Syntrophy

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In biology, syntrophy, [1] [2] [3] [4] syntrophism, [1] [5] [6] or cross-feeding [1] (from Greek syn meaning together, trophe meaning nourishment) is the cooperative interaction between at least two microbial species to degrade a single substrate. [2] [3] [4] [7] This type of biological interaction typically involves the transfer of one or more metabolic intermediates between two or more metabolically diverse microbial species living in close proximity to each other. [3] [5] Thus, syntrophy can be considered an obligatory interdependency and a mutualistic metabolism between different microbial species, wherein the growth of one partner depends on the nutrients, growth factors, or substrates provided by the other(s). [8] [9]

Contents

Microbial syntrophy

Syntrophy is often used synonymously for mutualistic symbiosis especially between at least two different bacterial species. Syntrophy differs from symbiosis in a way that syntrophic relationship is primarily based on closely linked metabolic interactions to maintain thermodynamically favorable lifestyle in a given environment. [10] [11] [12] Syntrophy plays an important role in a large number of microbial processes especially in oxygen limited environments, methanogenic environments and anaerobic systems. [13] [14] In anoxic or methanogenic environments such as wetlands, swamps, paddy fields, landfills, digestive tract of ruminants, and anerobic digesters syntrophy is employed to overcome the energy constraints as the reactions in these environments proceed close to thermodynamic equilibrium. [9] [14] [15]

Mechanism of microbial syntrophy

The main mechanism of syntrophy is removing the metabolic end products of one species so as to create an energetically favorable environment for another species. [15] This obligate metabolic cooperation is required to facilitate the degradation of complex organic substrates under anaerobic conditions. Complex organic compounds such as ethanol, propionate, butyrate, and lactate cannot be directly used as substrates for methanogenesis by methanogens. [9] 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. The key mechanism that ensures the success of syntrophy is interspecies electron transfer. [16] The interspecies electron transfer can be carried out via three ways: interspecies hydrogen transfer, interspecies formate transfer and interspecies direct electron transfer. [16] [17] Reverse electron transport is prominent in syntrophic metabolism. [13]

The metabolic reactions and the energy involved for syntrophic degradation with H2 consumption: [18]

A classical syntrophic relationship can be illustrated by the activity of ‘Methanobacillus omelianskii’. It was isolated several times from anaerobic sediments and sewage sludge and was regarded as a pure culture of an anaerobe converting ethanol to acetate and methane. In fact, however, the culture turned out to consist of a methanogenic archaeon "organism M.o.H" and a Gram-negative Bacterium "Organism S" which involves the oxidization of ethanol into acetate and methane mediated by interspecies hydrogen transfer. Individuals of organism S are observed as obligate anaerobic bacteria that use ethanol as an electron donor, whereas M.o.H are methanogens that oxidize hydrogen gas to produce methane. [18] [19] [20]

Organism S: 2 Ethanol + 2 H2O → 2 Acetate− + 2 H+ + 4 H2 (ΔG°' = +9.6 kJ per reaction)

Strain M.o.H.: 4 H2 + CO2 → Methane + 2 H2O (ΔG°' = -131 kJ per reaction)

Co-culture:2 Ethanol + CO2 → 2 Acetate− + 2 H+ + Methane (ΔG°' = -113 kJ per reaction)

The oxidization of ethanol by organism S is made possible thanks to the methanogen M.o.H, which consumes the hydrogen produced by organism S, by turning the positive Gibbs free energy into negative Gibbs free energy. This situation favors growth of organism S and also provides energy for methanogens by consuming hydrogen. Down the line, acetate accumulation is also prevented by similar syntrophic relationship. [18] Syntrophic degradation of substrates like butyrate and benzoate can also happen without hydrogen consumption. [15]

An example of propionate and butyrate degradation with interspecies formate transfer carried out by the mutual system of Syntrophomonas wolfei and Methanobacterium formicicum: [16]

Propionate＋2H2O＋2CO2 → Acetate- ＋3Formate- ＋3H+ (ΔG°'=＋65.3 kJ/mol)

Butyrate＋2H2O＋2CO2 → 2Acetate- ＋3Formate- ＋3H+ ΔG°'=＋38.5 kJ/mol)

