Expanding anaerobic alkane metabolism in the domain of Archaea

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Abstract

Methanogenesis and anaerobic methane oxidation through methyl-coenzyme M reductase (MCR) as a key enzyme have been suggested to be basal pathways of archaea1. How widespread MCR-based alkane metabolism is among archaea, where it occurs and how it evolved remain elusive. Here, we performed a global survey of MCR-encoding genomes based on metagenomic data from various environments. Eleven high-quality mcr-containing metagenomic-assembled genomes were obtained belonging to the Archaeoglobi in the Euryarchaeota, Hadesarchaeota and different TACK superphylum archaea, including the Nezhaarchaeota, Korarchaeota and Verstraetearchaeota. Archaeoglobi WYZ-LMO1 and WYZ-LMO3 and Korarchaeota WYZ-LMO9 encode both the (reverse) methanogenesis and the dissimilatory sulfate reduction pathway, suggesting that they have the genomic potential to couple both pathways in individual organisms. The Hadesarchaeota WYZ-LMO4–6 and Archaeoglobi JdFR-42 encode highly divergent MCRs, enzymes that may enable them to thrive on non-methane alkanes. The occurrence of mcr genes in different archaeal phyla indicates that MCR-based alkane metabolism is common in the domain of Archaea.

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Fig. 1: Classification of the 12 described MAGs.
Fig. 2: Phylogenetic affiliations of the McrA, McrB and McrG protein sequences of the 12 studied archaeal MAGs.
Fig. 3: Alkane metabolic schemes of the studied MAGs with previously unidentified mcr genes.

Code availability

All scripts and analyses necessary to perform metagenome processing can be accessed from GitHub (https://github.com/) or the websites provided in the original research articles. The specific links to the custom software are listed below: DIAMOND version 0.8.28.90: http://ab.inf.uni-tuebingen.de/software/diamond/, Sickle version 1.33: https://github.com/najoshi/sickle, MEGAHIT version 1.0.6-hotfix1: https://hku-bal.github.io/megabox/, Bowtie version 2.2.8: http://bowtie-bio.sourceforge.net/bowtie2/index.shtml, Prodigal version 2.6.3: http://compbio.ornl.gov/prodigal/, MaxBin version 2.2.4: http://sourceforge.net/projects/maxbin/, MetaBAT version 2.12.1: https://bitbucket.org/berkeleylab/metabat, CheckM version 1.0.7: http://ecogenomics.github.io/CheckM, compareM version 0.0.23: https://github.com/dparks1134/CompareM, MAFFT version 7.313: https://mafft.cbrc.jp/alignment/software/, trimAl version 1.4.rev2: http://trimal.cgenomics.org, IQ-Tree version 1.6.6: http://www.cibiv.at/software/iqtree, and RAxML version 8.0: https://github.com/stamatak/standard-RAxML.

Data availability

The data sets generated and/or analysed during the current study are available in the NCBI repository at https://www.ncbi.nlm.nih.gov/. The MAGs from the current study have been deposited in the NCBI GenBank under the project ID PRJNA475886.

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Acknowledgements

We thank R. K. Thauer for his advice on the discussed metabolic pathways, and V. Krukenberg and J. Wang for valuable discussion and suggestions for the manuscript. We are grateful to the researchers who published their sequence data on the NCBI (https://www.ncbi.nlm.nih.gov/), and to the US Department of Energy Joint Genome Institute (http://www.jgi.doe.gov/) for providing protein sequence files in collaboration with the user community. We thank the following sources for funding: the Natural Science Foundation of China (grant numbers 91751205, 41525011 and 91428308), the National Key R&D project of China (grant number 2018YFC0309800) and China Postdoctoral Science Foundation Grant (grant number 2018T110390). This study is also a contribution to the Deep Carbon Observatory.

Author information

Y.W. and F.W. designed the research, performed the analyses, developed the metabolic models and wrote the paper. G.W. developed the metabolic models and wrote the paper. J.H. provided useful discussion and helped with the double-blind assessments of the MAGs. F.W. and X.X. provided guidance and useful suggestion.

Correspondence to Fengping Wang or Xiang Xiao.

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Wang, Y., Wegener, G., Hou, J. et al. Expanding anaerobic alkane metabolism in the domain of Archaea. Nat Microbiol 4, 595–602 (2019) doi:10.1038/s41564-019-0364-2

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