In biology, syntrophy, syntrophism, or cross-feeding () is the cooperative interaction between at least two microbial species to degrade a single substrate. 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. 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 , , or substrates provided by the other(s).
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.
Syntrophy plays an important role in a large number of microbial processes especially in oxygen limited environments, methanogenic environments and anaerobic systems.
In anoxic or methanogenic environments such as wetlands, swamps, paddy fields, landfills, digestive tract of
, and anerobic digesters syntrophy is employed to overcome the energy constraints as the reactions in these environments proceed close to thermodynamic equilibrium.
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.
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
Lactic acid 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. The key mechanism that ensures the success of syntrophy is interspecies electron transfer.
The interspecies electron transfer can be carried out via three ways: interspecies hydrogen transfer, interspecies formate transfer and interspecies direct electron transfer.
Reverse electron transport is prominent in syntrophic metabolism.
The metabolic reactions and the energy involved for syntrophic degradation with H2 consumption:
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.
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. Syntrophic degradation of substrates like butyrate and benzoate can also happen without hydrogen consumption.
An example of propionate and butyrate degradation with interspecies formate transfer carried out by the mutual system of Syntrophomonas wolfei and Methanobacterium formicicum:
- 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 Methanosaeta or Methanosarcina
Examples
In ruminants
The defining feature of
, such as cows and goats, is a stomach called a
rumen.
The rumen contains billions of microbes, many of which are syntrophic.
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 the presence of syntrophic hydrogen-consuming microbes allows continued growth by metabolizing the waste products.
In addition, fermentative bacteria gain maximum energy yield when
protons are used as electron acceptor with concurrent
Hydrogen2 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 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).
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
Petroleum is of high ecological importance and can be effectively mediated through syntrophic degradation by complete mineralization of
alkane,
aliphatic and
hydrocarbon chains.
The hydrocarbons of the oil are broken down after activation by
fumarate, a chemical compound that is regenerated by other microorganisms.
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.
Syntrophic microbial communities are key players in the breakdown of aromatic compounds, which are common pollutants. The degradation of aromatic Benzoic acid to methane produces intermediate compounds such as formate, acetate, and H2. 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
Degradation of amino acids
Studies have shown that bacterial degradation of
amino acids can be significantly enhanced through the process of syntrophy.
Microbes growing poorly on amino acid substrates
alanine,
aspartate,
serine,
leucine,
valine, and
glycine can have their rate of growth dramatically increased by syntrophic H
2 scavengers. These scavengers, like
Methanospirillum and
Acetobacterium, metabolize the H
2 waste produced during amino acid breakdown, preventing a toxic build-up.
Another way to improve amino acid breakdown is through interspecies electron transfer mediated by formate. Species like
Desulfovibrio employ this method.
Amino acid fermenting anaerobes such as
Clostridium species,
Peptostreptococcus asacchaarolyticus,
Acidaminococcus fermentans were known to breakdown amino acids like
Glutamic acid with the help of hydrogen scavenging methanogenic partners without going through the usual Stickland fermentation pathway
Anaerobic digestion
Effective syntrophic cooperation between propionate oxidizing bacteria, acetate oxidizing bacteria and H
2/acetate consuming methanogens is necessary to successfully carryout anaerobic digestion to produce biomethane
Syntrophic theories of eukaryogenesis
Many
Symbiogenesis models of
eukaryogenesis propose that the first
Eukaryote cells were derived from
Endosymbiont facilitated by microbial syntrophy between
Prokaryote cells. Most of these models involve an
Archaea and an alphaproteobacterium, where the dependence of the
Archaea on the alphaproteobacterium leads the former to engulf the latter, the alphaproteobacterium then eventually becoming the
Mitochondrion. While these models share the concept of syntrophic interaction as a key driver of
Endosymbiont, they often differ on the exact nature of the metabolic interactions involved and the mechanisms by which
eukaryogenesis occurred.
Hydrogen hypothesis
In 1998, William F. Martin and Miklós Müller introduced the hydrogen hypothesis, proposing that
Eukaryote arose from syntrophic associations based on the transfer of H
2.
In this model, an syntrophic association arose where a anaerobic
Autotroph Methanogenesis Archaea was dependent on the H
2 made as a byproduct of anaerobic respiration by a facultatively anaerobic alphaproteobacterium.
This syntrophy led the alphaproteobacterium to become an
endosymbiont of the
Archaea, serving as the precursor to the
Mitochondrion.