Direct interspecies electron transfer (DIET) which involves electron transfer without any electron carrier such as H2 or formate was reported in the co-culture system of Geobacter mettalireducens and Methanosaeto or Methanosarcina [16] [21]

Examples

In ruminants

The defining feature of ruminants, such as cows and goats, is a stomach called a rumen. [22] The rumen contains billions of microbes, many of which are syntrophic. [14] [23] Some anaerobic fermenting microbes in the rumen (and other gastrointestinal tracts) are capable of degrading organic matter to short chain fatty acids, and hydrogen. [14] [9] The accumulating hydrogen inhibits the microbe's ability to continue degrading organic matter, but the presence of syntrophic hydrogen-consuming microbes allows continued growth by metabolizing the waste products. [23] In addition, fermentative bacteria gain maximum energy yield when protons are used as electron acceptor with concurrent H 2 production. Hydrogen-consuming organisms include methanogens, sulfate-reducers, acetogens, and others. [24]

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. [25] In acetogenesis processes, 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). [26]

Biodegradation of pollutants

Syntrophic microbial food webs play an integral role in bioremediation especially in environments contaminated with crude oil and petrol. Environmental contamination with oil is of high ecological importance and can be effectively mediated through syntrophic degradation by complete mineralization of alkane, aliphatic and hydrocarbon chains. [27] [28] The hydrocarbons of the oil are broken down after activation by fumarate, a chemical compound that is regenerated by other microorganisms. [29] 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. [29]

Syntrophic microbial communities are key players in the breakdown of aromatic compounds, which are common pollutants. [28] The degradation of aromatic benzoate to methane produces intermediate compounds such as formate, acetate, CO2 and H2. [28] The buildup of these products makes benzoate degradation thermodynamically unfavorable. These intermediates can be metabolized syntrophically by methanogens and makes the degradation process thermodynamically favorable [28]

Degradation of amino acids

Studies have shown that bacterial degradation of amino acids can be significantly enhanced through the process of syntrophy. [30] 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. [30] Another way to improve amino acid breakdown is through interspecies electron transfer mediated by formate. Species like Desulfovibrio employ this method. [30] Amino acid fermenting anaerobes such as Clostridium species, Peptostreptococcus asacchaarolyticus, Acidaminococcus fermentans were known to breakdown amino acids like glutamate with the help of hydrogen scavenging methanogenic partners without going through the usual Stickland fermentation pathway [14] [30]

Anaerobic digestion

Effective syntrophic cooperation between propionate oxidizing bacteria, acetate oxidizing bacteria and H2/acetate consuming methanogens is necessary to successfully carryout anaerobic digestion to produce biomethane [4] [18]

Examples of syntrophic organisms

Related Research Articles

Methanogens are microorganisms that produce methane as a metabolic byproduct in hypoxic conditions. They belong to the domain Archaea and are members of the phylum Euryarchaeota. Methanogens are common in wetlands, where they are responsible for marsh gas, and can occur in the digestive tracts of animals including ruminants and humans, where they are responsible for the methane content of belching and flatulence. In marine sediments, the biological production of methane, termed methanogenesis, is generally confined to where sulfates are depleted below the top layers. Methanogens play an indispensable role in anaerobic wastewater treatments. Other methanogens are extremophiles, found in environments such as hot springs and submarine hydrothermal vents as well as in the "solid" rock of Earth's crust, kilometers below the surface in the deep biosphere.

Methanogenesis or biomethanation is the formation of methane coupled to energy conservation by microbes known as methanogens. Organisms capable of producing methane for energy conservation have been identified only from the domain Archaea, a group phylogenetically distinct from both eukaryotes and bacteria, although many live in close association with anaerobic bacteria. The production of methane is an important and widespread form of microbial metabolism. In anoxic environments, it is the final step in the decomposition of biomass. Methanogenesis is responsible for significant amounts of natural gas accumulations, the remainder being thermogenic.

