chamber (Sidibé et al., 2010). Alongside the long-term problems in injection systems, filters and combustion chamber, doubts about the sustainability of using crude vegetable oil for fuels have to be considered. Vegetable oils are expensive, and their direct use in engines or as feedstock to produce petro-diesel substitutes would encounter the same economic and environmental problems that affect the conventional biodiesel and bioethanol industries (UNCTAD, 2010).
A more interesting solution is the usage of waste cooking oil (WCO; also called waste frying oil, WFO). Waste cooking oil is widely produced, inedible, and could serve as a low-cost and almost ready-to-use substitute for fossil origin diesel. As crude vegetable oil, waste cooking oil has a high viscosity. Besides, it is enriched with free fatty acids and, hence, can generate clogging problems in unmodified diesel vehicles, especially in temperate climates and during the ignition of the engine. Viscosity problems are usually bypassed by blending WCO with petrol diesel or by using transesterification to produce biodiesel (Pugazhvadivu et al., 2005; Al-Zuhair et al., 2009; Chen et al., 2009). Al-Zuhair et al. studied the production of biodiesel with lipases from Candida antarctica and Burkholderia cepacia, both free and immobilized in ceramic beads, with or without solvents. They found that clay micro-environments protected immobilized B. cepacia lipase from methanol damage (Al-Zuhair et al., 2009). Also, Pugazhvadivu et al. proposed solving the injection and filter-clogging problems by preheating the waste cooking oil (Pugazhvadivu et al., 2005), by comparing the performance of a diesel engine when using conventional diesel and waste frying oil, preheated at different temperatures, as fuel. They found that preheating the waste frying oil to 135ºC improved the overall yield of the engine. In particular, the brake specific energy consumption and brake thermal efficiency were improved, and the engine exhaust CO and smoke density were reduced considerably compared to WFO preheated at 75ºC. They concluded that WFO could be used as a diesel fuel by preheating it to 135ºC.
Bioethanol and biodiesel are frequently claimed as the most realistic alternatives to fossil fuels. These renewable fuels can be extensively produced, and both the fossil fuel distribution and engines can be easily adapted to work with blends of ethanol and gasoline, diesel and biodiesel, or even pure ethanol and pure biodiesel (Da Costa et al., 2010). But, in order to play a significant role in fossil fuel substitution, these renewable fuel industries should overcome technical limitations in production process efficiency and feedstock-related issues (UNCTAD, 2010). Decisions about feedstock election, catalysis technology or energy gain along the production process are of paramount importance for proper biodiesel and bioethanol production.
Bioethanol is produced from simple sugar-rich raw materials or from starchy feedstock, from which simple sugars can be easily processed and released, which are fermented to produce ethanol. Bioethanol production comprises three steps. Firstly, the complex sugars are hydrolysed to release glucose. Subsequently, the glucose is subjected to a second fermentation step carried out by yeasts such as Saccharomyces cerevisiae; for example, yielding ethanol and carbon dioxide. The third step consists of a thermochemical process and is based on the distillation of the diluted ethanol to obtain highly concentrated ethanol. When using lignocellulosic raw materials such as agricultural residues (corn stover, straw, sugar cane bagasse), forestry waste, wastepaper and other cellulosic residues, a chemical or enzymatic hydrolysis pretreatment to degrade the lignin is needed. This additional step reduces the efficiency of the process. Some improvements have been achieved by the engineering of cellulases from the Trichoderma genus fungi (Fukuda et al., 2006) and the utilization of microorganisms able to simultaneously express the cellulase and enzymes needed for the ethanol fermentation pathway, such as piruvate descarboxilases and alcohol dehydrogenases (Lu et al., 2006; van Zyl et al., 2007; Jegannathan et al., 2009; Rahman et al., 2009; van Dam et al., 2009). However, these improvements have still not generated an efficient and economically affordable process.
With regard to biodiesel, it consists of a mixture of fatty acid alkyl esters (FAAE) obtained by the transesterification of fatty acids and straight chain alcohols (generally ethanol or methanol), mainly from vegetable oils. When methanol is the alcohol of choice, the term used to refer to the biodiesel is fatty acid methyl esters (FAME), while the ethanol-derived biodiesel is known as fatty acid ethyl esters (FAEE). The properties of the biodiesel obtained from ethanol or methanol are very similar, but methanol is the preferred alcohol in spite of its toxicity and fossil fuel origin because of its low cost and wide availability (Ranganathan et al., 2008; Fjerbaek et al., 2009).
The commercially delivered biodiesel is mainly obtained by the chemical transesterification of the triglycerides contained in sunflower, rapeseed or palm oil. This process can be carried out by acid and alkaline liquid catalysts (Kawahara & Ono, 1979; Jeromin et al., 1987; Aksoy et al., 1988; Fukuda et al., 2001), or heterogeneous solid catalysts such as supported metals, basic oxides or zeolites (Cao et al., 2008). The preferred catalysts are the liquid ones, particularly the alkaline ones, because these catalysts are cheap, very versatile and yield less corrosive fuel than the acid catalysts. Also, liquid catalysts are preferred because the reusable solid catalysts are still withdrawn with mass transfer and reactant diffusion problems. However, the alkaline catalysis has several limitations, especially the futile consumption of the catalyst, problems of viscosity, mass transfer and recovery of biodiesel and by-products owing to the saponification of the catalyst and free fatty acids in the presence of water (Freedman et al., 1984; Zhang et al., 2003; Jaruwat et al., 2010). These problems are bypassed by high temperature reaction conditions, addition of organic solvents to manage the water presence or enhance the interface formation, or increase of the alcohol:catalysts ratio (Kawahara & Ono, 1979; Fukuda et al., 2001). Thus, the process requires high energy inputs to maintain high temperatures conducive to viable transesterification rates, and to separate methanol. Besides, the process generates alkaline waste water that requires treatment prior to its disposal (Jaruwat et al., 2010). Jointly, all these negative factors raise doubts about the sustainability and environmental benefits of the biodiesel industry.
Extensive bioethanol and biodiesel implantation has been followed by a panoply of economic, sociopolitical and environmental issues (Guerrero-Compeán, 2008). It is worth noting the strong dependency of these biofuels industries on crops used for human nourishment and the feeding of livestock (UNCTAD, 2010). Although a large number of patents have been proposed to solve many technical problems, the sudden peak in demand for biofuels has uncovered serious technical limitations of the currently used production systems. As a consequence, a growing controversy about the real sustainability and environmental friendliness of the actual biofuels industry has been generated (Fortman et al., 2008; Abdullah et al., 2009; Demirbaş, 2009; Yee et al., 2009; Jaruwat et al., 2010).
In addition, the consequences of biofuel production for farming practices or food markets, as well as real greenhouse gases (GHG) emission reduction along the biofuel life cycle, represent an important issue that, frequently, is not clearly treated. Parameters such as the kind of biofuel under study, feedstock, and energy inputs needed to maintain the process of transformation need to be taken into account. Also, the possibility of cogeneration of electricity or the exchange of energy between the biofuel synthesis and the feedstock transformation processes must be added to the model. Thus, wide variations in the net energy gain and consumption of resources can occur owing to the different assumptions made to calculate the overall benefits and drawbacks. Timilsina and collaborators draw a general picture of this issue over the OECD estimations. According to these authors, the most efficient biofuel production scheme is represented by sugarcane-based bioethanol in Brazil, with a 90% GHG reduction with respect to the gasoline equivalent. This high efficiency relies mainly on the high yield of this crop and the usage of sugarcane as an energy source for production plants and the cogeneration of electricity. Second-generation biofuels based on cellulosic feedstocks present a 70–90% GHG reduction relative to gasoline or diesel. Combined with electricity cogeneration, this kind of biofuel could have an even greater effect on GHG reduction, but they are still under development. Ethanol from sugar beet GHG reduction ranges from 40 to 60%, while wheat-based ethanol presents a 30–50% GHG reduction. The corn-based production of bioethanol is the least GHG-reducing biofuel and presents a low efficiency at GHG reductions varying from 0 (even negative in some cases) to 50% compared to gasoline (OECD, 2008; Timilsina & Shrestha, 2010).
Theoretically, biofuel implantation in transport and industry should solve, or at least improve, the ecological and economic problems derived from the unsustainability of the fossil fuel-based energy model.
However, recent field experiences indicate a much more complex scenario. The market economy and unbalanced relations between different sectors of the economy and national markets generate unpredictable dynamics of fuels’ raw material prices. In this context, the development of subsequent new commercial and industrial opportunities has altered the already unstable behaviour of the agricultural international markets. The sudden peak in demand for grain, owing to its usage as a raw material for the production of ethanol, has abruptly increased the prices of corn (Fischer et al., 2009). The demand pressure has operated similarly in the palm oil market, generating a palm oil tree and soy culture surface expansion in several regions, with spectacular dimensions in South-East Asia (Abdullah et al., 2009; Jaruwat et al., 2010), where the biofuels fever threatens biodiversity and has a deep social impact because of the proliferation of unregulated, intensive, agricultural practices and the switching of oil usage for traditional human nutrition, housekeeping and livestock feed (Fortman et al., 2008; Guerrero-Compeán, 2008; Demirbaş, 2009; UNCTAD, 2010; Yee et al., 2009).
Biodiesel usually costs over 0.5 US$/l, compared to 0.35 US$/l for petroleum-based diesel (Demirbaş et al., 2009). It is reported that the high cost of biodiesel is mainly due to the cost of virgin vegetable oil (Krawczyk, 1996; Connemann & Fischer, 1998). For example, the soybean oil price is currently 1.27 $/l while the palm oil price is 1.18 $/l (World-Bank, 2011). Biodiesel from animal fat is currently the cheapest option (0.4–0.5 US$/l), while the traditional transesterification of vegetable oil is, at present, around 0.6–0.8 US$/l (Bender, 1999). Zhang et al. (2007) stated that there is no global market for ethanol. Within the reasons for this, crop types, agricultural practices, land labour costs, production plant sizes, processing technologies and government policies can be cited. The cost of ethanol production in a dry mill plant currently totals 0.44 US$/l. Corn represents 66% of operating costs while energy (electricity and natural gas) to fuel the production plant represents nearly 20% of operating costs. Nevertheless, ethanol from sugar cane, produced mainly in developing countries with warm climates, is generally much cheaper to produce than ethanol from grain or sugar beet (Bender, 1999). For this reason, in countries like Brazil and India, sugar cane-based ethanol is becoming an increasingly cost-effective alternative to petroleum fuels. On the other hand, ethanol derived from cellulosic feedstock using enzymatic hydrolysis requires much greater processing than from starch or sugar-based feedstock, but feedstock costs for grasses and trees are generally lower than for grain and sugar crops. If targeted reductions in conversion costs are achieved, the total cost of producing cellulosic ethanol in EOCD countries could fall below that of grain ethanol.
