The top 10 publications in the ISI Web of Science database (Web of Science Core Collection) for ‘all years’ (1970–2016) with ‘biosorption’ in the topic.
Although there has been an intense study and exploitation of research regarding biosorption processes, the lack of coherent and similar methodologies, essential to the elaboration of any consequential and universal conclusion, associated with the lack of biosorption studies conducted at a pilot and industrial scale, with multicomponent solutions or real effluents, as well as the lack of information regarding the pollutant interactions makes the implementation and commercialization of biosorption technology very complicated. This chapter summarizes the existing knowledge and the experimental work conducted at a pilot scale or industrial scale with multicomponent solutions and critically reviews aspects related to biosorption research regarding the advantages, the disadvantages, the rationale, the scope and scientific value of biosorption processes and the obstacles to commercial success.
- organic pollutants
- pilot and industrial scale
Although the contamination of water resources is a widely recognized fact and a critical universal issue, it is still a common occurrence [1, 2]. The major sources of aquatic as well as terrestrial and atmospheric systems contamination are effluent outfalls and gas emissions from industries, agricultural activities and refinery contaminants  that end up entering water bodies via rain water, soil and groundwater systems. The contaminants comprise (i) inorganic chemicals such as metals, extensively used in a wide variety of industries, including metal plating, mining, batteries, electroplating, ceramic, chemical manufacturing of paint and coating, health-care products, extractive metallurgy, petrochemical and fine chemistry  and (ii) organic chemicals such as industrial solvents, volatile organic compounds (VOCs), pharmaceuticals, insecticides, pesticides, dyes  and food processing wastes .
The non-natural redistribution of these chemicals has culminated first in their increasing discharge and accumulation into the different environmental matrices and second in the development of environmental and health problems (Figure 1) [3, 4]. Therefore, there is a constant search for economical, efficient, effective and eco-friendly processes able to not only decontaminate wastewaters but also ensure that the presence of the pollutants discharged into the aquatic systems is below the permissible limits.
In the past decades, great attention and concern have been given to the continuous and increasing discharge of metals such as chromium, mercury, lead , cadmium and nickel into the environment. This increasing concern is due to metals’ inherent properties, (i) persistence in nature, (ii) tremendous toxicity even at low concentrations and (iii) tendency for bioaccumulation via food chain in living tissues, which may culminate in the triggering of several serious diseases and health disorders .
Chromium compounds, for instance, are carcinogenic and nephrotoxic in nature. Exposure to mercury and lead may provoke allergic skin reaction, eventual negative reproductive effects as well as damage to brain function and disruption of the nervous system . Cadmium exposure may cause severe damage in different organs including the testis, lungs, liver and kidneys and even lead to infertility [5, 6]. It also affects the action of enzymes and induces genomic instability through complex and multifactorial mechanisms, such as proteinuria, and an increase in the frequency of kidney stone formation, eventually causing certain types of cancer (group B1) . Besides being listed in the carcinogenic group B2, nickel has been implicated as a teratogen nephrotoxin and an embryotoxin element. Acute and chronic nickel exposure can cause several disorders such as cyanosis, chest pain, tightness, pulmonary fibrosis, skin dermatitis, lungs and kidney damage and renal oedema .
The capacities of metals to disrupt the function of fundamental biological molecules, such as DNA, proteins and enzymes, and to displace certain metals essential for the cell viability by similar metals are the two major causes of their toxicity. For instance, lead can replace calcium in the bone and other tissues where it is required, whereas cadmium can replace zinc in some proteins that require it for their structure as well as function .
More recently, the discharge of organic chemicals such as pharmaceutical products , volatile organic compounds, aromatic hydrocarbons  and dyes  has also caught the world attention, due not only to their persistence, toxicity and mobility in the environment but also to their widespread use and discharge as well as their impact on all forms of life.
Despite the fact that every single aspect connected to pharmaceutical efficiency and patient security to be under scrutiny , the complete extent and consequences of the presence of emerging pollutants in the environment matrices and on the wellbeing of all forms of life are not yet sufficiently studied in terms of toxicity, degradability and occurrence, allowing it to remain unregulated.
Pharmaceutical compounds have been detected at trace concentrations (ng/L levels) in a wide variety of environmental water samples including sewage flows, rivers, lakes, groundwater aquifers and drinking water . Although the concentrations of these pharmaceutical products have been detected at trace concentrations in a broad variety of aquatic environments, their continuous input may compose a potential threat for living organisms. Furthermore, pharmaceutical products are often synthesized in order to remain unchanged during their passage through the human body, which makes them and their metabolites persistent pollutants in environmental matrices .