<span class="mw-page-title-main">Sulfate-reducing microorganism</span> Microorganisms that "breathe" sulfates

Sulfate-reducing microorganisms (SRM) or sulfate-reducing prokaryotes (SRP) are a group composed of sulfate-reducing bacteria (SRB) and sulfate-reducing archaea (SRA), both of which can perform anaerobic respiration utilizing sulfate (SO2−
4) as terminal electron acceptor, reducing it to hydrogen sulfide (H2S). Therefore, these sulfidogenic microorganisms "breathe" sulfate rather than molecular oxygen (O2), which is the terminal electron acceptor reduced to water (H2O) in aerobic respiration.

An acetogen is a microorganism that generates acetate (CH3COO−) as an end product of anaerobic respiration or fermentation. However, this term is usually employed in a narrower sense only to those bacteria and archaea that perform anaerobic respiration and carbon fixation simultaneously through the reductive acetyl coenzyme A (acetyl-CoA) pathway (also known as the Wood-Ljungdahl pathway). These genuine acetogens are also known as "homoacetogens" and they can produce acetyl-CoA (and from that, in most cases, acetate as the end product) from two molecules of carbon dioxide (CO2) and four molecules of molecular hydrogen (H2). This process is known as acetogenesis, and is different from acetate fermentation, although both occur in the absence of molecular oxygen (O2) and produce acetate. Although previously thought that only bacteria are acetogens, some archaea can be considered to be acetogens.

<span class="mw-page-title-main">Sulfur-reducing bacteria</span> Microorganisms able to reduce elemental sulfur to hydrogen sulfide

Sulfur-reducing bacteria are microorganisms able to reduce elemental sulfur (S0) to hydrogen sulfide (H2S). These microbes use inorganic sulfur compounds as electron acceptors to sustain several activities such as respiration, conserving energy and growth, in absence of oxygen. The final product of these processes, sulfide, has a considerable influence on the chemistry of the environment and, in addition, is used as electron donor for a large variety of microbial metabolisms. Several types of bacteria and many non-methanogenic archaea can reduce sulfur. Microbial sulfur reduction was already shown in early studies, which highlighted the first proof of S0 reduction in a vibrioid bacterium from mud, with sulfur as electron acceptor and H
2 as electron donor. The first pure cultured species of sulfur-reducing bacteria, Desulfuromonas acetoxidans, was discovered in 1976 and described by Pfennig Norbert and Biebel Hanno as an anaerobic sulfur-reducing and acetate-oxidizing bacterium, not able to reduce sulfate. Only few taxa are true sulfur-reducing bacteria, using sulfur reduction as the only or main catabolic reaction. Normally, they couple this reaction with the oxidation of acetate, succinate or other organic compounds. In general, sulfate-reducing bacteria are able to use both sulfate and elemental sulfur as electron acceptors. Thanks to its abundancy and thermodynamic stability, sulfate is the most studied electron acceptor for anaerobic respiration that involves sulfur compounds. Elemental sulfur, however, is very abundant and important, especially in deep-sea hydrothermal vents, hot springs and other extreme environments, making its isolation more difficult. Some bacteria – such as Proteus, Campylobacter, Pseudomonas and Salmonella – have the ability to reduce sulfur, but can also use oxygen and other terminal electron acceptors.

Acetogenesis is a process through which acetate is produced by prokaryote microorganisms either by the reduction of CO2 or by the reduction of organic acids, rather than by the oxidative breakdown of carbohydrates or ethanol, as with acetic acid bacteria.

Microbial metabolism is the means by which a microbe obtains the energy and nutrients it needs to live and reproduce. Microbes use many different types of metabolic strategies and species can often be differentiated from each other based on metabolic characteristics. The specific metabolic properties of a microbe are the major factors in determining that microbe's ecological niche, and often allow for that microbe to be useful in industrial processes or responsible for biogeochemical cycles.

<i>Methanobacterium</i> Genus of archaea

Methanobacterium is a genus of the Methanobacteria class in the Archaea kingdom, which produce methane as a metabolic byproduct. Despite the name, this genus belongs not to the bacterial domain but the archaeal domain. Methanobacterium are nonmotile and live without oxygen, which is toxic to them, and they only inhabit anoxic environments.