Estimates show that ethanol in the EU becomes competitive when the oil price reaches 70 US$/barrel, while in the USA it becomes competitive at 50–60 US$/barrel. For Brazil and other efficient sugar producing countries such as Pakistan, Swaziland and Zimbabwe, the competitive ethanol price is much cheaper, between 25–30 US$/barrel. However, anhidrous ethanol, blendable with gasoline, is still more expensive, although prices in India have declined and are approaching the price of gasoline. Although the feedstock costs represent the majority of biofuels’ cost, the production plant size can reduce the final cost of the fuel. Thus, the generally larger USA conversion plants produce biofuels, particularly ethanol, at lower cost than plants in Europe. Production costs are much lower in countries with a warm climate such as Brazil, with less than half the costs of Europe. But, in spite of the reduced costs of production, ethanol from Brazil is competitive with gasoline owing to the huge sugar cane production and the cogeneration of electricity (Demirbaş et al., 2009).
Since the Arab oil embargo of the 1970s, Brazil has made an incomparable effort in the reduction of its energy dependency by intensifying and extending sugar cane-based bioethanol production. Although the alternative periods of scarcity and abundance of oil have marked fluctuations in the strength of the Brazilian Alcohol National Programme (Proalcool), the global trend has been an ascending progression in the total production of alcohol, as well as in the yield per hectare of sugar cane, and the implantation of this alcohol as transportation fuel. Today, Brazil is the second largest worldwide ethanol producer. In this way, Brazil has reduced its energy dependency, and has become the first ethanol exporter. According to Brazilian Government data, this milestone has been achieved on the basis of rural employment and welfare improvement. The key aspects of the Proalcool programme are a combination of technological advances, social planification and projection of the bioethanol industry. According to the Brazilian Government (Da Costa et al., 2010), owing to the high productivity of sugar cane, Brazil has expanded ethanol production and use without a significant increment in the fertile land surface used to cultivate sugar cane, or a food vs. fuel competition. However, there are several authors who are not so enthusiastic with the success of the Brazilian model, and point to the sugar cane industry as one of the reasons for the losses in biodiversity and the expansion of agricultural land over doubtfully catalogued marginal land, which is more relevant and dangerous than the Brazilian Government data indicates (Coelho et al., 2008; Gauder et al., 2011).
On the other hand, the American bioethanol industry choice of corn grain as its raw material has been followed by a dramatic rise in the prices of corn derivatives. Although the USA production of bioethanol supersedes the Brazilian one, the production:consumption ratio of the former (1:3) is much smaller than the latter (8:3). Despite its commercial orientation, the global efficiency of the USA model is low compared with the Brazil system and relies on the high importation taxes that protect the American industry from foreign ethanol inputs (Da Costa et al., 2010). Finally, the narrow margin of the USA production:consumption ratio suggests that the model has reached a production glass ceiling that blockades the medium-term implantation of biofuels in American society and hampers their exportation (UNCTAD, 2010; Da Costa et al., 2010).
The European and Asian strategy to improve climate change and fossil fuel depletion problems is based mainly on the chemically catalyzed biodiesel obtained from vegetable oils. There is a variety of feedstocks for the production of this biofuel, from inedible oils, (mainly rapeseed oil in Europe or jatropha oil in Asia), to edible oils (principally sunflower oil in Europe and palm oil or soybean oil in Asia, although corn, peanut, cotton seed or canola oil can also be cited) (Ranganathan et al., 2008; Abdullah et al., 2009). As the elected method for industrial biodiesel production is chemical catalysis, these vegetable oils are preferred to other heterogeneous lipids sources. These other lipids need pretreatment prior to their use (Peterson, 1986; Fortman et al., 2008), and include waste frying oils, waste-activated bleaching earth from the oil refinery industry, and even animal origin lipids such as beef tallow, lard, yellow grease and poultry grease or fat from fat traps, septic tanks, or waste water sludges. The need for economically viable vegetable oils for biodiesel production implies the cultivation of greater areas with oil-producing crops such as sunflowers or palm oil trees. Thus, the previously mentioned rising corn prices, owing to the derivation of huge amounts of grain for the industrial production of bioethanol, is neither an isolated case in developing biofuel industries nor the only aspect of the biofuel industry issue. Like the bioethanol industry, the European and Asian biodiesel industries have the energy and chemical problems associated with the current biofuels model. These limitations can be summarized according to nearly obsolete technology, being strongly dependent on chemical catalysis, non-renewable materials and promotion of non-sustainable market and farming practices (Guerrero-Compeán, 2008; Demirbaş, 2009; UNCTAD, 2010).
The industrial production of biodiesel needs to solve several technical problems in order to obtain this kind of biofuel in an efficient and sustainable way. The physical factors to consider can be summarized by pH, temperature, hydric activity, solvents and supports. Depending on the catalyst used to drive the transesterification reaction, some of the cited factors have different impacts on the global efficiency and feasibility of the process. A non-optimal configuration of the system can reduce significantly the biodiesel yield and compromise the viability of the production plant, especially if the upstream by-products, excess catalyst or auxiliary devices for solvent recovery hinder an easy, clean and rapid downstream processing of the biofuel.
As mentioned above, the chemical catalysis of the transesterification reaction requires high temperatures to achieve an acceptable reaction rate. In the case of the alkaline catalysis, the minimal temperature to produce conventional biodiesel is 60ºC, while in the acid catalysis the temperature ranges from 50 to 80ºC (Robles-Medina et al., 2009). Acid catalysis is slower than the alkaline one and generates a more corrosive fuel, so alkaline catalysts are preferred by the industry. It incurs a great energy cost in order to initiate and maintain the reaction (Kawahara & Ono, 1979; Aksoy et al., 1988; Cao et al., 2008). However, the utilization of sodium hydroxide as a catalyst has a serious limitation in the form of saponification of free fatty acids if water is present. This drives the increased consumption of the catalyst and downstream processing problems, such as the separation of glycerol and unreacted precursors. The solutions to manage this problem include using only virgin oils, often edible vegetable oils, instead of oils with high free fatty acids and water content, such as waste cooking oils or animal origin fats, as well as other residual fats. Higher temperatures, up to 120ºC, and the addition of organic solvents, or additional steps for free fatty acids esterification with sulphuric acid before performing the alkali-catalyzed transesterification are quite common as well (Jeromin et al., 1987).
When lipases are used as catalysts, it is possible to get over the saponification problems owing to their ability to transesterificate alcohols with both triacylglycerols and free fatty acids. Besides, lipases work as well in the presence of water. In fact, they need a certain hydric activity to maintain their tridimensional structure, so the presence of water is not a problem with this kind of catalyst — although excessive hydric activity affects the transesterification reaction because the substrates are water insoluble (Jaeger & Eggert, 2002; Shah et al., 2004; Gilham & Lehner, 2005; Fjerbaek et al., 2009). Lipases can operate at low or relatively low temperatures in the range of 20 to 70ºC, and at even lower temperatures if the enzyme has been obtained from psycrophilic microorganisms (Dabkowska & Szewczyk, 2009). Depending on the chosen lipase and preparation (free, immobilized or whole cell catalyst), lower temperatures (below 65ºC) can be applied to avoid the thermal denaturation of the enzyme, thus saving in production costs (Fukuda et al., 2008). Within the thermostable lipases, we can cite Burkholderia cepacia lipase (Amano PS lipase, from Amano Pharmaceutical Co., Japan), that reaches its highest activity at 60ºC (Dabkowska & Szewczyk, 2009), and the lipases obtained from Thermoanaerobacter thermohydrosulfuricus SOL1 and Caldanaerobacter subterraneous subsp. tengcongensis, which show their activity maximum at 75ºC and tolerate temperatures as high as 95ºC (Royter et al., 2009).
On the other side of the spectrum, the lipase from Bacillus sphaericus MTCC 7526 presents its optimal temperature at 15ºC, keeping stable until 30ºC, and the Microbacterium phyllosphaerae lipase presents the optimal temperature at 20ºC and deactivates when the temperature exceeds 35ºC, with the pH value fixed at 8 for both psycrophilic enzymes (Joseph et al., 2006; Srinivas et al., 2009). Therefore, pH plays an important role in the enzymatic production of biodiesel because it influences both the reaction rate and the thermal stability or solvents’ susceptibility of the lipases. An adequate pH can facilitate the optimization of the operation temperature and improve the activity of the enzyme. Gutarra and collaborators reported a high stability of the Penicillium simplicissimum lipase in the pH range 4.0–6.0, that showed the maximal activity at 50ºC and remained stable and active (although with a lower activity) even at 70ºC (Gutarra et al., 2009).
An alternative to the chemical transesterification of low quality oils with a relatively high concentration of water or free fatty acids consists of heterogeneous catalysis using acidic cation-exchange resins, supported metals (Zabeti et al., 2009), basic oxides or zeolites (Knezevic et al., 1998; Suppes et al., 2004). Even low cost alternatives such as waste eggshell have been proposed as well (Wei et al., 2009). These kind of catalysts are considered as an intermediate and relatively low-cost solution between the traditional homogeneous catalysts and the lipases. However, the cited heterogeneous catalysts are affected by the slow diffusion of the triglycerydes through their pores and require a higher alcohol:oil ratio to accelerate the reaction, in order to increase the production (Zabeti et al., 2009). Nevertheless, the heterogeneous catalysts can serve to improve the reusability and efficiency of immobilized enzymes and whole cell catalysts. Immobilization of enzymes on inert materials such as porous ceramic beads (Iso et al., 2001) or polymeric resins (Dizge et al., 2008; Dizge et al., 2009) can improve their performance. This improvement is owing to the protection that the pores’ microenvironment brings to the enzyme, avoiding the inhibition or damage of the enzyme caused by methanol or solvents. Another attractive approach to the immobilization is the so-called protein-coated microcrystals technology (PCMC). PCMC is based on the use of crystalized proteins as a support to the lipases, or in the direct use of crystalized lipases as solid catalysts (Raita et al., 2010). However, the real increase in reaction rate and enzyme stability with these immobilization techniques is usually lower than the theoretically expected. One of the reasons for these lower rate issues responds to the blockage of the pores of the used material as support because of the precipitation of glycerol or the insufficient circulation of substrates around the enzyme (Zabeti et al., 2009). The knowledge generated by the intense research on production and use of supports, resins and porous metallic alloys can be useful for enzymatic production of biodiesel. With this comparative approach, the optimization of the immobilized enzyme technology could be a reality in the short rather than medium term.
