Elusive microbe that consumes ethane found under the sea

A microorganism that consumes ethane in the absence of environmental oxygen has been discovered. In the depths of the sea, this microbe, which oxidizes ethane, partners with another that reduces sulfate to sulfide.
Stephen W. Ragsdale is in the Department of Biological Chemistry, University of Michigan Medical School, Ann Arbor, Michigan 48109-0606, USA.

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Plumes of natural gas emanate from the bottom of the ocean. These hydrocarbon emissions comprise around 90% methane, with ethane making up most of the rest. Such deep-sea sources are responsible for 5% of the methane, a greenhouse gas, present in Earth’s atmosphere1. The amount of hydrocarbon released from the deep sea into the atmosphere is substantially reduced by microorganisms that capture and use these gases as their sole source of cellular carbon and energy. Writing in Nature, Chen et al.2 describe the culmination of a ten-year scientific mission to identify and characterize the microorganisms and reactions that are responsible for ethane consumption at hydrocarbon seeps in the deep sea.

The microbes that metabolize the small alkane molecules methane, propane and butane to carbon dioxide in the absence of environmental oxygen (a process called anaerobic oxidation) have been identified, but those that use ethane have been elusive. Although the oxidation of alkanes by enzymes known as oxygenases in the presence of environmental oxygen (aerobic oxidation) is a thermodynamically favourable reaction, and thus likely to happen, the anaerobic process is thermodynamically unfavourable. Therefore, anaerobic alkane oxidation can occur only if it is coupled to an extremely thermodynamically favourable reduction reaction.

Chen et al. show that the anaerobic oxidation of ethane involves a mutually beneficial relationship, called syntrophy, between two microorganisms (Fig. 1). A newly identified microbe, the archaeon ‘Candidatus Argoarchaeum ethanivorans’, oxidizes ethane to CO2. Like all known anaerobic microbes that oxidize methane, propane and butane, Ca. A. ethanivorans is classified as an anaerobic methanotrophic (ANME) archaeon. Chen et al. show that the oxidation of ethane to CO2 requires another biochemical reaction, the reduction of sulfate to sulfide. The genome of Ca. A. ethanivorans lacks sulfate-reducing enzymes, but an analysis of the microorganisms that live in the same microbial culture as Ca. A. ethanivorans revealed the presence of two bacterial strains from the genus Desulfosarcina that reduce sulfate to sulfide.

Figure 1 | The fate of deep-sea hydrocarbons. The plumes of gas that are produced at the ocean bottom are composed mainly of methane, the smallest alkane molecule, but also contain smaller amounts of other alkanes, including ethane, propane and butane (quantities shown in teragrams per year; 1 Tg = 1012 grams)1,1013. Deep-sea microorganisms consume a large proportion of these gases, and only a small proportion ends up in the atmosphere, where it contributes to the greenhouse effect. The microbial oxidation of alkanes into carbon dioxide in the absence of oxygen (anaerobic oxidation) requires a complementary reaction comprising the reduction of sulfate to sulfide. These two reactions are carried out by distinct alkane-oxidizing (deep-colour symbols) and sulfate-reducing (pale symbols) microorganisms. Other microorganisms perform aerobic oxidation nearer the sea’s surface (not shown). Chen et al.2 identified the archaeon ‘Candidatus Argoarchaeum ethanivorans’ as the first known microbe to oxidize ethane anaerobically. They also identified two strains of bacterium from the genus Desulfosarcina that reduce sulfate to sulfide and enable ethane oxidation to occur.

There is active debate concerning the nature of the syntrophic relationship between alkane-oxidizing archaea and sulfate-reducing bacteria. Does it involve the exchange of metabolites such as hydrogen molecules, small organic molecules or sulfur-containing molecules between the partner species? Or does it involve the direct interspecies transfer of electrons? Evidence for the direct transfer of electrons is supported by the observation that alkane-oxidizing microbes contain genes that encode cytochrome enzymes with multiple haem groups, which catalyse reduction and oxidation reactions35; such reactions involve the transfer of electrons between molecules. Furthermore, transmission electron microscopy has revealed the presence of filament-like nanowire connections between methane- or butane-oxidizing microbes and sulfate-reducing microbes. These filaments are thought to be needed for interspecies electron transfer3,4. Nevertheless, contrasting evidence also shows that ANME archaea involved in marine methane oxidation produce a sulfur-containing molecule that is transferred to a sulfate-reducing partner microorganism6.