Anaerobic oxidation of methane (AOM) is a methane-consuming microbial process occurring in anoxic marine and freshwater sediments. AOM is known to occur among mesophiles, but also in psychrophiles, thermophiles, halophiles, acidophiles, and alkophiles. During AOM, methane is oxidized with different terminal electron acceptors such as sulfate, nitrate, nitrite and metals, either alone or in syntrophy with a partner organism.

In the taxonomy of microorganisms, the Methanothrix is a genus of methanogenic archaea within the Euryarchaeota. Methanothrix cells were first isolated from a mesophilic sewage digester but have since been found in many anaerobic and aerobic environments. Methanothrix were originally understood to be obligate anaerobes that can survive exposure to high concentrations of oxygen, but recent studies have shown at least one Candidatus operational taxonomic unit proposed to be in the Methanothrix genus not only survives but remains active in oxic soils. This proposed species, Ca. Methanothrix paradoxum, is frequently found in methane-releasing ecosystems and is the dominant methanogen in oxic soils.

Syntrophobacter wolinii is a non-motile, gram-negative and rod-shaped species of bacteria that was originally isolated from a wastewater digester. This species is able to perform propionate degradation and sulfate reduction. S. wolinii can be grown in co-culture or pure culture. 16s rRNA analysis shows its close relation to other sulfate reducers.

<i>Methanococcus maripaludis</i> Species of archaeon

Methanococcus maripaludis is a species of methanogenic archaea found in marine environments, predominantly salt marshes. M. maripaludis is a non-pathogenic, gram-negative, weakly motile, non-spore-forming, and strictly anaerobic mesophile. It is classified as a chemolithoautotroph. This archaeon has a pleomorphic coccoid-rod shape of 1.2 by 1.6 μm, in average size, and has many unique metabolic processes that aid in survival. M. maripaludis also has a sequenced genome consisting of around 1.7 Mbp with over 1,700 identified protein-coding genes. In ideal conditions, M. maripaludis grows quickly and can double every two hours.

Syntrophomonas zehnderi is a bacterium. It is anaerobic, syntrophic and fatty acid-oxidizing. The type strain is OL-4T. Cells are slightly curved, non-motile rods.

Syntrophus aciditrophicus is a gram-negative and rod-shaped bacterium. It is non-motile, non-spore-forming and grows under strictly anaerobic conditions, thus an obligate anaerobe. It degrades fatty acids and benzoate in syntrophic association with hydrogen-using microorganisms. Its genome was published in 2007.

Syntrophococcus sucromutans is a Gram-negative strictly anaerobic chemoorganotrophic Bacillota. These bacteria can be found forming small chains in the habitat where it was first isolated, the rumen of cows. It is the type strain of genus Syntrophococcus and it has an uncommon one-carbon metabolic pathway, forming acetate from formate as a product of sugar oxidation.

Interspecies hydrogen transfer (IHT) is a form of interspecies electron transfer. It is a syntrophic process by which H2 is transferred from one organism to another, particularly in the rumen and other anaerobic environments.

Desulfovibrio alcoholivorans is a bacterium from the genus of Desulfovibrio which has been isolated from alcohol industry waste water in France.

Methanogens are a group of microorganisms that produce methane as a byproduct of their metabolism. They play an important role in the digestive system of ruminants. The digestive tract of ruminants contains four major parts: rumen, reticulum, omasum and abomasum. The food with saliva first passes to the rumen for breaking into smaller particles and then moves to the reticulum, where the food is broken into further smaller particles. Any indigestible particles are sent back to the rumen for rechewing. The majority of anaerobic microbes assisting the cellulose breakdown occupy the rumen and initiate the fermentation process. The animal absorbs the fatty acids, vitamins and nutrient content on passing the partially digested food from the rumen to the omasum. This decreases the pH level and initiates the release of enzymes for further breakdown of the food which later passes to the abomasum to absorb remaining nutrients before excretion. This process takes about 9–12 hours.

Biological methanation (also: biological hydrogen methanation (BHM) or microbiological methanation) is a conversion process to generate methane by means of highly specialized microorganisms (Archaea) within a technical system. This process can be applied in a power-to-gas system to produce biomethane and is appreciated as an important storage technology for variable renewable energy in the context of energy transition. This technology was successfully implemented at a first power-to-gas plant of that kind in the year 2015.