Depending on the kind of catalyst used and the selected operation conditions in the biodiesel production plant, the alcohol to oil molar ratio will present a wide variation. Adding excess alcohol is a common practice, and could serve as reference. However, excess alcohol use implies higher reactant associated costs, especially when the alcohol of choice is ethanol, which is more expensive than methanol. Thus, a more detailed approach to the system optimization in terms of minimal alcohol consumption is needed. Besides, a fine adjustment of the alcohol to oil ratio allows the maximal biodiesel production in the shortest possible time span and with the lowest energy input (Shieh et al., 2003).
The optimization is a relatively simple task when homogeneous catalysts such as sulphuric acid or sodium hydroxide are used to perform the conventional transesterification of vegetable oils with methanol. High yields are achieved with a methanol to oil ratio of 1:1 with an alkaline catalyst (although to improve the yield this proportion rises to 6:1) and a 30:1 ratio when an acid catalyst is used (Zhang et al., 2003).
However, in the case of lipase-catalyzed biodiesel, the situation is more complex and the molar ratio of alcohol to oil varies depending on the type of lipase, the use of an immobilized or free enzyme, and the alcohol used. Similar to the chemical catalysts, an increase of the molar alcohol:oil ratio elevates the efficiency of the reaction, but an excessive alcohol content inhibits and even damages the enzyme, especially when using methanol and free enzymes. Although the lipase-based solvent-free systems are under intensive research, owing to advantages such as the direct saving in solvents and the indirect cost reductions in downstream processes, the utilization of lipases does not necessary mean abandoning the use of a certain amount of solvents. The addition of solvents like t-butanol, diesel oil, hexane or dioxane to the precursors of biodiesel usually allows a better mixing of the reactants. Thus, solvents relieve the problems associated with the different water solubility of lipids and alcohols. In addition, solvents provide a more durable interaction between the enzyme and its substrates, and can favour the circulation of reactants through resins and support pores in immobilized enzyme systems. This improved circulation confers some protection to the lipases against inhibition by substrates and damages by excessive alcohols. However, solvents’ addition has to be carefully studied, since an excess of solvent or an inadequate amount of solvent can affect the enzyme activity and stability. For example, Shieh et al. studied the optimal operation conditions to transesterificate soybean oil with methanol by Rhizomucor miehei lipase immobilized on macroporous weak anionic resin beads. They found that the best transesterification rate was obtained when the methanol:oil molar proportion was 3.4:1 at 36.5ºC (Shieh et al., 2003). Raita et al. studied the transesterification of palm oil with ethanol by Thermomyces lanuginosa lipase-coated microcrystals in the presence of t-butanol. In this case, the optimal conditions were ethanol to fatty acids 4:1 molar ratio and t-butanol:tryacylclycerides 1:1 molar ratio, at 45ºC (Raita et al., 2010. However, Tongboriboon et al. worked on the solvent-free transesterification of used palm oil with Thermomyces lanuginosa and Candida antarctica lipases immobilized in porous polypropylene powder, reporting that the best yield was achieved at an ethanol to oil ratio of 3:1, and the yield decreased when the molar ratio was increased to 4:1 at 45ºC (Tongboriboon et al., 2010). These authors pointed to the inhibition of the enzymes by an excessive amount of ethanol, although it is worth emphasizing that they worked on a solvent-free system, so the enzyme was relatively vulnerable to alcohol-driven damage. On the other hand, Shah et al used 4:1 ethanol to oil molar ratio as standard reaction settings in their study about the transesterification of jatropha oil with ethanol at 40ºC. The experimental design consisted of a solvent-free system and three different lipases (free and immobilized on Celite), namely Chromobacterium viscosum, Candida rugosa and Porcine pancreas lipases, although they did not try different alcohol to oil molar ratios (Shah et al., 2004).
As a response to the problems associated with the recent worldwide implantation of second-generation biofuels, some authors propose focusing on the processes involved in the production of such biofuels. This new approach consists of the utilization of microbial enzymes to achieve the current chemical pretreatment steps of cellulosic or starchy raw materials (Carere et al., 2008). Microorganisms deal with the degradation of lignocellulose, hemicellulose or lipid-rich materials by means of enzyme catalyzed processes at near to room temperature. Therefore, microbial enzymes could be used to make the current biofuels industry cleaner and greener. Furthermore, the production of biofuels would be coupled with the management of woody and oily wastes, converting these residues into suitable and cheap raw materials (Steen et al., 2010).
Another promising lipids source, still not implemented but currently being studied worldwide, is represented by microalgae. Microalgae have a high potential as biodiesel precursors because many of them are very rich in oils, sometimes with oil contents over 80% of their dry weight, although not all species are suitable as biodiesel production oils (Chisti, 2008; Manzanera, 2011). Besides, these microorganisms are able to double their biomass in less than 24 hours, achieving a reduction between 49 and 132 fold in the medium culture time required by a rapeseed or soybean field. Furthermore, microalgae cultures require low maintenance and can grow in wastewaters, non-potable water or water unsuitable for agriculture, as well as in seawater (Mata et al., 2010). The production of microalgae biodiesel could be combined with the CO2 removal from power generation facilities (Benemann, 1997), the treatment of waste water from which microalgae would remove NH4+, NO3- and PO43- (Aslan & Kapdan, 2006), or the synthesis of several valuable products, from bioethanol or biohydrogen to organic chemicals and food supplements (Banerjee et al., 2002; Chisti, 2007; Rupprecht, 2009; Harun et al., 2010). However, microalgae biomass-based biofuels have several problems ranging from the optimization of high density and large surface units of production to the location of the microalgae production unit. Anyway, the main decisions to take are the adoption of open or closed systems, and the election of batch or continuous operation mode. As will be discussed below, depending on the system and mode of operation choice, there will be different advantages and drawbacks.
Microalgae can be cultivated in open-culture systems such as lakes or (raceway) ponds, and in closed-culture systems called photobioreactors (PBRs). Open-culture systems are normally cheaper to build and operate, more durable and have a higher production capacity than PBRs. However, open systems are more energy expensive in terms of nutrient distribution owing to mass transfer problems, and have their depth limited to 15 cm, to ensure that the microalgae receive enough light to grow. Moreover, ponds are more sensitive to weather changes, and temperature, evaporation and light intensity controls are not feasible. Furthermore, these open systems require more land area than PBRs, and are more susceptible to contamination, both from bacteria and from microalgae present in the surroundings of culture installations (Manzanera, 2011).
In contrast, PBRs are more flexible and are intensive land-usage systems that can be configured according to the specific physical-chemical requirements of the algae of choice, allowing the cultivation of species unsuited to open ponds. Nutrient homogenization, light distribution, pH, temperature, CO2 and O2 control can be achieved in photobioreactors. Thus, closed systems provide more stable and appropriate growing conditions, allowing higher cell densities and minimizing contamination. Nevertheless, PBRs have several technical problems that make them non-competitive in applications that can be achieved in raceway ponds. Such problems are overheating, bio-fouling, shearing stress, oxygen accumulation, scaling-up difficulties and the high costs of building, operation and maintenance (Chen et al., 2011).
Within these problems, it is worth highlighting capital building investment and high operation costs. PBRs biomass production costs may be one order of magnitude higher than in open systems. If the biomass added value is high, PBRs can be competitive. Otherwise, open ponds will be the preferred option. However, the evaluation of performance of open and closed systems is complex and depends on several factors, such as algal species or productivity computation method. Three parameters are commonly used to evaluate productivity in microalgae cultivation installations. Firstly, volumetric productivity (VP), that is, productivity per unit of reactor volume (g/l d). The second parameter is area productivity (AP), defined as productivity per unit of ground area occupied by the reactor (g/m2 d). The third one is illuminated surface productivity (ISP), namely the productivity per unit of reactor illuminated surface area (g/m2 d). Nevertheless, the election of closed or open systems relies on more aspects apart from productivity, as will be discussed below (Richmond, 2010).
PBRs can be operated in batch or continuous mode. There are several advantages when using them in continuous mode. Firstly, continuous culture provides a higher control than batch mode. Secondly, growth rates can be regulated and keep in a steady state for long periods, and the biomass concentration can be modulated by dilution rate control. In addition, results are more reliable and reproducible owing to the steady state of continuous reactors, and the system yields better quality production (Molina et al., 2001).
However, there are limitations that can make the continuous process unsuitable for some cases. One of these limitations is the difficulty in controlling the production of some non-growth-related products. For instance, the system often requires feed-batch culturing and continuous nutrient supply that can lead to wash-out. Filamentous organisms can be difficult to grow in continuous PBRs because of the viscosity and heterogeneity of the culture medium. Another problem is that the original strain can be lost if it is displaced by a faster-growing contaminant. The contamination risk and loss of reliability of the bioreactor becomes more relevant when long incubation periods are needed, so the potential initial investment in necessary better quality equipment could rise and hamper the economic viability of the production unit (Mata et al., 2010).
The possible coproduction of high value chemicals could lead to the solution of the above problems, but it implies taking multiple parameters and options into consideration. The microalgae production units will suffer drastic changes, both in the operational aspect (temperature, insolation, wind, microalgal and bacterial or fungical contaminations etc.) and in the commercial one (oscillations in value of by-products, improvements in centrifugation or extraction strategies or development of non-algal biofuels, etc). Taking into consideration all the above mentioned parameters, it can be ascertained that any microalgae-based biodiesel project is unique. Hence, such projects must be designed by thinking in terms of a flexible or even multipurpose and adaptable installation (Richmond, 2010).
