Examples of fatty acids found in bacteria: formula, common and systematic names [modified from 27]
1. Introduction
As was published in [1], based on 16S rRNA sequences, prokaryotes are divided into two primary groups: Archaebacteria (Archaea) and Eubacteria (Bacteria). With the exception of Cyanobacteria, all the main lineages of photosynthetic organisms belong to the Eubacterial Phyla and the unrelated halobacterial species.
Within Eubacteria, photosynthetic organisms are found according to the following divisions: (i) gram-positive bacteria belonging to the family Heliobacteriaceae, (ii) green non-sulphur bacteria (also known as filamentous green bacteria) such as
Anoxygenic green and purple photosynthetic sulphur bacteria (GPSB/PPSB) are anaerobes. They do not release O2 by photosynthesis, and as electron donors for this process, they use sulphur and its derivatives. These microorganisms have bacteriochlorophyll (Bchl) and accessory carotene pigments that include spirilloxanthin, okenone and chlorobactene pigment series.
Photosynthetic pigments in green photosynthetic sulphur bacteria (GPSB) include Bchl c, d and e, as well as chlorobactene and isorenieratene. PPSB may contain Bchl
Morphological patterns are limited in bacteria, and phenotypical together with molecular properties have been used for the identification of these microorganisms. Chemotaxonomy takes into account fingerprint methods using proteins, nucleic acids, sugars isoprenoids and fatty acids, among other molecules. For example, an average of fatty acids can be easily obtained by gas chromatography (or by gas-liquid chromatography). This average is called a ‘fatty acid profile’ and a part of this profile is a pattern [2]. The pattern is generated by cleaning and adapting the fatty acid profile. Both are highly reproducible when growth conditions, the physiological age of the cells and analysis are well standardized. Subsequently, the fatty acid patterns can be used for the identification of bacteria, library generation, taxonomy, epidemiological and ecological studies [2], and obviously it is very useful for detecting bacteria in samples of different origins.
Photosynthetic prokaryotes have a great variety of fatty acids, and they are useful for distinguishing these microorganisms; actually, they are recommended for the description and identification of new species ([3, 4]). For example,
Fatty acids from whole cells of
Currently, studies have reported 12 fatty acids in complete cells from GPSB, and the fatty acid C14:0 accounts for 14% [6] to 27.10% [5]; the fatty acid C16:1 accounts for at least 37.3% in these bacteria [5].
Hexadecanoic is the third main fatty acid in GPSB [6] in quantities from 10% in
Minor fatty acids have been reported in these microorganisms and they include: C12:0, 12-Me-C14:0, 5-Me-C16:0, 14-Me-C16:0, C15:0, 15-Me-C16:1, C17:0, C18:0 and a cyclic fatty acid [5-7]. GPNSB (like
In oxygenic photosynthetic cyanobacteria - for example, in
Fatty acids of the Chromatiaceae family have been more studied than those from GPSB, and analysed strains of this family include members of the genera
The other family of PPSB, the Ectothiorhodospiraceae, has C18:1 as the main fatty acid, which contributes with 74.7% of the total extracted (96.7%) in
This chapter describes the influence of MgSO4 and NaCl on three cultures of GPSB (
2. Fatty acids analysis
The analysis of fatty acids as methyl esters has been used to identify bacteria species. Their composition and the ratios of these compounds are useful in identifying microorganisms. They are conserved if bacteria are grown in similar conditions [11]. Also, it has been pointed out that information such as phylogenetic data and similarities derived from the fatty acid analysis are in broad agreement with 16S rDNA results, and appear to accurately distinguish between most species [12].
The number of bacterial species evaluated is a limitation in comparing the information available about the fatty acid composition from bacteria [12]. GPSB and PPSB are also not an exception compared to the fatty acid studies on chemoheterotrophic bacteria. There are very few investigations about the influence on fatty acid compositions of the culture medium for bacterial growth (e.g., salinity), the age of the cells or the physical factors (e.g., temperature) used to culture the microorganisms.
Fatty acid analysis may also depend on the extraction technique; in some studies, different procedures have been applied to investigate the fatty acid compositions of
Different techniques and methods for fatty acid analysis have been developed since Abel et al. (1963) [14] proposed quantitative and qualitative analyses for characterizing microorganisms, where it was indicated that gas chromatography (GC) has the necessary sensitivity, rapidity and selectivity for such analyses. They considered that this is an extremely selective method, such that a single normal-sized colony of microorganisms is sufficient. This method requires a short time between preparation to examination, and organic and inorganic nutrients do not interfere. The fatty acid methyl esters (FAMEs) from cell membranes have been analysed using GC. These fatty acids were extracted from cell hydrolysates and derivatized to volatile methyl esters for further detection by GC [14].
Other detection methods for fatty acid analysis have also been applied. These include gas-liquid chromatography and mass spectrometry (MS), which is a rapid, automated method for analysing mixed populations, and the various configurations of MS offer combined advantages of speed, sensitivity and selectivity. The method also requires that molecules be vaporized into the gas phase before they can be ionized and analysed.