Formatotrophs are organisms that can assimilate formate or formic acid to use as a carbon source or for reducing power. Some authors classify formatotrophs as one of the five trophic groups of methanogens, which also include hydrogenotrophs, acetotrophs, methylotrophs, and alcoholotrophs. Formatotrophs have garnered attention for applications in biotechnology as part of a "formate bioeconomy" in which synthesized formate could be used as a nutrient for microoganisms. Formate can be electrochemically synthesized from CO2 and renewable energy, and formatotrophs may be genetically modified to enhance production of biochemical products to be used as biofuels. Technical limitations in culturing formatotrophs have limited the discovery of natural formatotrophs and impeded research on their formate-metabolizing enzymes, which are of interest for applications in carbon sequestration and astrobiology.

References

  1. 1 2 3 Gentry, Terry J.; Pepper, Ian L.; Pierson, Leland S. (2015-01-01), Pepper, Ian L.; Gerba, Charles P.; Gentry, Terry J. (eds.), "Chapter 19 - Microbial Diversity and Interactions in Natural Ecosystems", Environmental Microbiology (Third Edition), San Diego: Academic Press, pp. 441–460, doi:10.1016/b978-0-12-394626-3.00019-3, ISBN   978-0-12-394626-3 , retrieved 2023-12-27
  2. 1 2 Marietou, Angeliki (2021-01-01), Gadd, Geoffrey Michael; Sariaslani, Sima (eds.), "Chapter Two - Sulfate reducing microorganisms in high temperature oil reservoirs", Advances in Applied Microbiology, 116, Academic Press: 99–131, doi:10.1016/bs.aambs.2021.03.004, PMID   34353505 , retrieved 2023-12-27
  3. 1 2 3 4 5 Schink B, Stams AJ (2013). "Syntrophism Among Prokaryotes". In Rosenberg E, DeLong EF, Lory S, Stackebrandt E (eds.). The Prokaryotes: Prokaryotic Communities and Ecophysiology. Berlin, Heidelberg: Springer. pp. 471–493. doi:10.1007/978-3-642-30123-0_59. ISBN   978-3-642-30123-0.
  4. 1 2 3 Kamagata Y (2015-03-15). "Syntrophy in Anaerobic Digestion". Anaerobic Biotechnology. Imperial College Press. pp. 13–30. doi:10.1142/9781783267910_0002. ISBN   978-1-78326-790-3 . Retrieved 2022-11-11.
  5. 1 2 "syntrophism | biology | Britannica". 2022-09-30. Archived from the original on 2022-09-30. Retrieved 2023-12-27.
  6. ↑ "Syntrophism Definition & Meaning | Merriam-Webster Medical". 2022-08-19. Archived from the original on 2022-08-19. Retrieved 2023-12-27.
  7. ↑ Hao L, Michaelsen TY, Singleton CM, Dottorini G, Kirkegaard RH, Albertsen M, et al. (April 2020). "Novel syntrophic bacteria in full-scale anaerobic digesters revealed by genome-centric metatranscriptomics". The ISME Journal. 14 (4): 906–918. Bibcode:2020ISMEJ..14..906H. doi:10.1038/s41396-019-0571-0. PMC   7082340 . PMID   31896784.
  8. ↑ Dolfing J (January 2014). "Syntrophy in microbial fuel cells". The ISME Journal. 8 (1): 4–5. Bibcode:2014ISMEJ...8....4D. doi:10.1038/ismej.2013.198. PMC   3869025 . PMID   24173460.
  9. 1 2 3 4 Morris BE, Henneberger R, Huber H, Moissl-Eichinger C (May 2013). "Microbial syntrophy: interaction for the common good". FEMS Microbiology Reviews. 37 (3): 384–406. doi: 10.1111/1574-6976.12019 . PMID   23480449.