Microalgae are not the only option to produce biofuels from oily biomass. Multiple prokaryotes and eukaryotes can accumulate high amounts of lipids. But, as occurred with microalgae, not all species are suitable for biodiesel production owing to differences in the kind of storage lipids. Thus, as stated by Waltermann & Steinbüchel (2010), many prokaryotes synthesize polymeric compounds such as poly(3-hydroxybutyrate) (PHB) or other polyhydroxyalkanoates (PHAs), whereas only a few genera show accumulation of triacylglycerols (TAGs) and wax esters (WEs) in the form of intracellular lipid bodies. On the other hand, storage TAGs are often found in eukaryotes, while PHAs are absent, and WE accumulation has only been reported in jojoba (Simmondsia chinensis). All these lipids are energy and carbon storage compounds that ensure the metabolism viability during starvation periods. Similar to the formation of PHAs, TAGs and WE, synthesis is promoted by cellular stress and during imbalanced growth; for instance, by nitrogen scarcity alongside the abundance of a carbon source (Kalscheuer et al., 2004).
The most interesting prokaryote genera in terms of accumulation of TAGs are nocardioforms such as Mycobacterium sp., Nocardia sp., Rhodococcus sp., Micromonospora sp., Dietzia sp., and Gordonia sp, alongside streptomycetes, which accumulate TAGs in the cells and the mycelia. TAGs storage is also frequently shown by members of the gram-negative genus Acinetobacter (although, in this case, WE are the dominant inclusion bodies components) (Waltermann & Steinbüchel, 2010). Within eukaryotes, with the exception of algae, yeasts of the genera Candida (non albicans) (Amaretti et al., 2010), Saccharomyces (Kalscheuer et al., 2004; Waltermann & Steinbüchel, 2010) and Rhodotorula (Cheirsilp et al., 2011) are the most interesting ones to produce biodiesel feedstocks.
Steinbüchel and collaborators have worked on the heterologous expression of the non specific acyl transferase WS/DGAT from Acinetobacter calcoaceticus ADP1 in Saccharomyces cerevisiae H1246 (a mutant strain unable of accumulating TAGs) (Kalscheuer et al., 2004). These authors found that the yeast recovered the ability to accumulate TAGs, as well as fatty acid ethyl esters and fatty isoamyl esters. This finding showed that the Acinetobacter calcoaceticus transferase had a high potential for biotechnological production of a large variety of lipids, either in prokaryotic and eukaryotic hosts. From this basis, as will be discussed in detail in Section 4.3, they worked on Escherichia coli TOP 10 (Invitrogen) and obtained an engineered strain able to produce fatty acid ethyl esters (biodiesel) directly from oleic acid and glucose (Kalscheuer et al., 2006).
Another possibility is combining the biomass obtained from microalgae and yeast, as recently proposed by Cheirsilp et al. (2011). These authors studied a mixed culture of oleaginous yeast Rhodotorula glutinis and microalga Chlorella vulgaris in industrial wastes. The used effluents, including both a seafood processing wastewater and molasses from a sugar cane plant. They found a synergistic effect in the mixed culture. R. glutinis grew faster and accumulated more lipids in the presence of C. vulgaris, that acted as an oxygen generator for yeast, while the microalgae obtained surplus CO2 from yeast. The optimal conditions for lipid production were 1:1 microalga to yeast ratio initial pH of 5.0, molasses concentration at 1%, 200 rpm shaking, and light intensity at 5.0 klux under 16:8 hours light and dark cycles (Cheirsilp et al., 2011).
Pure or immobilized enzymes obtained from microorganisms could reduce the energy costs of industrial ethanol and biodiesel production. Nevertheless, the cellulases used to treat (ligno)cellulosic materials such as forestry residues, waste paper or straw are difficult to purify, like the lipases used for the transesterification of lipids yielding biodiesel. Hence, their price is still too high to make their usage economically viable (Shieh et al., 2003; Ranganathan et al., 2008). Another limiting factor for the use of enzymes is the inactivation and inhibition by reactants and substrates. These drawbacks are the object of an intensive effort to make possible the reutilization of enzymes through protein engineering (Ebrahimpour et al., 2008), in order to increase their stability and activity. Research interest is also targeted on immobilization in different supports or the usage of genetically engineered microorganisms, called whole cell catalysts, which carry the necessary enzymes, avoiding their exposure to inhibiting substrates and operating as microrefineries (Kalscheuer et al., 2006). In the case of biodiesel microbiological production that will be revealed in detail below, the authors proposing and developing this technology refer to this third-generation biofuel as ‘Microdiesel’. The microbial production of biodiesel requires the construction of genetically modified microorganisms, able to transesterificate ethanol with lipids and, if possible, able to produce it by themselves to optimize the whole process. Since their 2006 work on microdiesel production on the laboratory scale using an engineered Escherichia coli strain, Steinbüchel and collaborators have established the guidelines of microdiesel industry development. Their approach consisted of expressing heterologously in E. coli the genes from Zymomonas mobilis, encoding for piruvate decarboxylase (pdc) and alcohol dehydrogenase (adhB), as well as the Acinetobacter baylyi non specific acyl transferase ADP1 (atfA). The obtained strain was able to carry out the aerobic ethanol fermentation from sugars, as well as the enzymatic transesterification of this alcohol with the fatty acids derived from the lipidic metabolism, yielding FAEE, referred to as ‘microdiesel’ by the authors (Kalscheuer et al., 2006). Recently, Elbahloul and Steinbüchel have used the aforementioned microdiesel producing E. coli at a pilot plant scale, using glycerol and sodium oleate as carbon and fatty acids sources respectively, with promising results (Elbahloul & Steinbüchel, 2010). Nevertheless, their conclusions for both studies indicate that there is still a long way to go to the industrial application of their findings, and that the technique needs to be modified to make the engineered strains adaptable to different lipids rich sources and to lignocellulosic raw materials. These modifications would allow the usage of forestry and agricultural wastes, making the biodiesel production process at least as versatile as chemical transesterification.
Vegetable oils are expensive and require large areas of farmland for their production, so the direct usage of these oils for biodiesel production is expensive and unsustainable. However, there are multiple and as yet unexploited alternative fatty acid sources. Similarly, bioethanol production for its direct use as a biofuel or as a biodiesel precursor requires huge amounts of corn grain or sugar cane. Nevertheless, industrial residues such as the vegetable oil refinery waste, as well as farming, forestry, livestock and domestic solid and liquid waste (Chen et al., 2009; Dizge et al., 2009) are widespread and huge sources of lipids and carbon. Wang et al. proposed the soybean oil deodorizer distillate (SODD), a by-product from the soybean oil refineries that represents 0.3–0.5% of the soybean oil processed, to produce biodiesel. With 45–55% of triglycerides and 25–35% of free fatty acids, these authors estimated that around 80% of the SODD can be transformed into biodiesel in a transesterification with methanol by the Thermomyces lanuginosa and Candida antarctica lipases in the presence of tertbutanol and 3Å molecular sieve (Wang et al., 2006). Park et al. used waste-activated bleaching earth (ABE), a residue of the rapeseed or palm oil refinery industry that stores 35–40% of oil and can be used to synthesize multiple bulk chemicals, including biodiesel. As in the Wang example, these authors chose methanol as alcohol, but their solvent choice was fuel oil and kerosene, the catalyst was Candida cylindracea lipase and the obtained FAME was extracted with a filter press (Park et al., 2008). Al-Zuhair and colleagues studied the production of biodiesel from simulated waste cooking oil (SWCO) with free- and immobilized- on ceramic beads Candida antarctica and Burkholderia cepacia lipases, with or without organic solvent. They obtained the best yield when they used B. cepacia without organic solvent, and observed that the system worked better when the enzymes were immobilized, probably because the clay structural microenvironments offered the lipases protection against the methanol derived denaturation (Al-Zuhair et al., 2009). Recently, Steen et al., among others, have proposed the direct fermentation of cellulosic biomass to produce biodiesel, fatty alcohols, waxes and other valuable chemicals (Steen et al., 2010). Their approach combines the waste management and the guidelines defined by Steinbüchel et al. with the new trends in synthetic biology and consolidated bioprocesses. This multidisciplinary approach brings a new flexible, easy-to-modify toolbox, composed of genetically modified FAEE synthetic strains, harbouring the enzymatic apparatus needed to produce ethanol from raw (hemi)cellulosic materials, to transesterificate it with fatty acids, or to synthesize both the fatty acids and the ethanol directly from the cellulose (Steen et al., 2010).
The microdiesel concept initiated by Steinbüchel et al. can be combined with the management and reutilization of waste waters by the application of microbial lipases to transesterificate the lipids present in the dairy industry or urban wastewater sludges. The lipidic fraction of sludges from urban wastewater treatment represents between 17 and 30% of the dry weight. This lipidic fraction is formed by direct absorption of fats present in the water by the sludge particles and by the phospholipids released from the cell membranes of micro-organisms, as well as from metabolites and cell lysis by-products (Boocock et al., 1992; Shen & Zhang, 2003; Jardé et al., 2005).
Lipid-rich wastewaters require pretreatment in order to reduce the amount of lipids and ease the subsequent conventional treatment. The pretreatment is usually based on physical processes, the most common of which are fat traps, tilted plate separators (TPS), and dissolved air flotation (DAF) units. In addition, centrifuges and electroflotation systems are used occasionally (Willey, 2001). Fat traps are rectangular or circular vessels through which the wastewater passes under laminar-flow conditions, at a rate that allows the lipids to rise to the surface near to the outlet end of the trap. The separation principle is based on Stoke\'s law, relating rising velocity of a particle to its diameter, so the theoretical separation efficiency is dependent on depth. In practice, fat traps have a depth of 1.5 m, although if the accumulation of a bottom sludge is expected, then an additional 0.5 m would be added to the total liquid depth. Gravity flow is preferred to pumping when feeding the trap, in order to minimize the wastewater emulsification. Fat traps are used in the food industry and in restaurants (Willey, 2001).
