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Anaerobic Oxidation of Ethane by Archaea from a Marine Hydrocarbon Seep Song-Can Chen1,2, Niculina Musat1, Oliver J

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Anaerobic Oxidation of Ethane by Archaea from a Marine Hydrocarbon Seep Song-Can Chen1,2, Niculina Musat1, Oliver J LETTER https://doi.org/10.1038/s41586-019-1063-0 Anaerobic oxidation of ethane by archaea from a marine hydrocarbon seep Song-Can Chen1,2, Niculina Musat1, Oliver J. Lechtenfeld3, Heidrun Paschke3, Matthias Schmidt1, Nedal Said1, Denny Popp4, Federica Calabrese1, Hryhoriy Stryhanyuk1, Ulrike Jaekel5,8, Yong-Guan Zhu2,6, Samantha B. Joye7, Hans-Hermann Richnow1, Friedrich Widdel5 & Florin Musat1,5* Ethane is the second most abundant component of natural gas same basic mechanism—the formation of the thioethers propyl- or in addition to methane, and—similar to methane—is chemically butyl-coenzyme M9,21,22. By contrast, the alkane-degrading bacteria unreactive. The biological consumption of ethane under anoxic couple propane or butane oxidation to sulfate reduction in the same conditions was suggested by geochemical profiles at marine cell and initiate alkane oxidation by reaction with fumarate, yielding hydrocarbon seeps1–3, and through ethane-dependent sulfate alkyl-succinates6,23. reduction in slurries4–7. Nevertheless, the microorganisms and Ethane is the second most abundant hydrocarbon in gas of thermo- reactions that catalyse this process have to date remained unknown8. genic origin, often exceeding 10% by volume24, but is the least stud- Here we describe ethane-oxidizing archaea that were obtained ied with respect to anaerobic biodegradation8. Although its anaerobic by specific enrichment over ten years, and analyse these archaea utilization has been measured as ethane-dependent sulfate reduction using phylogeny-based fluorescence analyses, proteogenomics or ethane consumption in sediment slurries4–7, the microorganisms and metabolite studies. The co-culture, which oxidized ethane and reactions that catalyse this process remain unknown8. Here we completely while reducing sulfate to sulfide, was dominated by an use continued selective enrichment to reveal the microorganisms that archaeon that we name ‘Candidatus Argoarchaeum ethanivorans’; are capable of anaerobic ethane oxidation. The identified organisms other members were sulfate-reducing Deltaproteobacteria. The are related to a lineage of uncultured archaea, initiate ethane oxidation genome of Ca. Argoarchaeum contains all of the genes that are through coenzyme M thioether formation and apparently depend on necessary for a functional methyl-coenzyme M reductase, and sulfate-reducing bacteria. all subunits were detected in protein extracts. Accordingly, ethyl- A slurry with ethane-dependent sulfate reduction6 was cultivated coenzyme M (ethyl-CoM) was identified as an intermediate by (inoculum size: one-third by volume) over 10 years at 12 °C, a tempera- liquid chromatography–tandem mass spectrometry. This indicated ture that is also suitable for anaerobic methanotrophs25. This resulted in that Ca. Argoarchaeum initiates ethane oxidation by ethyl-CoM a sediment-free enrichment culture, termed Ethane12, which reduced formation, analogous to the recently described butane activation 10 mM sulfate during a period of approximately 7 months with strict by ‘Candidatus Syntrophoarchaeum’9. Proteogenomics further dependence on ethane addition. The approximate rate of ethane oxi- suggests that oxidation of intermediary acetyl-CoA to CO2 occurs dation was 4 mmol per day per gram cell dry weight, comparable with through the oxidative Wood–Ljungdahl pathway. The identification AOM rates (Supplementary Information). The molar ratios of con- of an archaeon that uses ethane (C2H6) fills a gap in our knowledge sumed ethane to formed sulfide in duplicate experiments were 1.63 and of microorganisms that specifically oxidize members of the 1.86 (Fig. 1a and Extended Data Table 1), indicating ethane oxidation homologous alkane series (CnH2n+2) without oxygen. Detection according to: of phylogenetic and functional gene markers related to those of 10–12 2−+ Ca. Argoarchaeum at deep-sea gas seeps suggests that archaea 4C 26H(g) ++7SO14 4H →+8CO(22g) 7H S(aq.