  10. ↑ Sieber JR, McInerney MJ, Gunsalus RP (2012). "Genomic insights into syntrophy: the paradigm for anaerobic metabolic cooperation". Annual Review of Microbiology. 66: 429–452. doi:10.1146/annurev-micro-090110-102844. PMID   22803797.
  11. ↑ McInerney MJ, Sieber JR, Gunsalus RP (December 2009). "Syntrophy in anaerobic global carbon cycles". Current Opinion in Biotechnology. 20 (6): 623–632. doi:10.1016/j.copbio.2009.10.001. PMC   2790021 . PMID   19897353.
  12. ↑ McInerney MJ, Rohlin L, Mouttaki H, Kim U, Krupp RS, Rios-Hernandez L, et al. (May 2007). "The genome of Syntrophus aciditrophicus: life at the thermodynamic limit of microbial growth". Proceedings of the National Academy of Sciences of the United States of America. 104 (18): 7600–7605. Bibcode:2007PNAS..104.7600M. doi: 10.1073/pnas.0610456104 . PMC   1863511 . PMID   17442750.
  13. 1 2 McInerney MJ, Sieber JR, Gunsalus RP (December 2009). "Syntrophy in anaerobic global carbon cycles". Current Opinion in Biotechnology. Chemical biotechnology ● Pharmaceutical biotechnology. 20 (6): 623–632. doi:10.1016/j.copbio.2009.10.001. PMC   2790021 . PMID   19897353.
  14. 1 2 3 4 5 6 Worm P, Müller N, Plugge CM, Stams AJ, Schink B (2010). "Syntrophy in methanogenic degradation.". (Endo)symbiotic Methanogenic Archaea. Microbiology Monographs. Vol. 19. Berlin, Heidelberg: Springer. pp. 143–173. doi:10.1007/978-3-642-13615-3_9. ISBN   978-3-642-13614-6.
  15. 1 2 3 4 Jackson BE, McInerney MJ (January 2002). "Anaerobic microbial metabolism can proceed close to thermodynamic limits". Nature. 415 (6870): 454–456. Bibcode:2002Natur.415..454J. doi:10.1038/415454a. PMID   11807560. S2CID   9126984.
  16. 1 2 3 4 Zhang M, Zang L (2019). "A review of interspecies electron transfer in anaerobic digestion". IOP Conf. Ser: Earth Environ. 310 (4): 042026. Bibcode:2019E&ES..310d2026Z. doi: 10.1088/1755-1315/310/4/042026 . S2CID   202886264.
  17. ↑ Rotaru AE, Shrestha PM, Liu F, Ueki T, Nevin K, Summers ZM, Lovley DR (November 2012). "Interspecies electron transfer via hydrogen and formate rather than direct electrical connections in cocultures of Pelobacter carbinolicus and Geobacter sulfurreducens". Applied and Environmental Microbiology. 78 (21): 7645–7651. Bibcode:2012ApEnM..78.7645R. doi:10.1128/AEM.01946-12. PMC   3485699 . PMID   22923399.
  18. 1 2 3 4 Zhang Y, Li C, Yuan Z, Wang R, Angelidaki I, Zhu G (2023-01-15). "Syntrophy mechanism, microbial population, and process optimization for volatile fatty acids metabolism in anaerobic digestion". Chemical Engineering Journal. 452: 139137. Bibcode:2023ChEnJ.45239137Z. doi:10.1016/j.cej.2022.139137. ISSN   1385-8947. S2CID   252205776.
  19. ↑ Wrede C, Dreier A, Kokoschka S, Hoppert M (2012). "Archaea in symbioses". Archaea. 2012: 596846. doi: 10.1155/2012/596846 . PMC   3544247 . PMID   23326206.
  20. ↑ Morris BE, Henneberger R, Huber H, Moissl-Eichinger C (May 2013). "Microbial syntrophy: interaction for the common good". FEMS Microbiology Reviews. 37 (3): 384–406. doi: 10.1111/1574-6976.12019 . PMID   23480449.
  21. ↑ Dubé CD, Guiot SR (2015). "Direct Interspecies Electron Transfer in Anaerobic Digestion: A Review". Biogas Science and Technology. Advances in Biochemical Engineering/Biotechnology. Vol. 151. pp. 101–15. doi:10.1007/978-3-319-21993-6_4. ISBN   978-3-319-21992-9. PMID   26337845.
