Syntrophy

In biology, syntrophy, synthrophy,[1] or cross-feeding (from Greek syn meaning together, trophe meaning nourishment) is the phenomenon of one species living off of the products of another species. In this type of biological interaction, the growth of one partner depends on the nutrients, growth factors, or substrates provided by the other partner. Jan Dolfing describes syntrophy as "the critical interdependency between producer and consumer".[2] This term for nutritional interdependence is often used in microbiology to describe this symbiotic relationship between bacterial species.[3][4] Morris et al. have described the process as "obligately mutualistic metabolism".[5]

Microbial syntrophy

Syntrophy plays an important role in a large number of microbial processes.

The defining feature of ruminants, such as cows and goats, is a stomach called a rumen. The rumen contains billions of microbes, many of which are syntrophic. One excellent example of this syntrophy is interspecies hydrogen transfer. Some anaerobic fermenting microbes in the rumen (and other gastrointestinal tracts) are capable of degrading organic matter to short chain fatty acids, and hydrogen. The accumulating hydrogen inhibits the microbe's ability to continue degrading organic matter, but syntrophic hydrogen-consuming microbes allow continued growth by metabolizing the waste products. In addition, fermentative bacteria gain maximum energy yield when protons are used as electron acceptor with concurrent H2 production. Hydrogen-consuming organisms include methanogens, sulfate-reducers, acetogens, and others. Some fermentation products, such as fatty acids longer than two carbon atoms, alcohols longer than one carbon atom, and branched-chain and aromatic fatty acids, cannot directly be used in methanogenesis. In acetogenesis process, these products are oxidized to acetate and H2 by obligated proton reducing bacteria in syntrophic relationship with methanogenic archaea as low H2 partial pressure is essential for acetogenic reactions to be thermodynamically favorable (ΔG < 0).[6]

The number of bacterial cells that live on or in the human body, for example throughout the alimentary canal and on the skin, is in the region of 10 times the total number of human cells in it.[7] These microbes are vital, for instance for the digestive and the immune system to function.[8]

Another example is the many organisms that feed on faeces or dung. A cow diet consists mainly of grass, the cellulose of which is transformed into lipids by micro-organisms in the cow's large intestine. These micro-organisms cannot use the lipids because of lack of oxygen in the intestine, so the cow does not take up all lipids produced. When the processed grass leaves the intestine as dung and comes into open air, many organisms, such as the dung beetle, feed on it.

Yet another example is the community of micro-organisms in soil that live off leaf litter. Leaves typically last one year and are then replaced by new ones. These micro-organisms mineralize the discarded leaves and release nutrients that are taken up by the plant. Such relationships are called reciprocal syntrophy because the plant lives off the products of micro-organisms. Many symbiotic relationships are based on syntrophy.

Biodegradation of pollutants

Syntrophic microbial food webs can play an integral role in the breakdown of organic pollutants such as oils, aromatic compounds, and amino acids.[9][10][11]

Environmental contamination with oil is of high ecological importance, but can be mediated through syntrophic degradation.[9] Alkanes are hydrocarbon chains that are the major chemical component of crude oils, and have been experimentally verified to be broken down by syntrophic microbial food webs.[9] The hydrocarbons of the oil are broken down after activation by fumarate, a chemical compound that is regenerated by other microorganisms.[9] Without regeneration, the microbes degrading the oil would eventually run out of fumarate and the process would cease. This breakdown is crucial in the processes of bioremediation and global carbon cycling.[9]

Syntrophic microbial communities are key players in the breakdown of aromatic compounds, which are common pollutants.[10] The degradation of aromatic benzoate to methane produces many intermediate compounds such as formate, acetate, CO
2 and H2.[10] The build up of these products makes benzoate degradation progressively less favourable. These intermediates can then be taken up and metabolized syntrophically by methanogens to make the whole process more thermodynamically favourable.[10]

Studies have shown that bacterial degradation of amino acids can be significantly enhanced through the process of syntrophy.[11] Microbes growing poorly on amino acid substrates alanine, aspartate, serine, leucine, valine, and glycine can have their rate of growth dramatically increased by syntrophic H2 scavengers. These scavengers, like Methanospirillum and Acetobacterium, metabolize the H2 waste produced during amino acid breakdown, preventing a toxic build-up.[11] Another way to improve amino acid breakdown is through interspecies electron transfer mediated by formate. Species like Desulfovibrio employ this method.[11]

Metabolic mechanism

The main motive behind a syntrophic relation between two bacterial organisms is generalized as a relationship where each participant's metabolic activity cannot independently overcome the thermodynamic pressure of the reaction under standard conditions even when a cosubstrate or nutrient is added into the environment. Therefore, the cooperation of the other participant is required to reduce the intermediate pool size.[12]

The Methanobacillus omelianskii culture is a classic example in demonstrating how two separate unfavourable reactions can be carried out by syntrophic interactions.[13] Organism S and organism M.o.H of Methanobacillus omelianskii oxidize ethanol into acetate and methane by a process called interspecies hydrogen transfer. Individuals of organism S are observed as obligate anaerobic bacteria that use ethanol as an electron donor, whereas M.o.H (Methanobacterium bryantii strain M.o.H) are methanogens that oxidize hydrogen gas to produce methane.[1][14] These two metabolic reactions can be shown as follows:

Organism S: 2 CH3CH2OH + 2 H2O → 2 CH3COO− + 2 H+ + 4 H2 (ΔG°' = +19 kJ)
Strain M.o.H.: 4 H2 + CO
2 → CH4 + 2 H2O (ΔG°' = -131 kJ)[12][15]

Complex organic compounds such as ethanol, propionate, butyrate, and lactate cannot be directly used as substrates for methanogenesis by methanogens. On the other hand, fermentation of these organic compounds cannot occur in fermenting microorganisms unless the hydrogen concentration is reduced to a low level by the methanogens.[6] In this case, hydrogen, an electron-carrying compound (mediator) is transported from the fermenting bacteria to the methanogen through a process called mediated interspecies electron transfer (MIET), where the mediator is carried down a concentration gradient created by a thermodynamically favourable coupled redox reaction.[16]

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References
  1. Wang, Lawrence; Ivanov, Volodymyr; Tay, Joo-Hwa; Hung, Yung-Tse (5 April 2010). Environmental Biotechnology Volume 10. Springer Science & Business Media. p. 127. ISBN 978-1-58829-166-0. Retrieved 3 March 2015.
  2. Dolfing, Jan (2014-01-01). "Syntrophy in microbial fuel cells". The ISME Journal. 8 (1): 4–5. doi:10.1038/ismej.2013.198. ISSN 1751-7362. PMC 3869025. PMID 24173460.
  3. Microbiology, by Prescott, Harley & Klein 6th edition
  4. Henderson's Dictionary of Biology, by Eleanor Lawrence, 14th edition
  5. Morris, Brandon E.L.; Henneberger, Ruth; Huber, Harald; Moissl-Eichinger, Christine (2013). "Microbial syntrophy: interaction for the common good". FEMS Microbiol Rev. 37 (3): 384–406. doi:10.1111/1574-6976.12019. PMID 23480449.
  6. Stams, Alfons J. M.; De Bok, Frank A. M.; Plugge, Caroline M.; Van Eekert, Miriam H. A.; Dolfing, Jan; Schraa, Gosse (1 March 2006). "Exocellular electron transfer in anaerobic microbial communities". Environmental Microbiology. 8 (3): 371–382. doi:10.1111/j.1462-2920.2006.00989.x. PMID 16478444.
  7. Crazy Way Microbes Colonize, Control The Human Body interview with Dr. Justin Sonnenburg, assistant professor of microbiology and immunology at Stanford University School of Medicine
  8. Microbes and the human body The Microbiology Society online
  9. Callaghan, A. V.; Morris, B. E. L.; Pereira, I. a. C.; McInerney, M. J.; Austin, R. N.; Groves, J. T.; Kukor, J. J.; Suflita, J. M.; Young, L. Y. (2012-01-01). "The genome sequence of Desulfatibacillum alkenivorans AK-01: a blueprint for anaerobic alkane oxidation". Environmental Microbiology. 14 (1): 101–113. doi:10.1111/j.1462-2920.2011.02516.x. ISSN 1462-2920. PMID 21651686.
  10. Ferry, J. G.; Wolfe, R. S. (February 1976). "Anaerobic degradation of benzoate to methane by a microbial consortium". Archives of Microbiology. 107 (1): 33–40. doi:10.1007/bf00427864. ISSN 0302-8933. PMID 1252087.
  11. Zindel, U.; Freudenberg, W.; Rieth, M.; Andreesen, J. R.; Schnell, J.; Widdel, F. (1988-07-01). "Eubacterium acidaminophilum sp. nov., a versatile amino acid-degrading anaerobe producing or utilizing H2 or formate". Archives of Microbiology. 150 (3): 254–266. doi:10.1007/BF00407789. ISSN 0302-8933.
  12. Schink, B. (1997-06-01). "Energetics of syntrophic cooperation in methanogenic degradation". Microbiology and Molecular Biology Reviews. 61 (2): 262–280. doi:10.1128/.61.2.262-280.1997. ISSN 1092-2172. PMC 232610. PMID 9184013.
  13. Morris, Brandon E.L.; Henneberger, Ruth; Huber, Harald; Moissl-Eichinger, Christine (2013). "Microbial syntrophy: interaction for the common good". FEMS Microbiol Rev. 37 (3): 384–406. doi:10.1111/1574-6976.12019. PMID 23480449.
  14. McInerney, Michael J.; Struchtemeyer, Christopher G.; Sieber, Jessica; Mouttaki, Housna; Stams, Alfons J. M.; Schink, Bernhard; Rohlin, Lars; Gunsalus, Robert P. (1 March 2008). "Physiology, Ecology, Phylogeny, and Genomics of Microorganisms Capable of Syntrophic Metabolism". Annals of the New York Academy of Sciences. 1125 (1): 58–72. doi:10.1196/annals.1419.005. PMID 18378587.
  15. Drake, Harold L.; Horn, Marcus A.; Wüst, Pia K. (1 October 2009). "Intermediary ecosystem metabolism as a main driver of methanogenesis in acidic wetland soil". Environmental Microbiology Reports. 1 (5): 307–318. doi:10.1111/j.1758-2229.2009.00050.x. PMID 23765883.
  16. Storck, Tomas; Virdis, Bernardino; Batstone, Damien J. (2016). "Modelling extracellular limitations for mediated versus direct interspecies electron transfer". The ISME Journal. 10 (3): 621–631. doi:10.1038/ismej.2015.139. PMC 4817672. PMID 26545286.
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