Chen et al. think that, for ethane oxidation, the transfer of a sulfur-containing metabolite is the process most likely to underlie the interaction between these two types of microorganism. This is because Ca. A. ethanivorans produces a lot of sulfur during growth, lacks the nanowire structures that have been observed in methane-oxidizing microbes, and grows as single cells rather than as a biofilm (a structure in which microbial cells stick to each other). All of these features could facilitate interspecies electron transfer. But Chen et al. also observed that the genomes of the sulfate-reducing bacteria they studied encode multi-haem cytochromes and the components of nanowire connections similar to those that are found in cultures of alkane-oxidizing and sulfate-reducing microbes grown together3. So, the jury is still out on how this interspecies coupling occurs.

What is the biochemical pathway for transforming ethane into CO2? Chen and colleagues demonstrate unambiguously that the genome of Ca. A. ethanivorans contains three genes that encode the subunits of a previously unknown enzyme, which we call here ethyl-coenzyme M reductase (ECR). They then identify the protein sequence of ECR using mass spectrometry. ECR is closely related to an enzyme called methyl-coenzyme M reductase (MCR), which is present in microorganisms that oxidize or generate methane. Chen et al. also identify the final product of the reaction catalysed by ECR, ethyl-coenzyme M.

Chen et al. modelled the 3D structures of the Ca. A. ethanivorans ECR and the butane-metabolizing enzyme (butyl-coenzyme M reductase) of ‘Candidatus Syntrophoarchaeum’4, and compared them with the known structure of the MCR of Methanothermobacter marburgensis7. On the basis of this structure comparison, as well as an alignment of the sequences of all known MCR-related proteins, they conclude that ECR and the other enzymes that metabolize non-methane hydrocarbon gases form a distinct cluster within an overarching group of enzymes called the alkyl-coenzyme M reductase (ACR) family, which catalyse the anaerobic oxidation of alkanes.

By analogy with the well-studied enzymatic mechanism of MCR8, it is likely that ECR initiates anaerobic ethane oxidation by transforming ethane into an ethyl radical molecule, which is very reactive. It will be exciting when researchers are able to generate sufficient amounts of ECR to determine its enzymatic and biophysical properties. For example, how does it selectively catalyse the oxidation of ethane when the natural gas plumes where Ca. A. ethanivorans grows are so rich in methane? The authors’ analysis did not reveal any obvious distinguishing features of the binding pockets of ACR enzymes, including ECR, that could explain their preference for metabolizing specific alkanes. However, the structures that the authors compared represent the inactive states of ACRs. It is to be hoped that the crystal structures of the active states of this enzyme family will soon be determined to help clarify this and other questions about their mechanism.

Chen et al. propose a plausible route from ECR-generated ethyl-coenzyme M to CO2. In this model, ethyl-coenzyme M is transformed into acetyl-coenzyme A, a molecule involved in many other metabolic processes, which is then oxidized through a mechanism called the reverse Wood–Ljungdahl pathway9. The authors identified proteins that are involved in this pathway using genomic and proteomic methods. However, the conversion of ethyl-coenzyme M to acetyl-coenzyme A still requires experimental validation. A similar gap in knowledge also exists for other non-methane oxidation pathways, including anaerobic butane oxidation by Ca. Syntrophoarchaeum4.

The next logical steps are to resolve the controversy regarding the nature of the communication between the newly identified ethane-oxidizing microorganism and its sulfate-reducing partner, and to build the metabolic bridge between ethyl-coenzyme M and acetyl-coenzyme A.

Nature 568, 40-41 (2019)

doi: 10.1038/d41586-019-00842-2


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