  22. ↑ "What's a Rumen". AnimalSmart.org. Retrieved 2022-11-21.
  23. 1 2 Ng F, Kittelmann S, Patchett ML, Attwood GT, Janssen PH, Rakonjac J, Gagic D (September 2016). "An adhesin from hydrogen-utilizing rumen methanogen Methanobrevibacter ruminantium M1 binds a broad range of hydrogen-producing microorganisms". Environmental Microbiology. 18 (9): 3010–3021. doi: 10.1111/1462-2920.13155 . PMID   26643468.
  24. ↑ Sapkota A (2022-07-12). "Syntrophism or Syntrophy Interaction- Definition, Examples". The Biology Notes. Retrieved 2022-11-21.
  25. ↑ Kang D, Saha S, Kurade MB, Basak B, Ha G, Jeon B, et al. (July 2021). "Dual-stage pulse-feed operation enhanced methanation of lipidic waste during co-digestion using acclimatized consortia". Renewable and Sustainable Energy Reviews. 145: 111096. doi:10.1016/j.rser.2021.111096. ISSN   1364-0321. S2CID   234830362.
  26. ↑ Stams AJ, de Bok FA, Plugge CM, van Eekert MH, Dolfing J, Schraa G (March 2006). "Exocellular electron transfer in anaerobic microbial communities". Environmental Microbiology. 8 (3): 371–382. Bibcode:2006EnvMi...8..371S. doi:10.1111/j.1462-2920.2006.00989.x. PMID   16478444.
  27. ↑ Callaghan AV, Morris BE, Pereira IA, McInerney MJ, Austin RN, Groves JT, et al. (January 2012). "The genome sequence of Desulfatibacillum alkenivorans AK-01: a blueprint for anaerobic alkane oxidation". Environmental Microbiology. 14 (1): 101–113. Bibcode:2012EnvMi..14..101C. doi:10.1111/j.1462-2920.2011.02516.x. PMID   21651686.
  28. 1 2 3 4 Ferry JG, Wolfe RS (February 1976). "Anaerobic degradation of benzoate to methane by a microbial consortium". Archives of Microbiology. 107 (1): 33–40. Bibcode:1976ArMic.107...33F. doi:10.1007/BF00427864. PMID   1252087. S2CID   31426072.
  29. 1 2 Callaghan AV, Morris BE, Pereira IA, McInerney MJ, Austin RN, Groves JT, et al. (January 2012). "The genome sequence of Desulfatibacillum alkenivorans AK-01: a blueprint for anaerobic alkane oxidation". Environmental Microbiology. 14 (1): 101–113. Bibcode:2012EnvMi..14..101C. doi:10.1111/j.1462-2920.2011.02516.x. PMID   21651686.
  30. 1 2 3 4 Zindel U, Freudenberg W, Rieth M, Andreesen JR, Schnell J, Widdel F (July 1988). "Eubacterium acidaminophilum sp. nov., a versatile amino acid-degrading anaerobe producing or utilizing H2 or formate". Archives of Microbiology. 150 (3): 254–266. Bibcode:1988ArMic.150..254Z. doi:10.1007/BF00407789. ISSN   0302-8933. S2CID   34824309.
  31. ↑ McInerney MJ, Bryant MP, Hespell RB, Costerton JW (April 1981). "Syntrophomonas wolfei gen. nov. sp. nov., an Anaerobic, Syntrophic, Fatty Acid-Oxidizing Bacterium". Applied and Environmental Microbiology. 41 (4): 1029–1039. Bibcode:1981ApEnM..41.1029M. doi:10.1128/aem.41.4.1029-1039.1981. PMC   243852 . PMID   16345745.
  32. ↑ Schöcke L, Schink B (September 1998). "Membrane-bound proton-translocating pyrophosphatase of Syntrophus gentianae, a syntrophically benzoate-degrading fermenting bacterium". European Journal of Biochemistry. 256 (3): 589–594. doi:10.1046/j.1432-1327.1998.2560589.x. PMID   9780235.
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