Dennis Searcy model
Dennis Searcy proposed that the precursors to
Mitochondrion were
Parasitism bacteria that developed a syntrophy with their hosts based upon the transfer of organic acids, H
2 transfer, and the reciprocal exchange of sulfur compounds.
Reverse flow model
The reverse flow model was created based on the metabolic analysis of Asgard archaea, which is thought to be the kingdom from which
Eukaryote emerged.
This model proposes that a syntrophic association arose where anaerobic ancestral Asgard archaea generated and provided reducing equivalents that facultative anaerobic alphaproteobacteria used in the form of H
2, small reduced compounds, or by direct
electron transfer.
Entangle-Engulf-Endogenize model
The Entangle-Engulf-Endogenize (E3) model was created in 2020 based on the isolation of syntrophic
archaea from deep sea marine sediment.
Unlike most other symbiogenetic models, the E3 model involves three separate types of microbes: a
Fermentation Archaea, a facultatively aerobic
organotroph (which was acts as the precursor of the mitochondria), and sulfur-reducing bacteria (SRB).
This model proposes that, originally, the
Fermentation Archaea may have degraded
Amino acid via syntrophic association with SRB and the facultatively aerobic
organotroph.
As
oxygen levels began to rise, however, the interaction with the facultatively aerobic
organotroph (which is though to have made the
Archaea more aerotolerant) became stronger became stronger until it was engulfed (a process facilitated by syntrophic interaction with SRB).
Additionally, the E3 model suggests that, instead of
Phagocytosis the facultatively aerobic
organotroph, the
Archaea used extracellular structures to enhance interactions and engulf the facultatively aerobic
organotroph.
Syntrophy hypothesis
The syntrophy hypothesis was proposed in 2001 by researchers Purificación López-García and David Moreira before being refined in 2020 by the same researchers.
Similarly to the E3 model, the syntrophy hypothesis suggests that
eukaryogenesis involved three different types of microbes: a complex sulfate-reducing
Myxococcota (the precursor to the
cytoplasm), an H
2-producing Asgard archaeon (the precursor to the
Cell nucleus), and a facultatively aerobic sulfide-oxidizing alphaproteobacterium (the precursor to
Mitochondrion).
In this model, the
Myxococcota forms syntrophic associations with both the Asgard archaeon (based on the transfer of H
2) and the alphaproteobacterium (based on the redox of sulfur), leading both to become
Endosymbiont of the
Myxococcota.
In this now obligatory
symbiosis, organic compounds were degraded in the
Periplasm of the
Myxococcota before being moved to the
Archaea for further degradation.
This interaction drove the
periplasm to develop and expand in close proximity with the
Archaea to facilitate molecular exchange, resulting in an endomembrane system, transport channels, and the loss of the
Archaea membrane.
Ultimately, the archaeon became the nucleus while the periplasmic endomembrane system became the endoplasmic reticulum.
Meanwhile, the consortium lost the metabolic capability for
Bacteria sulfate reduction and
Archaea energy
metabolism as it became more reliant on aerobic respiration performed by the alphaproteobacterium which, ultimately, became the
mitochondrion.
Examples of syntrophic organisms
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Syntrophomonas wolfei is a gram-negative, anaerobic, fatty-acid oxidizing bacterium that forms syntrophic associations with H2-using bacteria.
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Syntrophobacter fumaroxidans is a gram-negative anaerobic bacterium that can oxidize propionate in pure cultures or in syntrophic association with Methanospirillum hungateii.
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Pelotomaculum thermopropionicum is a thermophilic, anaerobic, syntrophic propionate-oxidizing bacterium that, in co-culture with Methanothermobacter thermautotrophicus, can grow on propionate, ethanol, lactate, 1-butanol, 1-pentanol, 1,3-propanediol, 1-propanol, and ethylene glycol.
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Syntrophus aciditrophicus is a gram-negative, obligately anaerobic, nonmotile, rod-shaped bacterium that, in syntrophic association with hydrogen/formate-using methanogens or sulfate reducers, degrades benzoate and fatty acids.
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Syntrophus buswellii is a gram-negative, anaerobic, motile, rod-shaped bacterium that, in syntrophic association with H2-using bacteria, degrades benzoate.
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Syntrophus gentianae is a obligately anaerobic bacterium that ferments benzoate in syntrophic association with H2-using bacteria.