Electron transfer in syntrophic communities of anaerobic bacteria and archaea

Key Points

  • Anaerobic methane formation and anaerobic methane oxidation are important microbial processes in the global carbon cycle. Both processes are mediated by syntrophic communities of bacteria and archaea. In methane formation, bacteria degrade organic compounds to form products that are substrates for the methanogenic archaea. In anaerobic methane oxidation, methanotrophic archaea degrade methane and form currently unknown compounds that are used as electron donors by sulphate-reducing bacteria.

  • Hydrogen and formate are key components in interspecies electron transfer in facultative and obligate syntrophic methanogenic communities. In facultative syntrophy, anaerobic bacteria have an energetic advantage over the methanogens, but they are not essential for growth. In obligate syntrophic communities, bacteria and archaea degrade and grow on a substrate that each organism alone could not metabolize. This results in physical aggregation of bacteria and archaea, which may have led to the evolution of the first eukaryotic cell.

  • Bacteria that grow in obligate syntrophic association with methanogens live at the limits of what is thermodynamically possible. They encounter an energetic barrier in the recycling of redox mediators. NADH oxidation can be coupled to proton reduction only at low hydrogen concentrations, which are created by the methanogen. FADH2 oxidation coupled to proton reduction requires not only a low hydrogen concentration but also supplementary energy input from reverse electron transfer. Possible mechanisms of reverse electron transfer can be deduced from available genome sequences.

  • Simple substrates that are known typical substrates for methanogenic archaea, such as methanol, acetate and formate, can also be degraded by syntrophic communities of bacteria and archaea. Also, substrates that are considered easily fermentable might require syntrophic communities. This suggests that the anaerobic food chain in methanogenic environments is even more complex and more versatile than previously thought.

  • The occurrence of the anaerobic oxidation of methane coupled to sulphate reduction has been demonstrated in many studies. It is clear that syntrophic communities of methanotrophic archaea, which perform reverse methanogenesis, and sulphate-reducing bacteria are involved. The mechanism of this syntrophic interaction is unclear. Analogous to methanogenic communities, we propose that multiple compounds are involved.

Abstract

Interspecies electron transfer is a key process in methanogenic and sulphate-reducing environments. Bacteria and archaea that live in syntrophic communities take advantage of the metabolic abilities of their syntrophic partner to overcome energy barriers and break down compounds that they cannot digest by themselves. Here, we review the transfer of hydrogen and formate between bacteria and archaea that helps to sustain growth in syntrophic methanogenic communities. We also describe the process of reverse electron transfer, which is a key requirement in obligately syntrophic interactions. Anaerobic methane oxidation coupled to sulphate reduction is also carried out by syntrophic communities of bacteria and archaea but, as we discuss, the exact mechanism of this syntrophic interaction is not yet understood.

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Figure 1: Syntrophic communities of bacteria and archaea in a sludge granule from a methanogenic reactor.
Figure 2: Different strategies to enrich microorganisms from anaerobic environments.
Figure 3: The biochemical pathways of syntrophic propionate and butyrate oxidation.
Figure 4: Possible biochemical mechanism of reverse electron transport to drive the endergonic conversion of succinate to fumarate.

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Acknowledgements

Our research was supported by grants of the divisions of Chemical Sciences, Earth and Life Sciences and the Technology Foundation of the Netherlands Science Foundation and the Darwin Center for Biogeology.

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DATABASES

Entrez Genome Project

Bacillus subtilis

Clostridium kluyveri

Desulfovibrio vulgaris

Escherichia coli

Methanococcus maripaludis

Methanosarcina barkeri

Pelotomaculum thermopropionicum

Ruminococcus albus

Shewanella oneidensis

Syntrophobacter fumaroxidans

Syntrophomonas wolfei

Syntrophus aciditrophicus

Wolinella succinogenes

FURTHER INFORMATION

Alfons J. M. Stams's homepage

DOE Joint Genome Institute

Glossary

Methanogenic environment

An anoxic environment in which organic matter is degraded and protons and CO2 act as the main electron acceptors. The limited range of substrates that are used by methanogenic archaea results in a syntrophic cooperation with microorganisms that degrade more complex organic compounds and form substrates for methanogens.

Syntrophic

A nutritional situation in which two or more organisms combine their metabolic capabilities to catabolize a substrate that cannot be catabolized by either one of them alone.

Reducing equivalent

Any kind of reduced redox mediator that is formed by the oxidation of organic or inorganic compounds.

Midpoint redox potential

The quantitative expression of the electrochemical property of redox-active compounds, relative to the redox couple H+/H2. A solution of 1 M H+ saturated with H2 at atmospheric pressure has a redox potential (E°) of 0 V. The E°′ at pH 7 is −0.414 V.

Standard Gibbs free energy change

(ΔG°′). The amount of energy that is released or needed in a chemical conversion. The standard conditions refer to 1 M for solutes, 105 Pa (1 atm) for gases, 298 K and a pH of 7. A reaction in which energy is released is an exergonic reaction and a reaction that requires energy is an endergonic reaction. ΔG°′ values are expressed as kJ mol−1.

Substrate level phosphorylation

The synthesis of high-energy phosphate bonds through the reaction of inorganic phosphate with an activated organic substrate. For fermentative bacteria, it is often the sole biochemical mechanism of energy conservation.

High-rate methanogenic bioreactor

A reactor that is used for the anaerobic treatment of industrial wastewaters with a high concentration of organic compounds. High loading rates can be applied because the biomass is present as dense aggregates (granular sludge) that allow uncoupling of the liquid retention time from the biomass retention time.

Reverse electron transport

The biochemical mechanism by which microorganisms can perform a chemical transformation that is endergonic under the prevailing conditions. It resembles the electron transport-driven mechanism of energy conservation from an exergonic reaction but operates in reverse.

Menaquinone

Abbreviation for methylnaphthoquinone, an electron carrier in the cytoplasmic membrane of many bacteria and archaea. Reduction by one electron yields the menasemiquinone anion, which on further reduction by a second electron takes two protons and thus forms menahydroquinone (also called menaquinol).

Electron bifurcation

Separation of the two electrons from ubiquinol at the quinol oxidation site of the bc1 complex (complex III) of the respiratory chain, which leads to a bifurcation of the two electrons to a high and a low potential pathway.

Homoacetogen

An anaerobic bacterium that can grow on H2 and CO2, forming acetate as a product. As homoacetogenesis is conditional, homoacetogens are also known as acetogens.

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Stams, A., Plugge, C. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol 7, 568–577 (2009). https://doi.org/10.1038/nrmicro2166

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