Meanwhile, tilted plate separators were developed in the petrochemical industry and are based on the fact that surface area, rather than depth, determines the oil separation. The introduction of tilted plates into a vessel provides many parallel gravity separators with a high surface to volume ratio in a shallow tank. Typically, TPS can occupy less than 10% of the area needed to install a conventional fat trap, although they have some disadvantages. They are susceptible to fouling if solid or semi-solid fat is present in the effluent and a crane is required to remove the plate pack for cleaning. Besides, the pumping systems have to be carefully selected and controlled to avoid surging and liquid depth fluctuations (Zeevalkink & Brunsmann, 1983; Willey, 2001). Finally, dissolved air flotation units are based on the flotation of lipids by means of microbubble clouds (60-70 μm bubble diameter) created by the injection into water of 6 bar pressure air through nozzles. Microbubbles attach to the surface of the fat and oil particles, increasing their rise rate. These systems are used both in the food industry (Willey, 2001) and in the mining wastewater treatment (Tessele, 1998). Once the pre-treatment has finished, wastewater can receive further treatment prior to its disposal or biological treatment. Thus, chemical treatment may be used to reduce the total fatty matter in wastewater. Such treatment uses aluminium sulphate, ferric chloride, or more usually, lime, to break the emulsion and coagulate the fat particles. Subsequently, the fats can be separated by flotation or sedimentation. The rate of sedimentation can be improved by a second-stage flocculation, involving the addition of low levels of polyelectrolyte (0.5-5.0 mg/l) to the wastewater once coagulation has taken place (Willey, 2001).
The use of sludges to produce biofuels is not a new idea itself, but the available literature focuses mainly on the methane production by anaerobic fermentation, currently applied in the majority of waste water treatment plants (WWTP) to provide energy to these installations, or for fermentative biohydrogen production, which is still not industrially available (van Groenestijn et al., 2002; Wang et al., 2003). Several groups have studied the in situ transesterification of WWTP sludges, but have focused on the chemical catalysis of the transesterification with methanol (Haas & Foglia, 2003; Mondala et al., 2009). However this method still presents the same limiting factors that affect the chemical transesterification of edible vegetable oils (Freedman et al., 1984). In spite of their chemical approach, these works provide useful information about several aspects of the biodiesel production process, especially at the first stages of the process. Thus, one common problem of chemical and enzymatic biodiesel production is the need for the pretreatment of the feedstock to make its lipids easily available to the catalyst. In the case of wastewater treatment sludge, this pretreatment step usually implies the use of organic or non-polar solvents to release the lipids from the organic matter (Antczak et al., 2009; Siddiquee & Rohani, 2011).
The most extended protocols rely on chloroform:methanol mixtures, as used in the Folch\'s method (Folch, 1957), in which a 2:1 chloroform:methanol reactant is mixed with the sample, where water acts as ternary component to form an emulsion. After equilibration with a fourth volume in saline solution, the emulsion separates in two phases: the lower one containing chloroform:methanol:water in the proportions 86:14:1 alongside the lipids; and the upper one containing the same solvents in proportions 3:48:47 and carrying the non-lipidic components of the sample. Bligh and Dyer\'s method is a simplified variant of the former, but requires the re-extraction of the sample residue with chloroform (Bligh & Dyer, 1959). Nevertheless, there are some methods with near to Folch\'s reagent yielding which use less toxic reagents, such as pure hexane or different combinations of hexane and other solvents, such as the hexane-isopropanol (3:2) blend proposed by Hara and Radin (Hara & Radin, 1978), or the ethyl acetate-ethanol (2:1) mixture used by Lin et al. (Lin et al., 2004). For a detailed revision of the solvents based extraction protocols, see Kuksis, 1994; Murphy, 1994; Kates, 1996.
In spite of being slightly less toxic than chloroform, the cited solvents are hazardous and present enough management risks to consider other extraction strategies. Several authors propose solvent-free methods based on ionic liquids (Ha et al., 2007), boiling the sludge or subjecting it to supercritical gases, mainly t-butanol (Wang et al., 2006; Royon et al., 2007), propane (Rosa et al., 2008), syngas (Tirado-Acevedo et al., 2010) and CO2 (Helwani et al., 2009), or even to extreme pressures and temperatures (cracking) (Saka & Kusdiana, 2001). All of them are costly and not feasible with the current technology (Siddiquee et al., 2011). A more realistic and ready-to-use option is extraction using hot ethanol, which can be used to perform the lipids’ extraction without using coadyuvant solvents. This approach to extraction can be illustrated with the works developed by Holser and Akin (2008) or Nielsen and Shukla (2004), among others. Although these authors have focused on the ethanol-based extraction of high value lipids from flax processing wastewater and egg yolk powder, respectively, their findings could be scaled and applied to biodiesel production from wastewater sludges. Nielsen and Shukla found that the use of ethanol at room temperature led to the extraction of nearly all the phospholipids, together with cholesterol and a minor part of the triacylglycerols, without special extraction and filtration devices. On the other hand, Holser and Akin performed a serial extraction of the lipids present in flax wastewater in three steps, under different temperature values (50, 80, 90 and 100ºC). They found that the most efficient extraction was achieved when the sample-ethanol mixture was heated to 90ºC and the reaction time was 15 minutes (Holser & Akin, 2008).
Considering the above findings, and taking into account the fact that the enzymatic production of biodiesel generally requires high alcohol to oil ratios, to improve the solubilization of the lipids and the formation of water-oil, enzyme-oil and enzyme-alcohol-oil interfaces, we propose that a suitable scheme for the production of biodiesel from WWTP sludge could be as simple as using a pressurized pretreatment tank, where the sludge is soaked in ethanol, kept at 90ºC under stirring and refluxed to subject the mixture to three extraction cycles. This is followed by incubation in a reaction tank where the extracted lipids, alongside with part of the ethanol used in the previous step, are added to a reaction mix containing the enzyme (free, immobilized or whole cell catalyst) and kept at the optimal temperature and pH conditions, to ensure both enzyme stability and an acceptable microdiesel production rate. Heat exchangers between the two tanks could serve to save energy, using the heat released before entering the second tank to preheat the sludge before entering the first one.
The system could even be autonomous in terms of ethanol requirements if the engineered microorganism used to produce the lipase was able to produce ethanol simultaneously, or if the cited tanks were coupled with a third reactor where bioethanol was produced from sugars present in the non-lipidic products obtained in the pretreatment tank by means of ethanol-producing yeast or bacteria strains. In the case of economic restrictions, some short-term cost reduction could be achieved by replacing the pretreatment pressurized tank with a non-pressurized unit, and keeping the temperature of the extraction mix below 79ºC, although it would imply medium-term economic losses because the lower extraction efficiency must be compensated by performing more extraction cycles at a higher reflux rate and a greater ethanol volume in the pretreatment tank, or even by the use of at least two serial pretreatment tanks.
As a short-term response to the consequences of greenhouse gas emissions and the unsustainability of the fossil fuel-based energy model, the industry has developed ready-to-use substitutes for traditional fossil fuels, delivered generally and ambiguously under the commercial ‘bio’ denomination. However, the first- and second-generation of so-called biofuels are neither of completely biological origin nor based on renewable and environmentally friendly feedstocks. In addition, the production techniques rely on high energy inputs, both in feedstock production (as is the case for rapeseed, soybean or palm oil) and in the biofuel synthesis (acid catalyzed biodiesel or corn bioethanol perfectly illustrate the neat energy gain problems). Alongside these problems, new and complex problems have emerged. Firstly, the increase in the prices of grain and vegetable oils used both to produce biofuels and for human nourishment and livestock feeding; and secondly, the expansion of agricultural land to increase production of sugar cane or vegetable oils to satisfy the huge demand for these sugar and lipid sources, generated by the abrupt increase in biofuels production. Thus, the development of cleaner and more sustainable biofuels is required to achieve the challenge to totally replace traditional fossil fuels by third-generation biofuels, independent of non-renewable precursors or inefficient industrial processes, that damage the environment directly and indirectly and threaten biodiversity and food security (UNCTAD, 2010).
A great variety of domestic, agricultural and industrial residues, from lignocellulosic forestry and agriculture waste to fatty acid rich waste waters, generated by the dairy, poultry or vegetable oil refinery industries, as well as the sludges from urban waste waters, can be used as precursors of biofuels. The treatment of these residues could be combined with the production of third-generation biofuels by enzymatic catalysis because the high cost of enzymes could be compensated by the low cost of the residues (or even the presence of incentives for residue reduction and management). But the massive application of these concepts requires a series of technical and biotechnological improvements, such as the optimization of lipids and sugars extraction, feedstock pretreatment processes, biofuels production plant design, heterogeneous catalysts and enzyme immobilization techniques, protein engineering of lipases, alcohol dehydrogenases or hydrolases to increase their activity and reusability, genetic engineering of microbes to facilitate both the pretreatment of precursors, and the synthesis and purification of the biofuels.
We thank the Junta de Andalucía (Spain) for funding this study through project reference P08-RNM-04180 and the Spanish Ministry of Science and Technology for funding through project reference CTM2009-09270. M. Manzanera received grants from the Programa Ramon y Cajal, (Ministerio de Educacion y Ciencia MEC, Spain, and ERDF, European Union).
Extremophile organisms capable of growing in extreme conditions draw considerable attention since they show that life is robust and adaptable and help us understand its limits. In addition, they show a high biotechnological potential [1, 2]. Most of the best-characterized extreme environments on Earth are geophysical constraints (temperature, pressure, ionic strength, radiation, etc.) in which opportunistic microorganisms have developed various adaptation strategies. Deep-sea environments, hot springs and geysers, extreme acid waters, hypersaline environments, deserts, and permafrost or ice are some or the most recurrent examples of extreme environments [3]. However, the atmosphere is rarely thought of as an extreme habitat. In the atmosphere, the dynamics of chemical and biological interactions are very complex, and the organisms that survive in this environment must tolerate high levels of UV radiation, desiccation (wind drying), temperature (extremely low and high temperatures), and atmospheric chemistry (humidity, oxygen radicals, etc.) [4]. These factors turn the atmosphere (especially its higher layers) into one of the most extreme environments described to date and the airborne microorganisms into extremophiles or, at least, multiresistant ones [5].