Gas chromatographic or high pressure liquid chromatographic separation increases the capability for analysing complex mixtures, and they together provide two complementary kinds of characterization. Such chromatographic separation could even distinguish chirality, which is usually invisible to MS [15]. Fatty acids analysis and quantification by GC is carried out by the extraction of lipids from microorganisms, followed by hydrolysis and methylation. The resulting FAME profiles are used for the identification and differentiation of these microorganisms [16]. Actually, there are standardized and automated techniques to asses these compounds; using the Microbial Identification System (MIS) it is a possibility, in a short time, for acquiring precise information about bacteria fatty acid compositions. This system is applied most frequently in the clinical market and it is limited in the number or environmental species they can identify. Nevertheless, microbial fatty acid profiles are unique from one species to another [2].
The MIS system – also known as the MIDI Sherlock Holmes System – which identifies microorganisms using FAMEs and GC, consists of large microbial libraries; the procedure for FAME analysis [17] may be summarized by the following steps: 1) harvesting (the removal cells from the culture media), 2) saponification (the lysis of the cells to liberate fatty acids), 3) derivatization (methylation, the formation of FAMEs), 4) extraction (the transfer of the FAMEs from the aqueous phase to the organic phase by the use of an organic solvent), 5) base wash (an aqueous wash or the organic extract prior to chromatographic analysis).
Alternative procedures have also been proposed for the extraction and separation of FAMEs without the previously described steps, such as by the direct injection of the culture broth, allowing the separation and quantification of alcohols and volatile and non-volatile fatty acids. This method simplifies the procedure for fatty acid identification and quantification [18].
Pyrolysis-MS is another technique that allows the direct analysis of bacteria (depending on the organism). With pyrolysis, the bacteria are broken (in an inert atmosphere) using heat to produce volatile, low molecular weight substances that are detected and quantified. This technique involves the analysis of the total cellular composition of the bacteria, and a single bacterial colony is sufficient for analysis [19].
This technique can be used to provide GC data from non-volatile/solid materials. A GC with an ion trap mass spectrometer (IT-MS) could be used for this kind of analysis [20].
2.1. Fatty acid definition
Lipids are defined as natural products that may be isolated from biological materials by extraction with organic solvents and which are usually insoluble in water. This definition includes sterols, terpenoids, isoprenoids, waxes and pigments, many of which are not present in bacteria [21], and the simplest are the fatty acids, as in Table 1. These are the fundamental building blocks of complex lipids, like fatty acyls, glycerolipids, glycerophospholipids, sphingolipids, sterol lipids, prenol lipids, saccharolipids and polyketides [22].
Microbial fatty acids are typically 12-24 carbons long and the common membrane fatty acids are 14-20 carbons long. These compounds are either ester- or ether-linked. The latter is rare, and has been found in the phospholipids of Archaea [23]. In general, bacteria contain fatty acids between C10 and C20 in length, but there are some eubacteria species that have polyunsaturated fatty acids, like
Fatty acids are essential to cells and their metabolic functions. These compounds are typically associated with energy storage and the structural fluidity of membranes; they form compounds that play important roles in cell signalling processes [26]. In addition, they function as metabolic intermediates and form part of the higher molecular weight lipids [27]. These carbon-based ‘backbone’ chains, may be elongated, shortened or altered by the activity of the elongase or desaturase enzymic activity, respectively, and longer fatty acids are results of lipogenesis. Moreover, the size of the fatty acid structure depends upon the addition or removal of double hydrogen bonds and catabolic activity [26].
Structurally, fatty acids are long chain monocarboxylic acids of the general formula R.COOH. Usually, the R-group has a long chain - commonly unbranched - consisting of an even number between eight and 24 carbon atoms [27]. The chain has a hydrophobic aliphatic tail that is either saturated or unsaturated [22], depending on the presence of double bounds in the R-group. Acids with one double bound are known as ‘mono-enoic’, those with two as ‘di-enoic’, and so on [27].
Fatty acids are structurally diverse and contain distinct classes that are defined at the molecular level, based on the degree of branching, the number and position of double bonds, the chain length, the
The major groups of fatty acids are: a) straight chain, b) branched chain, c) unsaturated, and d) cyclopropane. Straight chain fatty acids are found elsewhere in nature (e.g., C12, C14, C16, C18 and C20). However, the corresponding β− hydroxymyristic acid 3-OH and C12 are not normally found in higher organisms, but are common components of the boundary of lipids present in the walls of gram-negative bacteria. Branched fatty acids comprise two types: the iso-form (the methyl group is located on the penultimate carbon atom) and the anteiso (the methyl group is located in the antepenultimate carbon atom). The unsaturated acids found in bacteria are monounsaturated, whereby the double bound is most frequently found between carbon 11 and 12. The cyclopropane fatty acids - rarely found in higher organisms - are frequently encountered in bacteria. The biosynthetic precursors of these acids are the corresponding monounsaturated fatty acids; as a consequence, the major example is the cis-11-12 methylene hexadecanoid acid [21]. Table 1 contains some examples of fatty acids commonly found in bacteria.