The increased use of organic compounds in almost, if not all, industrial sectors as well as in household activities and consequent discharge and accumulation into the environment has increased in an extremely significant way in the past years [2, 12, 13, 14]. Most of these compounds are extremely toxic to humans due to (i) their general carcinogenic and mutagenic properties, (ii) their capacity to form intermediates with the same or even the higher level of toxicity  and (iii) their persistence and mobility into the different environmental matrices .
More than 1 × 105 dyes are currently marketed with an annual production exceeding 7 × 105 tons per year, of which about 2% are discharged directly to effluents from manufacturing operations, whereas 10% are discharged from textile and related industries . The dye lost through the practices of textile industry poses a serious problem for wastewater management and treatment, since it can reach loss values as high as 50%. About 2 × 105 tons of dyes are discharged annually into the environment, especially into water bodies .
Although chemical precipitation, reverse osmosis, complexation, solvent extraction, ion exchange, adsorption on granular activated carbon, condensation, thermal degradation, oxidation and incineration comprise the conventional abiotic methods usually employed to remove different types of pollutants from effluents , biotic methods such as water purification treatments and standard sewage as well as auxiliary reed bed and wetlands approaches  have been used for many years. The outstanding ability of microorganisms to detoxify organic and inorganic pollutants [15, 18] and to the downside of the abiotic methods which can be summarized (i) as expensive, (ii) not environmentally friendly and (iii) usually dependent on the concentration of the waste  makes them an attractive alternative to decontaminate contaminated solutions.
2. Biosorption: a general overview
Microorganisms, in particular bacteria and fungi, have been receiving particular attention in the area of environmental microbiology and biotechnology due to their ability not only to decompose a wide range of organic compounds, from natural and anthropogenic origin, but also to accomplish changes in the speciation and mobility of metals and radionuclides as well as other inorganic elements by oxidation-reduction and other changes, most of which are a direct consequence of metabolic properties of living organisms and microorganism .
Although the term
Some publications [18, 20, 21] indicate that most researchers define biosorption as a passive and metabolically independent process that can be performed either by dead biomass or fragments of cells and tissues or by living cells as an active and metabolic-dependent process. It is important to highlight that both mechanisms can overlap adding additional confusion in the use of the terminology.
It is also important to highlight that (i) biosorption is a crucial part of many processes taking place in nature, including, for example, antigen-antibody immune reactions and adsorption to host cells, as the first stage in virus replication or sorption in soil and that (ii) numerous methodological approaches used in medicine, life sciences and biotechnology are, in fact, based on biosorption processes, for instance, the staining of microbial cells for electron microscopy and targeted therapies in cancer treatment. It is therefore possible to affirm that many life phenomena are in some way related to interactions between a sorbate and biological surfaces . Basically, biosorption is a reversible and rapid process of binding of ions or neutral molecules from aqueous solutions onto functional groups that are present on the surface of biomass, independent on cellular metabolism, efficient and selective .
Presently, it is accepted that biosorption is a physico-chemical process, simply defined as the removal of substances from solution by biological material, and includes mechanisms such as absorption, adsorption, surface complexation ion exchange and precipitation . The addition of the prefix
The mesmerizing features of biosorption processes over traditional treatment methods comprise (i) economical operating costs; (ii) inexpensive biological materials, usually obtained from agriculture or from industrial wastes; (iii) high efficiency; (iv) no additional nutrient requirement; (v) minimization of biological or chemical sludge; (vi) biosorbent regeneration; and (vii) the possibility of metal recovery. In addition to all this captivating features, biosorption processes can be accomplished in an extensive range of pH values (from pH 3 to pH 9) and temperature values ranging from 4 to 90°C.
The first paper on biosorption was published in 1951, and since then, enormous efforts have been made to accomplish efficient, effective and economic biosorbents to be employed in wastewater treatment. Fundamental progresses have been accomplished over the past decades in order to understand the complex biosorption mechanisms, the methods for its quantification (equilibrium and kinetics) and the factors that influence efficiency and the rate of the process (Figure 2) .