\nIt is known that airborne cells can maintain viability during their atmospheric residence and can exist in the air as spores or as vegetative cells thanks to diverse molecular mechanisms of resistance and adaptation [2, 6]. The big question is whether some of them can be metabolically active and divide. Bacterial residence times can be several days, which facilitate transport over long distances. This fact, together with the extreme conditions of the atmosphere, has led researchers to think for years that they do not remain active during their dispersion. However, recent studies strongly suggest that atmospheric microbes are metabolically active and were aerosolized organic matter and water in clouds would provide the right environment for metabolic activity to take place. Thus, the role played by microorganisms in the air would not only be passive but could also influence the chemistry of the atmosphere. In any case, only a certain fraction of bacteria in the atmosphere would be metabolically active [2, 7].
\nDespite recognizing its ecological importance, the diversity of airborne microorganisms remains largely unknown as well as the factors influencing diversity levels. Recent studies on airborne microbial biodiversity have reported a diverse assemblage of bacteria and fungi [4, 8, 9, 10, 11, 12], including taxa also commonly found on leaf surfaces [13, 14] and in soil habitats [15]. The abundance and composition of airborne microbial communities are variable across time and space [11, 16, 17, 18, 19]. However, the atmospheric conditions responsible for driving the observed changes in microbial abundances have not been thoroughly established. One reason for these limitations in the knowledge of aerobiology is that until recently, microbiological methods based on culture have been the standard, and it is known that such methods capture only a small portion of the total microbial diversity [20]. In addition, because pure cultures of microorganisms contain a unique type of microbes, culture-based approaches miss the opportunity to study the interactions between different microbes and their environment.
\nAnother limitation for the study of aerial microbial ecology at higher altitudes or in open ocean areas is the difficulty of repeated and dedicated use of airborne platforms (i.e., aircraft or balloons) to sample the air. Most studies to date on the atmospheric microbiome are restricted to samples collected near the Earth’s surface (e.g., top of mountains or buildings). Aircraft, unmanned aerial systems (UASs), balloons or even rockets, and satellites could represent the future in aerobiology knowledge [5, 21, 22]. These platforms could open the door to conducting microbial studies in the stratosphere and troposphere at high altitudes and in open-air masses, where long-range atmospheric transport is more efficient, something that is still poorly characterized today. The main challenge in conducting these kinds of studies stems from the fact that microbial collection systems are not sufficiently developed. There is a need for improvement and implementation of suitable sampling systems for platforms capable of sampling large volumes of air for subsequent analyses using multiple techniques, as this would provide a wide range of applications in the atmospheric, environmental, and health sciences.
\nIn aerobiology, dust storms deserve special mention. Most of them originate in the world’s deserts and semideserts and play an integral role in the Earth system [23, 24]. They are the result of turbulent winds, including convective haboobs [25]. This dust reaches concentrations in excess of 6000 μg m−3 in severe events [26]. Dust and dust-associated bacteria, fungal spores, and pollen can be transported thousands of kilometers in the presence of dust [9].
\nIn this chapter, we approach the atmosphere as an extreme environment and make use of some advanced data from an example of an in situ study of the atmosphere: the analysis of bacterial diversity of the low troposphere of the Iberian Peninsula during an intrusion of Saharan dust using a C-212 aircraft adequately improved for aerobiological sampling.
\nIt is well known that there is a biota in the atmospheric air. The first study dates back to the nineteenth century, which speak about the presence and dispersion of microorganisms and spores in the atmosphere [27, 28]. Although the atmosphere represents a large part of the biosphere, the density of airborne microorganisms is very low. Estimates suggest that from the ground surface up to about 18 km above sea level (troposphere), there is less than a billionth of the number of cells found in the oceans, soils, and subsurface. Between approximately 18 and 50 km above sea level (stratosphere), temperature, oxygen, and humidity decrease and with them the number of cells. Above the ozone layer (between 18 and 35 km into stratosphere), ultraviolet (UV) and cosmic radiation become lethal factors. Once in the mesosphere (above 50 km), life is difficult to imagine; however microorganisms of terrestrial origin could arrive to the stratosphere from lower layers via different phenomena (human activity, thunderstorms, dust storms, or volcanic activity), and bacteria have been found isolated up to 41 km or in dust samples from the International Space Station (\nFigure 1\n) [6, 29]. Therefore, airborne microbes are always present in the atmosphere [11, 30, 31], and their permanence is dynamic, resulting in an environment with enormous variability. Estimates calculate that over 1021 cells are lifted into the atmosphere every year, leading to considerable transport and dispersal around the atmosphere, with a large portion of these cells returning to the surface due to different atmospheric events as part of a feedback cycle. Undoubtedly, airborne microbes play an important role in meteorological processes. They have been linked to the nucleation phenomena that lead to the formation of clouds, rain, and snow and to the alteration of precipitation events [32, 33, 34]. Their presence is essential to understand long-range dispersal of plant and potential pathogens [7, 35, 36] and maintain diversity in ground systems and could interfere with the productivity of natural ecosystems [17, 18]. On the other hand, airborne bacteria can have important effects on human health, being responsible for different phenomena such as seasonal allergies and respiratory diseases. Based on data from terrestrial environments, the global abundance of airborne bacteria has been estimated to range between 104 and 106 m−3 [37]. However, more recent studies incorporating direct counting by microscopy or quantitative PCR have provided more accurate estimates of the number of airborne microbes, which apparently point to a higher number of cells present in the atmosphere [38, 39, 40, 41].
\nDiagram displaying atmosphere layers, temperature and airborne emission sources. Yellow line marks atmospheric temperature. Bottom of the figures shows the common sources of aerosolized bacteria, with special attention to dust storms.
There is a great variety of airborne microorganism sampling systems, allowing us to select the most suitable one depending on our objectives [42]. On the other hand, no standardized protocols exist, which is a major pitfall when developing our objectives. This fact has led some authors to propose the creation of consortiums of interested parties for establishing standardized protocol reproducibility [20], as well as the need to establish global networks of aerobiological studies [11]. Two approaches are proposed: particles or cells can be collected passively or directly from the atmosphere. Passive media usually involves decanting [43] and collecting particles over snow [44] or through the collection of atmospheric water [45]. On the other hand, active methodologies entail three major approaches: filtration, impaction, and liquid impingement. All three approaches are very efficient when developing culture-dependent techniques. In contrast, culture-independent approaches produce some serious problems that make the work difficult: the high variability of the system and the low biomass mean that sampling campaigns are, in many cases, extremely inefficient [20]. Lastly, the use of airborne platforms is not very extended, but they represent a good opportunity to conduct a more direct study of the atmosphere [5, 19, 31].
\nFiltration is a simple and cheap method that is often efficient. It involves pumping air through a filter where the mineral and biological particles are trapped. Filters of different materials and porosity are available made of cellulose, nylon, polycarbonate or fiberglass, or quartz. Sizes used range from 0.2 to 8 μm, depending on the size of the particles to be captured and the capacity of the pump. In many cases, a PM10 filter can give better results when collecting smaller bacteria, as it allows greater airflow. Airflow filtration rates generally range between 300 and 1000 L/minute [4, 46]. Microorganisms trapped in the filter can be cultured, or the filters can be directly used for DNA extraction. In addition, filters are a very suitable support for microscopy, and countless holders for filters are available (an example is shown in \nFigure 2A\n).
\nThree different samplers of airborne microorganisms. (A) Filter holder and a filter (PALL Corporation). (B) Impinger sampling of bioaerosols (BioSampler, SKC, Inc.). (C) Six-stages Andersen Cascade Impactor (Thermo Fisher Scientific).
In impingement, particles are collected in a liquid matrix [20]. Normally a buffer is used such as phosphate buffer saline (PBS) that helps maintain the viability of the cells. One of the more widely used liquid impingers is BioSampler SKC (\nFigure 2B\n). In this case, the tangential movement of the particles inside the flow impinger retains the particles in the collecting liquid. The suspension obtained could be used for culturing or for molecular ecology assays [20]. One of the advantages of impingement collection is that it facilitates quantitative techniques such as flow cytometry or in situ hybridization [47].
\nIn this system, the particles generally impact into a petri dish with an enrichment medium. It is, possibly, the most efficient and most used method to conduct studies based on culture. Airflow impacting onto the plates is controlled by slots that allow the homogeneous distribution of the air. The system can be single stage or several stages in cascade, causing the particles to be distributed by size in the different petri dishes [20]. Some variants replace petri dishes with agarose filters or Vaseline strips, in order to carry out independent culture methodologies, but efficiency is very low. The original and more popular impactor is the Andersen cascade impactor (\nFigure 2C\n) [48].
\nSeveral studies explain and compare sampling methodologies in aerobiology, but most of them focus on the surface of the Earth (e.g., on top of mountains or buildings) or indoors [42, 49, 50, 51, 52, 53, 54]. However, small studies have been conducted at higher altitudes or in open sea areas. The use of airborne platforms (balloons, aircraft, rockets, etc.) for aerobiology sampling would allow conducting a direct study of the microbial ecology of the atmosphere. Another advantage of airborne platforms is the possibility of studying the vertical distribution of airborne microbial communities. In addition, some aircraft allow us to develop studies in the upper troposphere or in the stratosphere. Unfortunately, atmospheric microbial collection instruments have not been developed enough for airborne platforms.
\nAmong the different airborne platforms, aircraft, due to their versatility and access, are particularly interesting. Some studies have been conducted, but not enough samples have been developed yet, and efficiency is still very low. As already mentioned, the efficiency of samplers in soil-level aerobiology faces a series of problems (low biomass, high variability of populations, lack of standardized protocols). In the case of airplanes, in addition to these intrinsic problems associated with atmospheric microbial ecology, other additional ones exist: (1) the high velocity of the aircraft in relation to the relative quiescent air mass. This makes it difficult to obtain an isokinetic sampler and, therefore, one that is sufficiently efficient that would allow us to obtain a correct quantification of the incoming air [55]; (2) the sampler must be in a location on the airplane that avoids chemical contamination from the operation of the device. Previous studies have used wing-mounted air samplers or the roof of the aircraft to reduce the possibility of in-flight contamination [21, 22, 56, 57, 58]. Similarly, it should allow the aseptic collection of samples, avoiding microbiological contamination during the process. This operation, which can be very simple in the laboratory or at ground level, becomes tremendously complicated on an airplane, since air intakes that are part of the fuselage of the aircraft are often difficult to sterilize. It is therefore necessary to develop robust sterilization protocols. The spectacular work of DeLeon-Rodríguez of 2013 has been criticized in this aspect [40, 59]; (3) sampling time. A possible solution to the low biomass of the atmosphere is to increase sampling time, but in the case of flights, we are limited to the flight autonomy of the aircraft. Although scarce, some studies from airplanes have been conducted. The first studies that were conducted in airplanes were carried out by impaction on a petri plate with enrichment means, which allowed isolating microorganisms from the upper troposphere and even from the stratosphere [21, 57, 60]. However, advances in molecular ecology have caused the most recent studies to favor filtration [40, 58].