|
|
|
|
|
|||
C10 H20 O2 | C16:0 | Capric | Decanoic |
C12 H24 O2 | C12:0 | Lauric | Dodecanoic |
C14 H28 O2 | C14:0 | Myristic | Tetradecanoic |
C16 H32 O2 | C16:0 | Palmitic | Hexadecanoic |
C17 H34 O2 | C17:0 | Margaric | Heptadecanoic |
C18 H36 O2 | C18:0 | Stearic | Octadecanoic |
C20 H40 O2 | C20:0 | Arachidic | Eicosadecanoic |
|
|||
C16 H30 O2 | C16:1ω9 | Palmitoleic | Hexadec-9-enoic |
C18 H34 O2 | C18:1ω9 | Oleic | Octadec-9-enoic |
2.2. Nomenclature of fatty acids
Fatty acids are designated by the total number of carbon atoms followed by the total number of double bonds (e.g., a 16 carbon alkanoic acid is 16:0), beginning with the position of the double bound closest to the methyl-end (
2.3. Analysis of fatty acids from photosynthetic bacteria
Numerous papers have been published about the influence of the culture media in growing bacterial cells as well as the salinity in the bacteria fatty acid compositions. These have been done especially in heterotrophic bacteria, and it has been observed that when
The analysis of salinity effects on the fatty acid composition of photosynthetic bacteria has been done in PPSB, such as
The age of the cells is another factor that may change the fatty acid composition of bacteria as well as the cells of all living organisms. In many techniques, it has been suggested that it is very important to use bacterial cells of the same age for fatty acid analysis, especially for chemotaxonomical purposes.
In order to study the influence of MgSO4 and NaCl and the age of the cells in the fatty acid composition of GPSB and PPSB, respectively, the bacterial strains included in Table 2 were used. This table contains the origin, the phenotypical characteristics and optimal culture conditions (NaCl) of the microorganisms.
|
For all the experiment, two wild strains were used: a PPSB strain T9s642 (
For culturing these bacteria, a basal medium enriched with water samples was used. This was also used for the isolation and growth of these photosynthetic bacteria and contained the following: distilled water 950 ml, KH2PO4 1.0 g, NH4Cl 0.50 g, MgSO4.7H2O 0.40 g, CaCl2.2H2O 0.50 g, and NaCl 2.0% (only for marine strains). It was sterilized by autoclave and, once cooled, was supplemented with a 1.0 mL SL10 solution (GPSB) and SL12 (PPSB), Vitamin B12 1.0 mL (2.0 mg/100 mL distilled water), and 30 mL of sodium bicarbonate solution 5% [30]. 6.0 mL and 10.0 mL of Na2S.9H2O 5% (v/v distilled water) were added as an electron donor for
2.3.1. Influence of MgSO4 and NaCl on cultures of GPSB
The influence of MgSO4 and NaCl on cultures of GPSB (T11s) were observed by growing the bacteria in the basal medium, as described before, and modified as follows: condition T11S = NaCl (2.0%) and MgSO4.7H2O 0.3% g; condition C11S = NaCl (0.0%), MgSO4.7H2O 0.04% g; and condition MG11S = NaCl (0.0%) and MgSO4.7H2O 0.3% g, respectively. Conditions T11S and C11S are optimal for marine and freshwater GPSB, respectively. In all cases, the pH was adjusted to 6.5 using a diluted H2S sterilized solution. Strains of GPSB, DSMZ249 and DSMZ 266 were used as references, and they were cultured under the condition C11S (optimal for freshwater strains).
2.3.2. Influence of cell age on the fatty acid composition of PPSB
In order to investigate the influence of bacterial cell age on the fatty acid composition of PPSB, a wild strain of
All the bacteria cultures (green and purple) were grown in 1.5 L glass flasks, the temperature of incubation was 23ºC and, as the light source, bulbs of incandescent (for
The mass cultures of GPSB and PPSB were obtained by adding a previously sterilized and neutralized solution of Na2S.9H2O. It was added to the cultures when the sulphur source (electron donor) was depleted, which was detected using an acetate paper pH tester. Cultures were grown for 15 days (with the exception of
2.3.3. Fatty acid extraction and analysis by GC and GC-MS
The procedure for total fatty acid analysis has been described previously in [7], and the lyophilized cells of GPSB and PPSB (250 mg and 500 mg, respectively) were used for fatty acid extraction by saponification followed by diazomethane derivation. The resulting FAMEs were identified using a standard methyl ester mixture and the final identification was confirmed using GC and MS (GC-MS). Cell lipids from each sample were saponified by adding 2.0 mL benzene and 8.0 mL KOH solution (5.0 g/100 mL methanol), containing 5% (w/v) under a temperature of 80°C (using a cover bath), over four hours. Once the sample was cooled to room temperature, it was acidified to pH = 1 with a H2SO4 solution (20% v/v).
FAMEs were prepared by adding to each sample 2.0 g N-Nitroso-N-methylurea (Sigma) dissolved in a pre-cooled solution of 30.0 mL diethyl ether, 2.0 g KOH and 6.0 mL distilled water. This mixture was stirred for 5-10 minutes and the supernatant was removed and placed in a new tube containing KOH pellets cooled on ice. Finally, diazomethane was added and the dried lipids were achieved within 10-20 min and the content was evaporated at 40°C in a water bath.