+)12H2O that are able to oxidize ethane through ethyl-CoM are widespread members of the local communities fostered by venting gaseous Δ=G′ −.73 2kJper molethane alkanes around these seeps. Natural gas venting from deep marine horizons towards the sediment Grown Ethane12 cultures were turbid and light microscopy revealed surface is a potent source of energy and carbon for microbial commu- small single cocci (with a diameter of around 0.5 μm) as the abundant nities using various electron acceptors (or ‘oxidants’). The high abun- morphotype. Amplicon and metagenome sequencing consistently dance of sulfate in seawater (a concentration of 28 mM; by contrast, retrieved a distinct archaeal phylotype affiliated with the anaerobic the concentration of oxygen is approximately 0.3 mM) often results in methanotrophic (ANME)-2d cluster of Methanosarcinales (Fig. 1b extended anoxic subsurface zones that are shaped by the reduction of and Supplementary Table 1). This phylotype, named Eth-Arch1, sulfate to sulfide13. Here, anaerobic oxidation of methane (AOM) is a constituted on average 65% of the total number of cells (Fig. 2a, b prominent process carried out by various archaea14–16. According to and Supplementary Table 2). Cells of the Eth-Arch1 phylotype grew geochemical depth profiles, ethane, propane, n-butane and iso-butane mostly unattached. Many formed protruding smaller vesicular struc- (non-methane alkanes) may also be biodegraded1–3. Involved micro- tures that had DAPI and catalysed reporter deposition–fluorescence organisms have been identified so far for the degradation of propane in situ hybridization (CARD–FISH) signals (Fig. 2f–h and Extended and n-butane, and are either bacteria or archaea6,9,17,18. Like the AOM Data Fig. 1), suggesting division by budding, which is an alternative archaea, those that oxidize propane and butane also depend on cell-division mechanism found across major archaeal phyla26. In syntrophic interactions with sulfate-reducing bacteria9,19,20. The acti- addition, two phylotypes of Desulfosarcina-affiliated sulfate-reducing vation of propane and butane in the archaea apparently involves the bacteria (SRB) were identified, Eth-SRB1 and Eth-SRB2, each 1Department of Isotope Biogeochemistry, Helmholtz Centre for Environmental Research – UFZ, Leipzig, Germany. 2State Key Laboratory of Urban and Regional Ecology, Research Center for Eco- Environmental Sciences, Chinese Academy of Sciences, Beijing, China. 3Department of Analytical Chemistry, Helmholtz Centre for Environmental Research – UFZ, Leipzig, Germany. 4Department of Environmental Microbiology, Helmholtz Centre for Environmental Research – UFZ, Leipzig, Germany. 5Max Planck Institute for Marine Microbiology, Bremen, Germany. 6Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, China. 7Department of Marine Sciences, University of Georgia, Athens, GA, USA. 8Present address: Department for Research Infrastructures, The Research Council of Norway, Oslo, Norway. *e-mail: [email protected] 108 | NATURE | VOL 568 | 4 APRIL 2019 LETTER RESEARCH ab5 Archaeoglobales Guaymas Basin sediment (KJ569648) Ca. A. ethanivorans Amsterdam mud volcano (FJ649528) ANME-1 Ca. M. nitroreducens 4 Ca. Methanoperedens sp. BLZ1 ) –1 Ca. S. butanivorans l ANME-2ab Ca. S. caldarius 3 GoM-Arch 87 Methanosarcinaceae ANME-2c Methanocellales M. shengliensis ANME-3 Methanosaeta 0.1 2 Methanomicrobiales Desulfobacteraceae Hydrate Ridge (AM229186) Ethane, sulde (mmol Gulf of Cadiz (FJ813539) Seabed sediment (HE803866) Eth-SRB1 Eth-SRB2 1 c Hydrothermal seep (KP091115) Gulf of Mexico sediment (AM745215) Desulfococcus oleovorans Hxd3 Desulfococcus multivorans DSM 2059 Desulfosarcina sp. BuS5 0 Desulfosarcina cetonica JCM 12296 Butane12-HyR 050 100 150 200 250 300 350 Desulfosarcina variabilis Propane12-GMe 0.05 Time (days) Desulfatibacillum alkenivorans AK-01 Fig. 1 | Ethane oxidation with sulfate and major 16S rRNA gene diamonds). Similar results were obtained with n = 4 biological replicates. phylotypes. a, The Ethane12 culture oxidized ethane (two different starting b, Candidatus Argoarchaeum ethanivorans is affiliated with a lineage of concentrations of ethane; black and grey diamonds, 2.7 and 1.6 mmol l−1, uncultured Methanosarcinales. c, Eth-SRB1 and Eth-SRB2 share over 95% respectively) while reducing sulfate to sulfide (corresponding black and 16S rRNA gene identity and belong to the marine SEEP-SRB1 group of the grey circles). Cultures without ethane did not produce sulfide (white Desulfosarcina–Desulfococcus clade. Filled circles on branch nodes indicate circles). Ethane concentrations were stable in sterile incubations (white bootstrap values >60%; scale bars, nucleotide subsitutions per site (b, c). − accounting for about 15% of the total number of cells (Figs. 1c, 2a, b and ethenesulfonate (C2H3O3S ), respectively. Identical mass peaks and Supplementary Table 2). Their cells were morphologically distinct, and fragments were obtained with synthetic ethyl-CoM (Fig. 3b, c). appearing as slightly curved rods (1.0–1.5 μm by 0.3 μm) and larger These findings were further corroborated by liquid chromatography– ellipsoids (2.0–2.5 μm by 1 μm), respectively; they were also found tandem mass spectrometry (LC–MS/MS) analyses, yielding identical predominantly as single cells (Fig. 2a, b). An estimated 10% of the total retention time and mass transitions for extracted metabolites and the culture biomass occurred as archaeal–bacterial aggregates (Fig. 2c–e). synthetic standard (Fig. 3d–f). Because the abundance of the archaeal phylotype
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