\nThe European Facility for Airborne Research (EUFAR) program brings together infrastructure operators of both instrumented research aircraft and remote sensing instruments with the scientific user community. However, it lacked aircraft prepared for microbiological sampling. The National Institute for Aerospace Technology (INTA) belonging to the Spanish Ministry of Defence has two CASA C-212-200 aircraft that were suitably modified to be used as flying research platforms. Now, these two aircraft are a unique tool for the study of atmospheric microbial diversity and the different environments of the EUFAR program. Our research group has a CASA-212 aircraft with an air intake located on the roof of the aircraft. A metal tube fits the entrance and is fitted inside the aircraft to a filter holder, a flowmeter, and a pump (\nFigure 3\n). This simple system is easy to sterilize, and both the metal tube and the filter holder can be replaced in flight by other sterile ones if we want to take different samples. Using PM10 fiberglass filters, we can obtain isokinetic conditions and pass 1800 L of air per hour through the filter, as indicated by the flowmeter.
\nAirborne microorganisms sampler installed in INTA’s CASA C-212-200 aircraft.
In a series of recent experiments, we tried to install a multi-sampler system in our aircraft, where we had five systems in parallel and connected to the same intake of the plane: one filter holder, two impingement systems, and two impactors (\nFigure 4\n). The results clearly showed that in the case of our aircraft, filtration was more efficient (data not shown).
\nMulti-sampler system tested in INTA’s CASA C-212-200 aircraft. (A) Impinger sampler, design and manufacture own. (B) Impactor sampler (Impaktor FH6, Markus Klotz GmbH). (C) Coriolis μ (Bertin Technologies SAS) a impinger biological air sampler. (D) Filter holder (PALL Corporation). (E) Six-stages Andersen Cascade Impactor (Thermo Fisher Scientific).
Aerobiology studies have traditionally focused on the collection of bacterial cells and the analysis of samples by total counting and culture-based techniques. It is known that such methods capture only a small portion of the total microbial diversity [61]. The almost exclusive use, for years, of these methodologies is one of the reasons for these limitations in the knowledge of aerobiology. In addition, culture-dependent methods do not allow us to study the interactions between different species of microorganisms. Culture-independent methods have been used to assess microbial diversity, increasing the specificity of microbial identification and the sensitivity of environmental studies, especially in extreme environments. These methods have recently been applied to various areas of airborne microbiology [62, 63, 64, 65] revealing a greater diversity of airborne microorganisms when compared to culture-dependent methods. Some good studies approach the challenges and opportunities of using molecular methodologies to address airborne microbiology [20, 66]. Although molecular ecology methods allow the rapid characterization of the diversity of complex ecosystems, the isolation of the different components is essential for the study of their phenotypic properties in order to evaluate their role in the system and their biotechnological potential. A combination of culture-dependent and culture-independent methods is ideal to address the complete study of the system.
\nModern culture-independent approaches to community analysis, for example, metagenomics and individual cell genomics, have the potential to provide a much deeper understanding of the atmospheric microbiome. However, molecular ecology techniques face several particular challenges in the case of the atmospheric microbiome: (1) very low biomass [20]; (2) inefficient sampling methods [20]; (3) lack of standard protocols [9, 20]; (4) the composition of airborne microbes continuously changes due to meteorological, spatial, and temporal patterns [7, 62, 67, 68, 69, 70]; and (5) avoidance of the presence of foreign DNA in the system [59]. Because these issues are not yet resolved, most of the non-culturing approaches focus on microbial diversity, where they are highly efficient.
\nThe most recurrent techniques are those based on DNA extraction, gene amplification of 16S/18S rRNA, and next-generation sequencing (NGS) technologies. Often, this approach is more efficient due to the greater efficiency and sensitivity of this process, as opposed to gene cloning and Sanger sequencing; thus some authors are inclined toward metagenomics instead of amplification. This provides more information and avoids an intermediate step, but bioinformatic processing is tedious and often only provides data in relation to diversity, making the annotation of the rest of the information very complicated [20]. These approaches can be complemented with quantitative methods such as qPCR, flow cytometry, or fluorescence in situ hybridization (FISH) [41, 47, 66, 71]. FISH is surely the best and most specific cell quantification methodology that exists. However, in the case of aerobiology, it cannot always be used. A minimum number of cells must exist so that we can observe and count them under a fluorescence microscope. Due to the variability of microbial populations in the air, this is not always achieved. In our research group, we have obtained very good results in this regard, optimizing cell concentration. \nFigure 5\n shows epifluorescence micrographs of bacteria from an air sample. On this occasion, sampling was performed using a biological air sampler (Coriolis μ, Bertin Technologies SAS), where biological particles are collected and concentrated in a liquid (PBS). Sampling was conducted for 2 hours at ground level, pumping a total of 36,000 L of air. After this time, the sample was paraformaldehyde fixed and filtered through a 0.2 μm pore size, hydrophilic polycarbonate membrane, 13 mm diameter (GTTP, Millipore). A half sample was hybridized with the universal Bacteria domain probe, EUB338I-III [72], following a conventional protocol [73]. The second half was hybridized with the probe NON338 [74] as negative control. In this case, an average of 140 cells per liter of air was counted. Occasionally, FISH also allows to observe bacteria attached to mineral particles (\nFigure 5C\n–\nD\n).
\nEpifluorescence micrographs of bacteria from an air sample. (A and C) DAPI-stained cells; (B and D) same fields a A, and C, respectively, showing cells hybridized with probes EUB338I-III (Cy3 labeled), specific for Bacteria domain. All micrographs correspond to the same hybridization process, performed with a sample obtained after 4 hours sampling at ground. C and D show microorganisms attaches to a mineral particles (arrow sign). Bars, 5 μm.
DNA gives us much information about the diversity of the system, but if we wish to obtain information about the metabolic activity that is taking place in the ecosystem, metabolomic and metatranscriptomic approaches are needed [50, 66]. In the case of the atmosphere, this is crucial, since we are not fully certain if the cells present are active. Some studies indicate that a part of the microorganisms in the atmosphere are developing an activity [6], but until we conduct RNA-based and metabolite-based studies, we will not have the certainty that this is the case. The big problem is that it is very difficult to carry out these studies using the current microbial capture systems.
\nScanning electron microscopy (SEM) also provides much information of the aerobiology [7]. Specifically, it allows the characterization of eukaryotic cells (e.g., diatoms) and, above all, pollens and fungal spores, from which we can obtain great information with good images alone. \nFigure 6A\n shows pine tree pollen observed via SEM in a sample obtained after a 30 minutes flight of the C-212 aircraft.
\nSEM images of different airborne samples. (A) Pinus pollen. Ground sample after 2 hours sampling. (B) Air sample collected from C-212-200 aircraft during a Saharan dust intrusion (February 24, 2017). Filter appear completely cover of mineral particles. (B and C) Biological particles sampled using C-212-200 aircraft. (E) Diatomea sampled by C-212-200 aircraft in a fligth along the northern coast of Spain (9 March 2017). (F) Cell attached to mineral particles and organic matter.
As mentioned above, factors, such as the shortage of nutrients and substrates, high UV radiation, drying, changes in temperature and pH, or the presence of reactive oxygen species, make the atmosphere an extreme environment. However, it is possible that the high variability of its conditions is the one characteristic that makes this environment more extreme [1, 20]. Among the cells present in the atmosphere, a considerable portion appears in the resistance forms capable of withstanding low-temperature and high-radiation conditions. This is what probably happens with fungi and gram-positive bacteria. Bacillus strains recurrently isolated from the atmosphere have characteristics and a capacity to sporulate very similar to strains isolated from the soil. Undoubtedly, another part of the cells will be in the form of latency and may even suffer modifications of the cell wall and slow down or stop their metabolic activity [75, 76]. These transformations can improve resistance to physical stresses, such as UV radiation [58]. On the other hand, some of the bacteria present in the atmosphere, such as Geodermatophilus, show pigmentation that undoubtedly protects it from excessive radiation. The microorganisms that are usually detected in the atmosphere originate mainly from the soil, which means they will share similar mechanisms of resistance. In some strains, metabolic adaptations have been observed to lack nutrients such as cytochrome bd biosynthesis to survive iron deprivation [77]. Deinococcus is also a recurrent genus in the atmosphere, which, like those in soil, has multiresistance mechanisms based on high DNA-repair efficiency. Bacteria that do not form spores and certain archaea, in contrast, often have genomes rich in G + C, which may increase tolerance to UV rays and overall survival [78].
\nAnother strategy of resistance could be cell clustering and adhesion to particles. Several studies have confirmed the loss of viability and shielding or the reflective properties of the mineral particles as an important role for the protection of UV radiation [19, 31]. In that sense, it is very possible that many cells have mechanisms that promote aggregation. In our samples, we often find the cells adhered to each other or to minerals, which undoubtedly makes them more resistant (\nFigure 6\n).
\nGlobal and regional models have been used to explain bioaerosol emission, transport, and atmospheric impact [17, 18, 79, 80, 81, 82, 83, 84]. Even so, it is not an easy phenomenon to explain, since it depends on a large number of factors. On the one hand, there are numerous sources of tropospheric aerosols, which include sea salt, volcanic dust, cosmic dust, industrial pollutants, and desert and semidesert areas [6, 85]. We must also consider the factors that make the transfer of particles possible, for example, meteorological phenomena, solar radiation, temperature, tides, erosion, etc. [85]. On the other hand, anthropogenic activities can also affect dust emissions indirectly, by changing the climate and the hydrological cycle. In these aerosols, microorganisms will be included in a greater or lesser number. The degree of richness in cells of tropospheric aerosols will depend largely on the source of emission. Thus, the large wooded masses or fields of crops provide the atmosphere with a good number of microorganisms due to the effect of air or the aerosols produced by rain. Similarly, anthropogenic activity contributes large amounts of bacteria to the environment, treatment plants, and composting areas being sources of airborne microorganisms [85].