The FAMEs were analysed by injecting 2.0 µL of the sample, previously dissolved with n-hexane (0.04-1.0 mL), in a HP-5890A gas chromatograph equipped with a flame ionization detector and a silica capillary column (15 m x 0.25 mm I.D.) with cross-linked methyl silicone (HP-1, Hewlett-Packard). The column was programmed from 175°C to 300°C within 15 minutes. The injector and detector temperature were 275°C and 300°C, respectively. Helium was used as a carrier gas with a flow rate of approximately 1.0 mL/min, and the split ratio was approximately 1:50. Finally, a HP3396 integrator was used for the chromatogram integration and the identification of the FAMEs was done by comparing the retention time of each fatty acid, using a standard mixture of FAMEs.
For the GC-MS analysis, an HP-5890 gas chromatograph attached to a HP5989X quadripole mass spectrometer was used with a methyl polysiloxane column TRB1 (30 m). The injector and detector temperatures were both 225°C, and two ramps were used: one from the initial temperature 10°C/min to 240°C and the other with 40°C/min to 270°C. The injection mode was splitless.
The standard deviations and means were calculated based on the integration areas of the fatty acid peaks.
3. Results
3.1. Influence of the MgSO4 and NaCl cultures on GPSB
Strain T11S was isolated from superficial water samples from Tampamahoco lagoon (Veracruz, México). One of the characteristics of this bacterium is that it is able to tolerate physical and chemical environmental changes. For this reason, it was selected to investigate the changes in fatty acid composition due to salinity (NaCl and MgSO4). However, no changes of the fatty acid profile have been observed as a response to NaCl and MgSO.7H2O changes. In all the strains analysed, 12 fatty acids comprising saturated, unsaturated, branched and cyclic acids were detected, as has been reported previously [7].
All the fatty acids detected in the GPSB had chains with no more than 18 carbons (Table 2). In the
Wild and reference strains of
All the strains were incubated in similar physical (temperature and illumination) conditions, but specific culture conditions were used for each one. The culture medium for DSMZ266 and DSMZ249 was the same as with C11S (this is without NaCl and 0.04 g MgSO4.7H2O), but it is evident that the condition C11S conserves the same fatty acid pattern as T11S and MG11S.
The collection strains have less saturated fatty acids than T11S, while MG11S and C11S have similar quantities of these fatty acids; inversely, the collection strains have more unsaturated fatty acids than the experimental cultures (T11S, MG11S and C11S). It is very important to note that the branched fatty acids recorded were similar to all the strains cultured in the same conditions (DSMZ266, DSMZ249 and C11S); it is evident that the bacterium of marine origin (T11S) cultured in optimal conditions produced more branched fatty acids than the strains cultured in freshwater conditions as in DSMZ266 and DSMZ249. It has been pointed out that the presence of branched chain fatty acids confers to the membrane a greater degree of flexibility [31].
The cyclic fatty acid was present in greater quantities in DSMZ249 than in DSMZ266 and T11S. When there was an increase in NaCl or Mg salts, the production of C17Cy fatty acid decreased too. It is evident that in optimal conditions for T11S, there was less production of C17Cy fatty acid, so the presence of this fatty acid is as follows: MG11S>C11S>T11S. Cyclopropane acid production in cells is a mechanism for preserving membrane integrity, preventing the formation of abnormal structures [32].
The values of the standard deviation for each fatty acid of T11S, MG11S and C11S were between 0.009 and 1.828, which is evidence that the changes in the fatty acid compositions of
3.2. Influence of the culture age (20 and 30 days of growth) on the fatty acids composition of PPSB
It has been proposed that cell age is among the factors that affect the fatty acid compositions of living organisms. The influence of this factor in the fatty acid composition of bacterial cells has been studied in heterotrophic bacteria, and cultures of 24 and 48 hours incubation have been proposed as the optimal age (Microbial Identification System) for the fatty acid analysis of these bacteria. However, the exponential phase has been proposed for fatty acid analysis in photosynthetic bacteria [33]. In addition, stationary or low stationary phases, after three and six days of growth, have been indicated too [34]. Nevertheless, and frequently, the age of the cells that they used for fatty acid analysis was not mentioned.