Although the majority of the biosorption research conducted till now has been performed on microbial systems, mainly bacteria, microalgae and/or fungi, with metals and related substances (Table 1), the term is now being applied to all types of organic compounds and to particulates.
|1||Review of second-order models for adsorption systems ||1402|
|2||Biosorption of heavy metals ||1323|
|3||A review of the biochemistry of heavy metal biosorption by brown algae ||1133|
|4||Application of biosorption for the removal of organic pollutants: A review ||1002|
|5||Biosorbents for heavy metals removal and their future ||903|
|6||Application of chitosan, a natural aminopolysaccharide, for dye removal from aqueous solutions by adsorption processes using batch studies: A review of recent literature ||832|
|7||Removal of Congo Red from water by adsorption onto activated carbon prepared from coir pith, an agricultural solid waste ||759|
|8||Activated carbons and low cost adsorbents for remediation of tri- and hexavalent chromium from water ||757|
|9||Adsorption of several metal ions onto a low-cost biosorbent: Kinetic and equilibrium studies ||749|
|10||Interactions of fungi with toxic metals ||740|
The massive research concerning biosorption of metals is an unsurprising fact, taking into account not only the toxicity effect and increased discharge of these contaminants into the environment but also the nature of adsorption and ion exchange mechanisms. Nevertheless, it is also crucial to highlight that regardless the continuous increase in published research related to the biosorption of hazardous substances and/or elements, there has been little or no exploitation in a pilot and industrial scale and/or context  and on the decontamination of multicomponent solutions [3, 4, 7, 22, 23]. In fact, despite the biosorption process that has been discussed in literature for 60 years with over 13,000 scientific papers in peer-reviewed journals , so far most of this research was performed in a laboratory scale, using batch tank reactors or packed mini-column, and has not been extensively implemented in an industrial scale and in multicomponent solutions. The team of Professor Bohumil Volesky from McGill University, Canada, and his company BV Sorbex comprise the few researchers that have contributed to the scale-up of sorption process field, from a laboratory scale to a pilot or industrial scale . The team of the Centre of Biological Engineering from the University of Minho, Portugal, has also been contributing to the study and understanding of (i) the scale-up of biosorption processes from a laboratory scale to a pilot scale and (ii) the increase of solution complexity to be decontaminated, evolving from single-component solutions to multicomponent solutions, mixing organic and inorganic compounds [3, 4, 7, 9, 15, 24], the main subject of this chapter.
3. Biosorption in multicomponent solutions
Although most of industrial and household effluents and wastewater are composed by a cocktail of contaminants made of metal residues and organic compounds, few studies regarding the simultaneous removal of multicomponent solutions have been conducted and optimized, studies that would better simulate the behaviour of the pollutants present in real effluents. The effect that different types of contaminants (inorganic versus inorganic and inorganic versus organic) have on each other and the effect that different initial concentrations of metal exert on the bioremoval (biodegradation and biosorption among other biological processes) of the organic contaminant have also been poorly investigated. For these reasons, the authors opted to review the state of the art of biosorption from multicomponent solutions, from a laboratory scale to a pilot and/or industrial scale.
Costa and Tavares  studied the ability of two fungi and one bacteria (
More complex systems were further evaluated  with a suspended bacterial culture of
Attempting to mimetize the complexity of real effluents and wastewaters, biosorption experiments of multicomponent solutions (Al(III), Ni(II), Cd (II) and Mn(II)) by a
At a pilot scale, it was observed that the biosorption percentage of all the sorbates (organic and inorganic) tended to increase through time and followed the sequence diethylketone > Al(III) > Cd(II) ≈ Ni(II) ≥ Mn(II), and this is explained by the bioavailability and structural similarity between Ni(II) and Cd(II) that promote the uptake of Cd(II) by the cell enzymes instead of Ni(II) and by the combination of the reduced size of the ionic radius of Mn(II) associated with its reduced electronegativity and the small porosity of the support. The complete bioremoval of diethylketone and its metabolites was achieved, even after the addition of diethylketone to the bioreactor and the sorption percentage of each metal increased through time.
The effect of different initial concentrations of Cd(II), Cu(II), Zn(II), Pb(II) and As(II) (10 mg/L or 100 mg/L) on the bioremoval of fluorene (10 mg/L) by
3.1. Correlation between metal concentration and microbiological processes
Metals including cadmium, chromium (III and VI), copper, lead, mercury, nickel and zinc are reported to inhibit microbiological processes such as acidogenesis, methanogenesis, nitrogen transformation, biomass production and enzymatic activity .
Although studies concerning the influence of metals on organic contaminant bioremoval are scarce, it has been demonstrated that those elements are able to inhibit organic contaminant bioremoval, under both aerobic and anaerobic conditions.
