Divergent methyl-coenzyme M reductase genes in a deep-subseafloor Archaeoglobi

Creators: Boyd, Joel A.; Jungbluth, Sean P.; Leu, Andy O.; Evans, Paul N.; Woodcroft, Ben J.; Chadwick, Grayson L.; Orphan, Victoria J.; Amend, Jan P.; Rappé, Michael S.; Tyson, Gene W.

Abstract

The methyl-coenzyme M reductase (MCR) complex is a key enzyme in archaeal methane generation and has recently been proposed to also be involved in the oxidation of short-chain hydrocarbons including methane, butane, and potentially propane. The number of archaeal clades encoding the MCR continues to grow, suggesting that this complex was inherited from an ancient ancestor, or has undergone extensive horizontal gene transfer. Expanding the representation of MCR-encoding lineages through metagenomic approaches will help resolve the evolutionary history of this complex. Here, a near-complete Archaeoglobi metagenome-assembled genome (MAG; Ca. Polytropus marinifundus gen. nov. sp. nov.) was recovered from the deep subseafloor along the Juan de Fuca Ridge flank that encodes two divergent McrABG operons similar to those found in Ca. Bathyarchaeota and Ca. Syntrophoarchaeum MAGs. Ca. P. marinifundus is basal to members of the class Archaeoglobi, and encodes the genes for β-oxidation, potentially allowing an alkanotrophic metabolism similar to that proposed for Ca. Syntrophoarchaeum. Ca. P. marinifundus also encodes a respiratory electron transport chain that can potentially utilize nitrate, iron, and sulfur compounds as electron acceptors. Phylogenetic analysis suggests that the Ca. P. marinifundus MCR operons were horizontally transferred, changing our understanding of the evolution and distribution of this complex in the Archaea.

Additional Information

© 2019 The Author(s). This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 07 October 2018; Revised 29 November 2018; Accepted 11 December 2018; Published 16 January 2019. Code availability: All unpublished software used in this publication are available on github; sequence_windower (https://github.com/geronimp/window_sequence); EnrichM (github.com/geronimp/enrichM); GenomeTreeTK (github.com/dparks1134/GenomeTreeTk); CompareM v0.0.22 (https://github.com/dparks1134/CompareM); fastacxxch.count.py, (github.com/geronimp/HandyScripts/blob/master/99_random/fastacxxch.count.py); FinishM (v0.0.7 github.com/wwood/finishm). GTDB-Tk (github.com/Ecogenomics/GTDBTk). Data availability: The datasets analysed during the current study are available in the NCBI SRA, accession number SRR3723048. The Candidatus "Polytropus marinifundus" genome is available under the NCBI bioproject SAMN10474933. All alignments and phylogenetic trees are available in the Supplementary Files 1–20. We thank the captain and crew, A. Fisher, K. Becker, C. G. Wheat, and other members of the science teams on board R/V Atlantis cruise AT18-07. We also thank the pilots and crew of remote-operated vehicle Jason II. This research was supported by two grants from the National Science Foundation: Microbial Observatories (MCB06-04014 to MSR), and the Science and Technology Center for Dark Energy Biosphere Investigations (C-DEBI; OCE-0939564 to JPA). This study used samples and data provided by the Integrated Ocean Drilling Program. This material is based upon work supported by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research program under Award Number. Genomic Science Program of the United States Department of Energy Office of Biological and Environmental Research (DE-SC0016469, DE-SC0010580, DE-SC0016440); Australian Research Council (ARC) Future Fellowship (FT170100070 to G.W.T.); ARC Postgraduate Award (to JAB); ARC Discovery Early Career Researcher Award (DECRA; DE-160100248 to BJW); ARC DECRA (DE-170100428 to PNE). Author contributions: JAB and SPJ contributed equally to this work. MSR, JPA, and GWT designed the overall study and procured funding. JAB, SPJ, MSR, and GWT designed and carried out experiments and analyses around specific microbial hypotheses. JAB, SPJ, and GWT wrote the manuscript. All authors edited, reviewed and approved the final manuscript. The authors declare that they have no conflict of interest.

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