In the present experiment, the cells of two strains of PPSB from marine origin were used. For fatty acid analysis, the cells of these bacteria were collected after 15, 20 and 30 days of growth in optimal conditions according to their origins. They were also incubated under the same light and temperature conditions. The results of the fatty acid analysis of
The fatty acid analysis of these bacteria revealed the presence of nine of these compounds. All these fatty acids have been reported before for members of the Chromatiaceae family [7, 9]. The major fatty acids were C18:1, C16:1 and C16:0 and less quantities of: C12:0, C14:0 and C17:0, C18:0 and C20:1. These conformed between 92% and 93% of the total compounds extracted from the cells of two
|
There were no qualitative changes in the fatty acid compositions of DSMZ4395 and T9s642 due to cell ages, and the quantitative changes were minimal: both strains conserved the fatty acid pattern that it is characteristic for members of the Chromatiaceae family, but strain DSMZ4395 produced almost the same quantities of C16:0 (16.2-16.8%) and C16:1 (17.5-18.2%), which is characteristic of halophilic microorganisms like
On the other hand, in the wild
The influence of age on the fatty acid compositions of bacteria has also been studied in microorganisms like
The changes in branched fatty acids, such as iC15:0 and C15:0 (e. g , increases and decreases, respectively), are the result of aged cells in a strain of
3.3. Uses of fatty acids analysis (other than chemotaxonomy)
Two goals of chemotaxonomy are to measure the number of changed molecules as a descriptor of the chemical relevance of two bacteria and also to provide a list of changed molecules to discover biomarkers [39].
Bacteria contain lipids in concentrations of 0.2-50% of dry weight, and for fatty acid analysis lipid compositions are important. These are mainly: phospholipids (structural elements of the cell membrane), glycolipids (elements of cell membrane structures but less common than phospholipids; abundant in Actinomycetes), lipid A (present in the outer membrane of gram-negative bacteria; part of the lipopolysaccharides) and lipoteichoic acids (present in gram-positive bacteria) [2].
Profiles of fatty acids have been used to distinguish pathogenic bacteria species for fish, like the genus
The presence of bacteria in sponges has been detected because they produce large quantities of iso-, anteiso-cyclopropyl- and monomethyl-branched fatty acids. Using fatty acid analysis, it is possible to distinguish different symbionts (photosynthetic and non-photosynthetic) present in marine sponges and provide estimates of bacterial symbiont abundances [41].
Special fatty acids from phospholipids have been used for characterizing bacteria and photosynthetic life forms. Fatty acids linked to these molecules in the members of Chromatiaceae and Ectothiorhodospiraceae were analysed, and it is evident that the fatty acid pattern does not change. As has been indicated before, these compounds have great value in determining bacterial phylogeny, providing a useful set of features for characterizing strains, and they give important information about microbial communities in environmental samples.
Phospholipid fatty acids could be used as biomarkers because they degrade rapidly after cell death and are not present in storage lipids or in anthropogenic contaminants. Bacteria contain phospholipids as relatively constant proportions in their biomass [41], and with these it is possible to estimate the microbial biomass in environmental samples where the bacteria of subsets in microbial communities contain specific signature fatty acids in their phospholipids [42]. Using phospholipid fatty acids (as methyl esters) analysis, it is possible to measure attributes or microbial communities, such viable biomass and microbial structures as well as nutritional and physiological status [41, 43]; these compounds, as well as bacterial fatty acid ratios, have been used to disclose bacterial connections in the marine food web and their importance in supplying material and energy to the higher trophic levels [44].
In addition, lipids have been used to establish possible links between modern and ancient microbial communities and to add to the understanding of the evolutionary histories of the organisms in the various environments. The analysis of phospholipids provides information about the viable biomass and biological diversity, and on the other hand information about the glycolipids of the activity of photosynthetic microorganisms in the environment. In addition, sterols and hopanoids - which are better preserved in the geological records - offer insights into the presence of microorganisms in paleoenvironments [45]. In bacterial membranes, the fatty acids of phospholipids are linked by ester bonds to glycerol and form a phospholipid bilayer, while archaeal membranes have phospholipids containing two polar heads linked by isoprenoid chains and ether linkages to glycerol [44]. As such, these linkages are markers for detecting archaeal bacteria.
3.4. Lipidomics studies: some examples
Lipidomics has been applied in physiological studies, such as the change in the lipidomic profiling of
Lipidomics has revealed that under cold stress,
In addition, lipidomics have been applied to the understanding of the lipogenesis of free fatty acids from the symbiosis between cnidarian-dinoflagellate [26] as well as the study of the lipidomics of human pathogenic mycobacteria. It is possible to get the lipidomics datasets to assess lipid changes during infection or else among clinical strains of mycobacteria tuberculosis [39].
4. Conclusions
As was mentioned before, the influence of NaCl in the culture medium increases the concentration of the saturated fatty acids C16:0 and decreases the production of the unsaturated C16:1 and C18:1. The presence in the culture medium of both MgSO4 and NaCl reduces the production of the saturated fatty acids C14:0 and C18:0 and increases the production of the unsaturated C16:1 and C18:1. The change of the relative abundances of the fatty acids due to the changes of MgSO4 and NaCl in the culture media of
Although advances in the technologies for fatty acid analysis have been reported, the isolation and culturing of novel strains as well as the fatty acid analysis of photosynthetic prokaryotes remains scarce, and it is very important to encourage the investigation of these microorganisms. With new sources of genetic materials from photosynthetic bacteria and the application of new technologies - for example lipidomics - which are more precise, it will be possible to discover new fatty acid structures and to evaluate the sources of these compounds of biotechnological interest and novel chemotaxonomic biomarkers. In addition, the physiological role of fatty acids in the cell membranes of photosynthetic bacteria and their role in environmental trophic chains could be explored.