Cadmium, chromium (II), copper, mercury and zinc were found to inhibit the biodegradation of 2,4-DME in lake water samples inoculated with either a sediment or an aufwuch (floating algal mat) sample . In the aufwuch samples, mercury revealed to be the most toxic metal, with a microbial inhibitory concentration (MIC) of 2 × 10−3 mg total mercury/L, whereas in the sediment samples, zinc was the most toxic metal with a MIC of 6 × 10−3 mg total zinc/L. Naphthalene (NAPH)-degrading
Not all studies were focused on the effect of single metals on bioremoval of a single, pure organic pollutant. Benka-Coker and Ekundayo  investigated the impact of copper, manganese, lead and zinc on crude oil biodegradation by
3.2. Correlation between metal concentration and bioremoval inhibition
It is acknowledged that the bioremoval of an organic pollutant decreases as the concentration of bioavailable metal increases in co-contaminated systems (Figure 3). However, this pattern is not always observed. Two other additional patterns describing the effect of metals on the bioremoval of organic pollutants have been shown.
Low metal concentration enhances bioremoval of organic pollutant; high metal concentrations inhibit it—additional pattern 1: diverse studies showed a pattern of metal toxicity in which low metal concentrations enhance bioremoval activity, till the maximum level of stimulation is reached. After this point, an increase in metal concentration will lead to an increase in metal toxicity (Figure 3, Line 2). Sustaining this pattern is the result obtained by Capone et al.  showing that methanogenesis was enhanced by the addition of some metals.
Bioremoval inhibition of organic pollutants is due to low metal concentration; lower bioremoval inhibition of organic pollutants is due to high metal concentration—additional pattern 2: several studies suggested that low concentrations of metal strongly inhibit bioremoval activity, until a maximum of inhibition is achieved (Figure 3, Line 3). After this point, an increase in metal concentration will lead to a decrease of metal toxicity. An example is the work conducted by Said and Lewis  where an increase in metal concentration was responsible for a decrease in 2,4-DME bioremoval.
Briefly, the existence of different patterns of responses of organic pollutants towards metals is possible to assume and that this variety of responses makes the understanding and prediction of metal toxicity in the environment more difficult, since these elements may influence both the ecology and physiology of the pollutant-degrading microorganisms.
Unless the models used to predict the influence of metals on the bioremoval of organic pollutants incorporate both the ecologic and physiologic effects of metals towards the pollutant-degrading microorganisms, they may fail their main purpose.
3.3. Biosorption in multi-metal solutions
As previously mentioned, despite the research concerning biosorption processes has been well documented in the literature, biosorption of different metal ions by different types of biological materials has been mainly conducted in single-metal solutions . Information concerning biosorption studies in binary- [30, 31, 32, 33, 34], tertiary- [31, 32, 33, 34, 35] and quaternary-component solutions  is very scarce. Moreover, the use of different evaluation methodologies makes any attempt to draw any meaningful and universal conclusion very difficult and, on the other hand , the influence that anions may exert on the biosorption process of metal cations has been somehow neglected.
3.3.1. Effect of anions
Three aspects related to the influence of anions on the biosorption processes are usually considered in the available literature: (i) the influence that the anion has on the maximum biosorption capacity of the sorbent, in single-metal solutions ; (ii) the influence of anion concentration on the biosorption of several metal ions, in multi-metal solutions [37, 38, 39, 40, 41]; and (iii) the nature of the biosorbent that can influence significantly the effect of the anion on the biosorption capacity .
The biosorption of four metals—Cr(VI), Co(II), Ni(II) and Zn(II)—by the
Kuyuca and Volesky  studied the biosorption of Co(II) ions in the presence of SO42− and PO43− by the brown macroalga
The degree of inhibition for the biosorption of La(III), Cd(II), Pb(II) and Ag(I) cations, by the
As referred previously, the influence of the anion on the biosorption capacity will vary depending on the metal ion oxidation state, as it was observed for the biosorption of Cr(III) and CR(VI) ions , with the following inhibitory orders SO42− > Cl− ≈ NO3− and NO3− > SO42−.
3.3.2. Effect of the ionic concentration
Considering the limited number of active sites present on the biosorbent surface, it is accepted that the biosorption capacity of the biosorbent towards a specific pollutant (metal or not) in a multicomponent solution is inferior to the one in single-component solutions; therefore, the contaminants will compete for the active sites, available for sorption .