\nDesert dust storms play a major role in particle emissions and with them that of microorganisms. In this way, most of the material reaching the atmosphere from the surface comes from desert and semidesert areas, which is known as desert dust. The Sahara-Sahel desert, the Middle East, central and eastern Asia, and Australia are the major sources of desert dust, although all the arid zones of the world are emission sources [9, 86]. Dust storms are atmospheric events typically associated with dry lands due to the preponderance of dried and unconsolidated substrates with little vegetation cover. The strong and turbulent winds that blow on these surfaces raise fine-grained material, a large part of which consists of particles the size of silt (4–62.5 μm) and clay (<4 μm), reducing visibility to less than 1 km. The atmospheric concentrations of PM10 dust exceed 15,000 μg/m3 in severe events [87], although the concentrations naturally decrease with the distance from the areas of origin, extending hundreds of kilometers. The dust particles and cells associated with them are transported in this manner and will be deposited finally, by the effect of rain, snow, or other meteorological phenomena. Therefore, there is a continuous transfer of mineral and biological matter through the atmosphere that moves from the air to the terrestrial environment and changes its geographical area [7, 24].
\nThe Sahara-Sahel desert located in northwestern Africa is one of the major sources of windblown dust in the world [9]. This phenomenon has an impact on the Mediterranean coastline, but Saharan dust has been transported toward the north of Europe and has been found on numerous occasions in the Alps [88, 89] or blown toward the Atlantic and Caribbean [8, 90]. It has been estimated that 80–120 tons of dust are transported annually through the Mediterranean toward Europe [23, 91, 92]. In particular, dust transported by the winds can reach an elevation of up to 8 km in the atmosphere over the Mediterranean basin [93]. Because of its geographic position, the Iberian Peninsula is often affected by these dust events. Specifically, the Sahara-Bodele depression, located at the southern edge of the Sahara desert, has been described as the richest dust source reaching the Iberian Peninsula. Southern Spain is the main area affected, but dust can reach the Pyrenees and even France [43]. Different researchers have studied the mineralogical and chemical composition of Saharan dust, which has been observed to contain calcite, dolomite, quartz, different clay minerals, and feldspars as the main mineral components [94]. The intrusion of big amounts of these components is an important influence on nutrient dynamics and biogeochemical cycling in the atmosphere of the Iberian Peninsula.
\nDespite the large number of studies on dispersion, geochemistry, and mineralogy of African dust, few are focused on microbiology. All these studies conclude that there are microbes associated with dust because there are higher concentrations of aerosolized microorganisms during dust events [43, 90, 93, 94, 95, 96]. However, the magnitude of the concentrations and the specific microbes associated with dust events remain the subject of debate. On the other hand, the viability of these microorganisms is another big question. The United States Geological Survey (USGS) develops the Global Dust Program to investigate the viability of microorganisms transported in dust masses. USGS authors using DNA sequencing of the ribosomal gene were able to isolate and identify more than 200 viable bacteria and fungi in St. John’s samples in the USA [8, 36, 90]. Fungi and bacteria associated with atmospheric dust can be recovered and cultivated, but they must be gram-positive bacteria and many spore formers, which makes them resistant to the extreme conditions of the atmosphere.
\nTherefore, fungi and bacteria associated with dust may have been isolated from dust intrusions, but a percentage of the viable ones already remains an unanswered question. Another big question is the activity of these cells in the atmosphere. It is clear that they are resistant to extremophile conditions, but the question is whether they are developing their life cycle in this particular environment. This question could be answered by molecular ecology methodologies based on the isolation and sequencing of mRNA, but low atmospheric biomass and high variability are, once again, the great problem when developing this type of RNA-based methodologies. On the other hand, clinical records point to many of the viable microorganisms identified in the Saharan dust as the cause of respiratory diseases (asthma and lung infections or allergic reactions), cardiovascular diseases, and skin infections [7, 90, 97, 98]. It is known that other microbes associated with dust in the air are pathogenic to humans, including those that cause anthrax and tuberculosis, or to livestock (such as foot and mouth disease) or plants [7, 90, 97, 98]. Characterization, quantification, and feasibility studies are vital to address these problems.
\nIt is common to find fungal spores belonging to the genus Aspergillus, Nigrospora, Arthrinium, and Curvularia associated with Saharan dust. Bacterial taxa comprised a wide range of phyla, including Firmicutes, Proteobacteria, Actinobacteria, and Bacteroidetes. Generators of genus spores such as Clostridium and Bacillus are very common, along with other gram-positive ones such as Geodermatophilus or Streptococcus. Also, Alphaproteobacteria, a very common bacterium class in soils (e.g., the family Sphingomonadaceae), are associated with dust [4, 9]. As regards Archaea, there are few studies of the atmosphere, in general, and of dust, in particular, that focus on this domain. Surely, reduced cases of pathogenic archaea have been studied to a lesser extent. Aeropyrum is the most detected genus of airborne archaea, but it is related to marine aerosols [11]. On the other hand, studies of pollen associated with dust are widespread. An interesting study investigated pollen transported from North Africa to Spain through Saharan dust and found that pollen from five non-native plant species was detected exclusively during dust events [99]. Lastly, viruses and virus-like particles have a great interest in the emission of dust. One study mentions virus-like particles associated with a transoceanic dust event. This report is based on epifluorescent microscopy of filters stained with a specific nucleic acid stain. An increase in the order of magnitude of virus-like particles was observed, from 104 to 2105 m−3 between the baseline condition and dust conditions in the Caribbean [41]. It is speculated that free airborne viruses show worse resistance to high ultraviolet radiation and dry air associated with long-distance transport in dust events resist worse than others [9].
\nFour aerobiology sampling flights took place during February and March 2017 using the CASA C-212-200 aircraft from INTA. The study focused on microbial diversity in the atmosphere of the Iberian Peninsula during and after a Saharan dust intrusion. Flights took place under four different conditions: (1) during a strong Sahara dust storm that reached the north of the Iberian Peninsula, from February 22 to 24, 2017 (February 23, 2017) (\nFigure 7\n); (2) following precipitation (February 28, 2017); (3) following a dry period (March 8, 2017); and (4) along the northern coast of Spain (March 9, 2017). In each flight, samples were collected at different altitudes, and air samples were obtained simultaneously at ground level. A total of 20 samples were collected and are being analyzed. Cell presence was observed by scanning electron microscopy (SEM), and bacterial diversity is being studied by DNA extraction, 16S rRNA gene amplification, and Illumina MiSeq sequencing. Results are being analyzed via bioinformatics and biostatistical software (MOTHUR, SPSS, STAMP, CANOCO, and PAST) which will allow us to compare the results between the different flows and scenarios.
\nSaharan dust intrusion. Dust pours off the northweat Afrincan coast and blankets the Iberian Peninsula, 23 February, 2016. NASA satelital imagen via MODIS.
Although this study is not yet finished, some data can be advanced in this chapter. \nFigure 6\n shows SEM microphotographs obtained from samples in different scenarios. In general, the samples obtained during the days of dust intrusion (flight of February 23) appear completely covered with mineral particles. In these cases, more biological cells were detected than in the rest of the days. In the particular case of samples from the marine coast flight, more diatoms were observed (\nFigure 6E\n).
\nThe analysis of diversity using the Shannon index showed that, in all cases, diversity was greater on days of Saharan dust intrusion, both in the samples taken from the ground and those taken at higher altitudes with the aircraft. This indicates that Saharan dust contributes microorganisms that are not present in the atmosphere on a daily basis. Diversity analysis showed phylum characteristics of soils, being Alpha- and Betaproteobacteria the most abundant classes. All of the analyses performed showed that bacterial diversity detected at ground level and in-flight samples during the dust intrusion event were similar among one another. The genus taxonomic levels of Sphingomonas, Geodermatophilus, Methylobacter, Rhizobiales, Bacillus, or Clostridium were present in every sample, but their sequences were more abundant in the case of ground samples and dust intrusion samples collected during the day flight. However, sequences of the genus Flavobacterium, Streptococcus, or Cupriavidus were most abundant in the case of samples collected during flight.
\nPreliminary conclusions show that bacterial diversity of airborne bacteria during days of dust intrusion is higher and similar to bacterial diversity commonly detected in soil samples. Further analyses are being conducted with these samples to obtain a complete description of the evolution of bacterial diversity during those days.
\nIntense UV radiation, low pressure, lack of water and nutrients, and freezing temperatures turn the atmosphere into an extreme environment, especially its upper layers. However, it is widely known that airborne bacteria, fungal spores, pollen, and other bioparticles exist. Numerous bacteria and fungi have been isolated and can survive even at stratospheric altitudes. Microbial survival in the atmosphere requires extremophilic characteristics, and therefore airborne microbiota is potentially useful for biotechnological applications. The role of airborne microbial communities is vital in the Earth, including interactions among the atmosphere, biosphere, climate, and public health. Airborne microorganisms are involved in meteorological processes and can serve as nuclei for cloud drops and ice crystals that precede precipitation, which influences the hydrological cycle and climate. Furthermore, their knowledge is essential in understanding the reproduction and propagation of organisms through various ecosystems. Furthermore, they can cause or improve human, animal, and plant diseases.
\nAirborne platforms that allow conducting a direct study of microorganisms in the atmosphere and molecular methodologies (e.g., “omics”) could represent a major opportunity for approaching this question. Nevertheless, some challenges must yet be solved, such as low biomass, efficiency of sampling methods, the absence of standard protocols, or the high variability of the atmospheric environment.
\nDeserts and arid lands are one of the most important sources of aerosol emissions. Clouds of dust generated by storms mobilize tons of mineral particles, and it is known that microorganisms remain attached to the particles being transported over long distances. The large number of mineral particles and microorganisms thus placed into the atmosphere has global implications for climate, biochemical cycling, and health. North African soils, primarily the Sahara Desert, are one of the major sources of airborne dust on Earth. Saharan dust is often transported to southern Europe and could even reach high altitudes over the Atlantic Ocean and the European continent. Again, airborne platforms could be a perfect opportunity for conducting a direct study of the microbiology of this kind of events.
\nThis work has been supported by grants from the Spanish government (
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