Acknowledgments
We thank the Universitat Autónoma de Barcelona (UAB), Spain, where all the experimental elements of the present work were performed with academic and technical support from Doctors Marina Luquin, Jodi Mas and Manuel Muñoz. Financial support from the Consejo Nacional de Ciencia y Tecnología (CONACyT, México) and the Universidad Autónoma Metropolitana-Xochimilco are gratefully acknowledged.
References
- 1.
Gupta RS, Mukhtar T, and Singh B. Evolutionary relationships among photosynthetic prokaryotes ( Heliobacterium chlorum ,Chloroflexus aurantiacus , Cyanobacteria,Chlorobium tepidum and Proteobacteria): implications regarding the origin of Photosynthesis. Molecular Microbiology 1999; 32(5) 893-906. DOI: 10.1046/j.1365-2958.1999.01417.x. - 2.
Janse JD, 1992 Whole cell fatty acid analysis as a tool for classification of phytopathogenic pseudomonas bacteria PhD Thesis. p. 121 http://Library.wur.nl/WebQuery/clc/338144 accessed in 08 08 2013 - 3.
Imhoff JF, Caumette P. Recommended standards for the description of new species of anoxygenic phototrophic bacteria. International Journal Systematic and Evolutionary Microbiology 2004; 54(4) 1415-1421. DOI: 10.1099/ijs.0.03002-0. - 4.
Tindall BJ, Rosselló-Móra R, Busse HJ, Ludwig W, and Kampfer P. Notes on the characterization of prokaryote strains for taxonomic purposes. International Journal of Systematic and Evolutionary Microbiology 2010; 60(1) 249–266. DOI: 10.1099/ijs.0.016949-0. - 5.
Knudsen E, Jantzen E, Bryan K, Ormerod JG, and Sirevag R. Quantitative and structural characteristics of lipids in Chlorobium andChloroflexus . Archives of Microbiology 1982; 132(2) 149-154. http://link.springer.com/article/10.1007/BF00508721. - 6.
Kenyon CN, Gray AM. Preliminary analysis of lipids and fatty acids of Green Bacteria and Chloroflexus aurantiacus . Archives of Microbiology 1974; 120(1) 131-178. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC245741/pdf/jbacter00334-0147.pdf. - 7.
Núñez-Cardona, MT (2012). Fatty acids analysis of photosynthetic sulfur bacteria by gas chromatography. Gas chromatography-Biochemicals, Narcotics and Essential Oils. In Tech Publications, 117-138. http://cdn.intechopen.com/pdfs/31528/InTech-Fatty_acids_analysis_of_photosynthetic_sulfur_bacteria_by_gas_chromatography.pdf. - 8.
Caudales R, Wells J. Differentiation of Free-Living Anabaena andNostoc Cyanobacteria on the basis of fatty acid composition. International Journal of Systematic Bacteriology 1992; 42(2) 246-251. DOI: 10.1099/00207713-42-2-246. - 9.
Núñez-Cardona MT, Donato-Rondon CCh, Reynolds CS, Mas J. A purple sulfur bacterium from a high-altitude lake in the Colombian Andes." Journal of Biological Research. Thessalon 9 2008; 17-24. http://www.jbr.gr. - 10.
Bryantseva IA, Tourova TP, Kovaleva OL, Kostrikina NA, and Gorlenko VM. Ectothiorhodospira magna sp. nov., a new large alkaliphilic purple sulfur bacterium. Microbiology 2010; 79(6) 780-790. - 11.
Walcott R, Langston D, Sanders F, and Gitaitis R. Investigating Intraspecific Variation of Acidovorax avenae subsp.citrulli using DNA fingerprinting and whole cell fatty acid analysis. Phytopathology 2000; 90(2) 191-196. http://dx.doi.org/10.1094/PHYTO.2000.90.2.191. - 12.
Tighe SW, De Lajudie P, Dipietro K, Lindström K, Nick G, and Jarvis B. Analysis of cellular fatty acids and phenotypic relationships of Agrobacterium ,Bradyrhizobium, Mesorhizobium ,Rhizobium and Sinorhizobium species using the Sherlock Microbial Identification System. International Journal of Systematic and Evolutionary Microbiology 2000; 50(2) 787–801. DOI: 10.1099/00207713-50-2-787. - 13.
Moss C, Lambert M, and Merwin W. Comparison of Rapid Methods for Analysis of Bacterial Fatty Acids. Applied Microbiology 1974; 28(1) 180-185. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC186596/pdf/applmicro00013-0102.pdfhttp://aem.asm.org/content/28/1/80.short. - 14.
De Gelder J. Raman spectroscopy as a tool for studying bacterial cell compounds PhD in Sciences Chemistry Universiteit Gent. 2008. http://hdl.handle.net/1854/LU-472114. Accessed in 03 08 2013. - 15.
Fenselau C. Mass spectrometry for characterization of microorganisms an overview. ACS Symposium Series. American Chemical Society: Washington DC. 1995 Chapter 1; 1-6 http://pubs.acs.org/doi/pdf/10.1021/bk-1994-0541.ch001. - 16.
