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Crystal structure of a key enzyme for anaerobic ethane activation

Cedric J. Hahn https://orcid.org/0000-0002-2581-7215, Olivier N. Lemaire https://orcid.org/0000-0002-4389-5786, Jörg Kahnt, Sylvain Engilberge https://orcid.org/0000-0001-8680-6790, Gunter Wegener https://orcid.org/0000-0002-6819-373X [email protected], and Tristan Wagner https://orcid.org/0000-0002-3382-8969 [email protected]Authors Info & Affiliations
Science
2 Jul 2021
Vol 373, Issue 6550
pp. 118-121
DOI: 10.1126/science.abg1765
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How to feed an enzyme ethane

When released from ocean floor seeps, small hydrocarbons are rapidly consumed by micro-organisms. Methane is highly abundant and is both produced and consumed by microbes through well understood biochemical pathways. Less well understood is how ethane, also a major natural component of gaseous hydrocarbons, is metabolized. To understand how microbes take advantage of this energy and carbon source, Hahn et al. solved the x-ray crystal structures of an enzyme they call ethyl coenzyme-M reductase, which converts ethane into the thioether ethyl-coenzyme M as the entry point for catabolism. They found an expanded active site and, using a xenon gas derivatization experiment, a distinctive tunnel through the protein that is proposed to permit access of the gaseous substrate.
Science, abg1765, this issue p. 118

Abstract

Ethane, the second most abundant hydrocarbon gas in the seafloor, is efficiently oxidized by anaerobic archaea in syntrophy with sulfate-reducing bacteria. Here, we report the 0.99-angstrom-resolution structure of the proposed ethane-activating enzyme and describe the specific traits that distinguish it from methane-generating and -consuming methyl-coenzyme M reductases. The widened catalytic chamber, harboring a dimethylated nickel-containing F430 cofactor, would adapt the chemistry of methyl-coenzyme M reductases for a two-carbon substrate. A sulfur from methionine replaces the oxygen from a canonical glutamine as the nickel lower-axial ligand, a feature conserved in thermophilic ethanotrophs. Specific loop extensions, a four-helix bundle dilatation, and posttranslational methylations result in the formation of a 33-angstrom-long hydrophobic tunnel, which guides the ethane to the buried active site as confirmed with xenon pressurization experiments.

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Supplementary Material

Summary

Materials and Methods
Supplementary Text
Figs. S1 to S16
Tables S1 to S3
References (36–58)

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Volume 373 | Issue 6550
2 July 2021

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Received: 15 December 2020
Accepted: 28 May 2021
Published in print: 2 July 2021

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Acknowledgments

We thank the Max Planck Institute for Marine Microbiology and the Max-Planck-Society for continuous support. We thank the SOLEIL and SLS synchrotrons for beam time allocation and the respective beamline staffs of Proxima-1 and X06DA for assistance with data collection, with specific regards to P. Legrand. We also acknowledge C. Probian and R. Appel for their continuous support in the Microbial Metabolism laboratory. We are thankful to R. Amann and R. K. Thauer for their critical views on the manuscript and their stimulating discussions. We thank K. Knittel for her inputs during a regular exchange. We thank A. Teske for organizing the sampling campaign of the Guaymas Basin hydrothermal vents (NSF grant 1357238). Funding: Additional funds came from the Deutsche Forschungsgemeinschaft funding the Cluster of Excellence “The Ocean Floor—Earth’s Uncharted Interface” (EXC-2077–390741603) at MARUM, University Bremen. S.E. was granted by SNF grant 200021_182369. Author contributions: C.J.H., O.N.L., G.W., and T.W. designed the research. C.J.H., O.N.L., and G.W. performed cultivation and culture experiments. C.J.H., O.N.L., and T.W. purified and crystallized the proteins. S.E., O.N.L., and T.W. collected x-ray data and built the models. O.N.L. and T.W. analyzed the structures. S.E. and T.W. performed and analyzed the xenon-pressurization experiments. J.K., O.N.L., and T.W. analyzed the F430 cofactor and posttranslational modifications. C.J.H., O.N.L., G.W., and T.W. interpreted the data and wrote the paper, with contributions and final approval of all co-authors. Competing interests: The authors declare no competing interests. Data and materials availability: All structures were validated and deposited in the Protein Data Bank (PDB) under the following accession numbers: 7B1S, native ethyl-coenzyme M reductase from Ca. E. thermophilum; 7B2C, Xenon-pressurized ethyl-coenzyme M reductase from Ca. E. thermophilum and 7B2H, Xenon-pressurized methyl-coenzyme M reductase from M. marburgensis. Raw and processed data for x-ray crystallography and mass spectrometry experiments are hosted at Zenodo (35). All other data are available in the manuscript or the supplementary materials.

Authors

Affiliations

Cedric J. Hahn† https://orcid.org/0000-0002-2581-7215
Max Planck Institute for Marine Microbiology, Bremen 28359, Germany.
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Olivier N. Lemaire† https://orcid.org/0000-0002-4389-5786
Max Planck Institute for Marine Microbiology, Bremen 28359, Germany.
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Jörg Kahnt
Max Planck Institute for Terrestrial Microbiology, Marburg, Germany.
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Sylvain Engilberge https://orcid.org/0000-0001-8680-6790
Paul Scherrer Institute (PSI), Villigen PSI, Villigen, Switzerland.
Present address: European Synchrotron Radiation Facility (ESRF), Grenoble, France.
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Gunter Wegener* https://orcid.org/0000-0002-6819-373X [email protected]
Max Planck Institute for Marine Microbiology, Bremen 28359, Germany.
Center for Marine Environmental Sciences (MARUM), University of Bremen, Bremen, Germany.
Alfred Wegener Institute Helmholtz Center for Polar and Marine Research, Bremerhaven, Germany.
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Tristan Wagner* https://orcid.org/0000-0002-3382-8969 [email protected]
Max Planck Institute for Marine Microbiology, Bremen 28359, Germany.
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Funding Information

Deutsche Forschungsgemeinschaft: EXC-2077 – 390741603
Max Planck Gesellschaft

Notes

*
Corresponding author. Email: [email protected] (G.W.); [email protected] (T.W.)
†
These authors contributed equally to the work.

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