Fagundes-Klen et al.  observed that the amount of Zn(II) biosorbed by
It is therefore worth noting that as the ionic concentrations become higher, there is a growing force able to overcome the mass resistance transfer of metal ions through the biosorption process. The published data  showed that even though lead ions (Pb2+) have higher affinity than copper (Cu2+) to be biosorbed by an algae belonging to the genera
3.3.3. Effect of electronegativity and atomic weigh of metals
In multi-metal solution, the electronegativity and atomic weight of metals can also have an important role in the biosorption process and efficiency. Biosorption experiments showed that when mixed, Ni(II) and Zn(II) sorption by wheat straw presented different performances, revealing a competition between both metals for the actives sites present on the biosorbent surface and a higher preference for Zn(II) rather than Ni(II) . These results are easily justified taking into consideration the more appealing physical characteristics of Zn(II): lower electronegativity and higher atomic weight of Zn(II). The oxygen-containing group present on the wheat straw (negative sites) repels Ni(II) more than Zn(II), making it more difficult to be sorbed.
3.3.4. Effect of temperature
As previously mentioned (see Section 2, Figure 2), temperature also plays an important role on the biosorption processes, as well as on all biological and physico-chemical processes. The biosorption of Cr(III), Cu(II) and Zn(II) by wine-processing waste sludge (WPWS) in a ternary system was found to be significantly affected by temperature. At normal conditions, the biosorption of these three metals in a mixture by WPWS followed the trend Cr(III) > Cu(II) > Zn(II). However, when the temperature decreases to 10°C, the biosorption of Cr(III) was inferior than Cu(II) .
4. Critical assessment concerning the biosorption research on multicomponent solutions
As previously mentioned, in the past few decades, there has been an intense study and research concerning biosorption processes to treat contaminated environmental matrices and wastewaters. However, it is doubtful whether such a remarkable rise in published output has significantly enhanced the knowledge about biosorption process, or aided any industrial exploitation, which so often is the primary underlying principle for such investment and work [18, 19, 21]. Despite the incontestable progress made over decades of research, most of the biosorption studies are still conducted at a laboratory scale and involve (i) the characterization of a selected sorbent, which will sorb a given contaminant from solution, (ii) the study of the effect of physico-chemical parameters may have on biosorption and (iii) the use of metals. Considering that the majority of elements present in the periodic table are classified as metals, the potential number of ‘original’ research is most likely beyond comprehension, especially if coupled with the gigantic number of microbial species, strains and metabolites/derived substances. It is therefore expected that the output of publications related to biosorption shows no sign of decreasing and will be increased due to the continuing number of new journals, including those that are web based [18, 19].
It is also logical to infer that several technical and scientific issues should be solved in order to meet the industrial demands and bring the biosorption technology into commercialization. Based on this, several future perspectives can be made:
Although a large number of biological materials are available, it is still essential to find and/or prepare more economic, efficient and selective sorbents.
It is necessary to elaborate, improve and/or simplify the mathematical models used to describe the multicomponent systems.
To achieve the best biosorption performance, it is crucial to identify the biosorption mechanism underlying relatively to the class of biosorbents used.
To obtain the best biosorption performance, it is essential to identify the biosorption mechanism in relation to the general group of the selected biosorbent.
Biosorption studies should also be conducted at a pilot or industrial scale and with multicomponent solutions or, if possible, real effluents and wastewaters. This will allow to understand the interactions between all the sorbents and the sorbate and thus optimize the biosorption process, promoting its future commercialization.
Although there is a significant number of patents and publications available, the biosorption process has been so far mainly performed at a laboratory scale. Up-scale of the biosorption processes should be enhanced.
In order to apply the biosorption technology at an industrial scale, economic analyses are necessary to estimate the overall cost of the sorbent and biosorption process.
Additional attention should be paid to the application of biosorption technology in product separation, recovery and purification.
The use of similar and universal evaluation methodologies allows to draw meaningful and universal conclusions .
Eradicate the poor and misleading communications, and the use of loose terminology, which is associated with the great complexity of biosorption phenomena, has intricated the process of prioritizing fundamental scientific and commercial tasks and of creating clear information for the industry.
This study was supported by the Portuguese Foundation for Science and Technology (FCT) under the scope of the research project PTDC/AAG-TEC/5269/2014, the strategic funding of UID/BIO/04469/2013 unit and COMPETE 2020 (POCI-01-0145-FEDER-006684) and BioTecNorte operation (NORTE-01-0145-FEDER-000004) funded by the European Regional Development Fund under the scope of Norte 2020—Programa Operacional Regional do Norte. Filomena Costa thanks FCT for a PhD grant (SFRH/BD/77666/2011).