Bastida F, Kandeler E, Moreno JL. Ros M, Garcıa CA, and Hernandez T. Application of fresh and composted organic wastes modifies structure, size and activity of soil microbial community under semiarid climate. Journal of Analytical and Applied Pyrolysis 2005; 73 69–75. DOI:10.1016/j.apsoil.2008.05.007. - 17.
Kunitsky, C., Osterhout G, and Sasser M. Identification of microorganisms using fatty acid methyl ester (FAME) analysis and the MIDI Sherlock Microbial Identification System. Encyclopedia of rapid microbiological methods 2006; 3: 1-18. - 18.
Bories C, Rimbault A, and Leluan G. Simplified gas chromatographic procedure for identification and chemotaxonomy of anaerobic bacteria. Annals Institute Pasteur/Microbiol. Microbiology 1987; 138, 587-592. http://www.sciencedirect.com/science/article/pii/0769260987900445. - 19.
Brondz, I, Olsen, I. Microbial chemotaxonomy: chromatography, electrophoresis and relevant profiling techniques. Journal of Chromatography B: Biomedical Sciences and Applications 1986: 379 367-411. http://www.ncbi.nlm.nih.gov/pubmed/2426294. - 20.
Akotoa L, Pelb R, Irtha H, Brinkmana U ATh., Rene, and Vreuls RJJ. Automated GC–MS analysis of raw biological samples Application to fatty acid profiling of aquatic micro-organisms. Journal of Analytical and Applied Pyrolysis. 2005; 73(1) 69–75. DOI:10.1016/j.jaap.2004.11.006. - 21.
Shaw, N. Lipid Composition as a Guide to the Classification of Bacteria. Advances in Applied Microbiology 1974; 17: 63. - 22.
Khalil BM, Hou W, Zhou H, Elisma F, Swayne LA, Blanchard AP, Yao Z, Bennett SAL, and Figeys D. Lipidomics era: Accomplishments and challenges. Mass Spectrometry Reviews 2010; 29(6) 877-929. DOI: 10.1002/mas.20294. - 23.
Piotrowska-Seget Z, Mrozik A. Signature Lipid biomarker (SLM) analysis in determining changes in community structure of soil microorganisms. Polish Journal of Environmental Studies 2003 12(6); 669-675, http://www.pjoes.com/pdf/12.6/669-675.pdf. - 24.
Russell N, Nichols D. Polyunsaturated fatty acids in marine bacteria–a dogma rewritten. Microbiology 1999; 145(4) 767-779. DOI: 10.1099/13500872-145-4-767. - 25.
Yang S, Lee J-H, Ryu J-S, Kato Ch, Sang-Jin, Kim S-J. Shewanella donghaensis sp. nov., a psychrophilic, piezosensitive bacterium producing high levels of polyunsaturated fatty acid, isolated from deep-sea sediments. International Journal of Systematic and Evolutionary Microbiology 2007; 57 208–212. DOI: 10.1099/ijs.0.64469-0 - 26.
Dunn SR, Thomas MC, Nette GW, and Dove SG. A lipidomic approach to understanding free fatty acid lipogenesis derived from dissolved inorganic carbon within cnidarian-dinoflagellate symbiosis. PloS one 2012; 7(10) e46801. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0046801 - 27.
Hawker LE, Linton AH. Microorganisms function, form and environment 1971 pp. 727 P. London UK, Edward Arnold Ltd. ISBN 7131-2278-1. - 28.
Marr AG, Ingrahan JL. Effect of temperature on the composition of fatty acids in Escherichia coli . Journal of Bacteriology 1962; 84 1262-1267. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC278056/pdf/jbacter00464-0150.pdf. - 29.
Imhoff, JF, Thiemann. B. Influence of salt concentration and temperature on the fatty acid compositions of Ectothiorhodospira and other halophilic phototrophic purple bacteria. Archives of Microbiology 1991; 156 (5) 370-375. http://link.springer.com/article/10.1007/BF00248713#page-1. - 30.
Pfennig N, Trüper HG. Isolation of Members of the families Chromatiaceae and Chlorobiaceae. Springer Verlag 1981. - 31.
Cho K, and Salton M. Fatty acid composition of bacterial membrane and wall lipids. Biochimica. Biophysica Acta 1966; 116(1) 73-79. http://www.sciencedirect.com/science/article/pii/0005276066900932. - 32.
Valderrama M, Monteoliva-Sánchez M, Quesada E, and Ramos-Comenzana A. Influence of salt concentration of the cellular fatty acid composition of the moderately halophilic bacteria Halomonas salina . Research in Microbiology 1998; 149(9) 675-679. http://dx.doi.org/10.1016/S0923-2508(99)80015-1. - 33.
Imhoff JF. Lipids, fatty acids and quinones in taxonomy and phylogeny of anoxygenic phototrophic bacteria, In Green Photosynthetic Bacteria. Plenum Press.1988 http://link.springer.com/chapter/10.1007%2F0-306-47954-0_10#page-1. - 34.
