Abstract

The anaerobic formation and oxidation of methane involve unique enzymatic mechanisms and cofactors, all of which are believed to be specific for C1-compounds. Here we show that an anaerobic thermophilic enrichment culture composed of dense consortia of archaea and bacteria apparently uses partly similar pathways to oxidize the C4 hydrocarbon butane. The archaea, proposed genus ‘Candidatus Syntrophoarchaeum’, show the characteristic autofluorescence of methanogens, and contain highly expressed genes encoding enzymes similar to methyl-coenzyme M reductase. We detect butyl-coenzyme M, indicating archaeal butane activation analogous to the first step in anaerobic methane oxidation. In addition, Ca. Syntrophoarchaeum expresses the genes encoding β-oxidation enzymes, carbon monoxide dehydrogenase and reversible C1 methanogenesis enzymes. This allows for the complete oxidation of butane. Reducing equivalents are seemingly channelled to HotSeep-1, a thermophilic sulfate-reducing partner bacterium known from the anaerobic oxidation of methane. Genes encoding 16S rRNA and methyl-coenzyme M reductase similar to those identifying Ca. Syntrophoarchaeum were repeatedly retrieved from marine subsurface sediments, suggesting that the presented activation mechanism is naturally widespread in the anaerobic oxidation of short-chain hydrocarbons.

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Acknowledgements

We thank R. Appel, K. Büttner, I. Kattelmann and S. Menger for assistance in cultivation and molecular work, B. Scheer for proteomic analyses, and M. Sickert, J. Then Bergh and K. Dürkop for support in standard synthesis and LC-MS/MS analyses. We thank as well A. Férnandez-Guerra, H. Gruber-Vodicka and P. Offre for supporting us with bioinformatics and biochemistry. We thank A. Boetius for discussions and financial support provided by her Leibniz Grant of the Deutsche Forschungsgemeinschaft (DFG). Research was further financed by the DFG Research Center and Cluster of Excellence MARUM and the Deep Carbon Observatory (Deep Life grant 11121/6152-2121-2329-9973-CC to G.W.), the Max Planck Society and the Helmholtz Society. We are indebted to A. Teske and the shipboard party, the crew and pilots of research expedition AT15-16 Research Vessel Atlantis and Research Submersible Alvin (NSF Grant OCE-0647633). We acknowledge the Centre for Chemical Microscopy (ProVIS) at the Helmholtz Centre for Environmental Research supported by European regional Development Funds (EFRE – Europe funds Saxony) for using their analytical facilities.

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Author notes

    • Katie J. Harding

    Present address: University of California at Santa Cruz, Ocean Sciences Department, Santa Cruz, California 95064, USA.

Affiliations

  1. Max-Planck Institute for Marine Microbiology, 28359 Bremen, Germany

    • Rafael Laso-Pérez
    • , Gunter Wegener
    • , Katrin Knittel
    • , Friedrich Widdel
    • , Katie J. Harding
    • , Viola Krukenberg
    • , Dimitri V. Meier
    • , Michael Richter
    •  & Florin Musat
  2. Alfred Wegener Institute Helmholtz Center for Polar and Marine Research, 27570 Bremerhaven, Germany

    • Rafael Laso-Pérez
    • , Gunter Wegener
    • , Viola Krukenberg
    •  & Halina E. Tegetmeyer
  3. MARUM, Center for Marine Environmental Sciences, University Bremen, 28359 Bremen, Germany

    • Gunter Wegener
  4. Center for Biotechnology, Bielefeld University, 33615 Bielefeld, Germany

    • Halina E. Tegetmeyer
  5. Max Planck Institute for Biophysical Chemistry, 37077 Göttingen, Germany

    • Dietmar Riedel
  6. Helmholtz Centre for Environmental Research − UFZ, 04318 Leipzig, Germany

    • Hans-Hermann Richnow
    • , Lorenz Adrian
    • , Thorsten Reemtsma
    • , Oliver J. Lechtenfeld
    •  & Florin Musat

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Contributions

G.W. and F.M. retrieved the original samples and performed cultivation. R.L.-P., G.W. and F.M. designed research. R.L.-P., K.K., K.J.H. and V.K. designed the CARD-FISH probes and performed microscopy. R.L.-P., G.W. and F.M. performed physiological experiments. H.E.T. prepared and sequenced the DNA and RNA libraries. R.L.-P., V.K., D.V.M. and M.R. performed metagenomic and transcriptomic analyses. R.L.-P., K.K. and K.J.H. performed phylogenetic analysis. D.R. performed thin-sectioning and electron microscopy. H.-H.R., L.A. and F.M. performed proteome analyses. T.R., O.J.L. and F.M. analysed metabolic intermediates. R.L.-P., G.W., F.W. and F.M. developed the metabolic model, and wrote the manuscript with contributions of all co-authors.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Gunter Wegener or Florin Musat.

Reviewer Information

Nature thanks T. Ettema, M. Jetten, S. Ragsdale and R. Thauer for their contribution to the peer review of this work.

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