Kenyon CN. Fatty acid composition of unicellular strains of blue-green algae. Journal of Bacteriology 1972; 109(2): 827-834 http://jb.asm.org/content/109/2/827.short. - 35.
Sorokin DY, Tourova TP, Muyzer G, and Kuenen GJ. Thiohalospira halophila gen. nov., sp. nov. andThiohalospira alkalphila sp. nov., novel obligately chemolithoautotrophic, halophilic, sulfur-oxidizing gammaproteobacteria from hypersaline habitats. International Journal of Systematic and Evolutionary Microbiology 2008; 58 1685–1692. DOI: 10.1099/ijs.0.65654-0. - 36.
Sorokin DY, Tatjana P. Tourova, Gesche Braker, and Gerard Muyzer G. Thiohalomonas denitrificans gen. nov., sp. nov. and Thiohalomonas nitratireducens sp. nov., novel obligately chemolithoautotrophic, moderately halophilic, thiodenitrifying Gammaproteobacteria from hypersaline habitats. International Journal of Systematic and Evolutionary Microbiology 2007; 57: 1582–1589. DOI: 10.1099/ijs.0.65112-0. - 37.
Law JH, Zalkin H, and Kaneshiro T. Transmethylation reactions in bacterial lipids. Biochimica et Biophysica Acta (BBA)-Specialized Section on Lipids and Related Subjects 1963; 70 143-151. http://www.sciencedirect.com/science/article/pii/0006300263907340. - 38.
Hack SK, Garchow H, Odelson DA, Forney LJ, and Klug MJ. Accuracy, reproducibility, and interpretation of fatty acid methyl ester profiles of model bacterial communities. Applied and Environmental Microbiology 1994; 60(7) 2483-2493. http://pubmedcentralcanada.ca/pmcc/articles/PMC201674/pdf/aem00024-0287.pdf. - 39.
Layre E, Sweet L, Hong S, Madigan CA, Desjardins D, Young DC, Cheng T-Y, Annand J-W, Kim K, Shamputa IC, McConnell MJ, Debono A, Behar SM, Minnaard AJ, Murray M, Barry CE, Matsunaga I, and Moody DB. Comparative Lipidomics Platform for Chemotaxonomic Analysis of Mycobacterium tuberculosis. Chemistry and Biology 2011; 18 1537–1549. DOI 10.1016/j.chembiol.2011.10.013. - 40.
Piñeiro-Vidal M, Pazos F, and Santo Y. Fatty acid analysis as a chemotaxonomic tool for taxonomic and epidemiological characterization of four fish pathogenic Tenacibaculum species Letters in Applied Microbiology 2008; (5): 548–554, DOI:10.1111/j.1472-765X.2008.02348.x. - 41.
Guillan FT, Soilov IL, Thompson JE, Hogg RW, Wilkinson CR, and Djerassi C. Fatty acid as biological markers for bacterial symbionts in sponges 1988; 23(1) 1139-1135. http://link.springer.com/article/10.1007/BF02535280 - 42.
Ahmad A, Gharaibeh, and Kent J. Voorhees. Characterization of lipid fatty acids in whole-cell microorganisms using in situ supercritical fluid derivatization/extraction and Gas Chromatography/Mass Spectrometry. Analytical Methods 1996; 68(17) 2805–2810. DOI: 10.1021/ac9600767. - 43.
Tunlid A, Hoitink HAJ, Low C, and White DC. Characterization of bacteria that suppress Rhizoctonia damping-off in bark compost media by analysis of fatty acid biomarkers. Applied and Environmental Microbiology 1989; 55(6)1368-1374. http://aem.asm.org/content/55/6/1368.short. - 44.
De Carvalho, Caramujo. Lipids of prokaryotic origin at the base of marine food webs. Marine Drugs 2012; 10 2698-2714; DOI:10.3390/md10122698. www.mdpi.com/journal/marinedrugs. - 45.
Fang J, Chan O, Joeckel RM, Huang Y, Wang Y, Bazylinski DA, Moorman TB, and Clement BJ. Biomarker analysis of microbial diversity in sediments of a saline groundwater seep of Salt Basin, Nebraska. Organic Geochemistry 2006; 37(8) 912–931. DOI:10.1016/j.orggeochem.2006.04.007. - 46.
Lu N, Weia D, Chena F, and Yang ST. Lipidomic profiling reveals lipid regulation in the snow alga Chlamydomonas nivalis in response to nitrate or phosphate deprivation. European Journal of Lipid Science and Technology 2012; 114(3) 253-265. http://dx.doi.org/10.1016/j.procbio.2013.02.028. - 47.
Su X, Xu J, Yan X, Zhao P, Chen J, Zhou Ch, Zhao F, and Li S. Lipidomic changes during different growth stages of Nitzschia closterium f. minutissima . Metabolomics 2013; 9 300–310. DOI: 10.1007/s11306-012-0445-1. - 48.
Chen D, Yan X, Xu J, Su X, and Li L. Lipidomic profiling and discovery of lipid biomarkers in Stephanodiscus sp. under cold stress. Metabolomics 2013; 9 949-959 doi:10.1007/s11306-013-0515-z.