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Published Version (PDF 1MB) This may be the author’s version of a work that was submitted/accepted for publication in the following source: Vanwonterghem, Inka, Evans, Paul N., Parks, Donovan H., Jensen, Paul D., Woodcroft, Ben J., Hugenholtz, Philip, & Tyson, Gene W. (2016) Methylotrophic methanogenesis discovered in the archaeal phylum Ver- straetearchaeota. Nature Microbiology, 1, Article number: 161701-9. This file was downloaded from: https://eprints.qut.edu.au/200369/ c 2016 Macmillan Publishing Limiited This work is covered by copyright. Unless the document is being made available under a Creative Commons Licence, you must assume that re-use is limited to personal use and that permission from the copyright owner must be obtained for all other uses. If the docu- ment is available under a Creative Commons License (or other specified license) then refer to the Licence for details of permitted re-use. It is a condition of access that users recog- nise and abide by the legal requirements associated with these rights. If you believe that this work infringes copyright please provide details by email to [email protected] License: Creative Commons: Attribution 4.0 Notice: Please note that this document may not be the Version of Record (i.e. published version) of the work. Author manuscript versions (as Sub- mitted for peer review or as Accepted for publication after peer review) can be identified by an absence of publisher branding and/or typeset appear- ance. If there is any doubt, please refer to the published source. https://doi.org/10.1038/nmicrobiol.2016.170 ARTICLES PUBLISHED: 3 OCTOBER 2016 | ARTICLE NUMBER: 16170 | DOI: 10.1038/NMICROBIOL.2016.170 OPEN Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota Inka Vanwonterghem1,2,PaulN.Evans1,DonovanH.Parks1,PaulD.Jensen2, Ben J. Woodcroft1, Philip Hugenholtz1 and Gene W. Tyson1* Methanogenesis is the primary biogenic source of methane in the atmosphere and a key contributor to climate change. The long-standing dogma that methanogenesis originated within the Euryarchaeota was recently challenged by the discovery of putative methane-metabolizing genes in members of the Bathyarchaeota, suggesting that methanogenesis may be more phylogenetically widespread than currently appreciated. Here, we present the discovery of divergent methyl- coenzyme M reductase genes in population genomes recovered from anoxic environments with high methane flux that belong to a new archaeal phylum, the Verstraetearchaeota. These archaea encode the genes required for methylotrophic methanogenesis, and may conserve energy using a mechanism similar to that proposed for the obligate H2-dependent methylotrophic Methanomassiliicoccales and recently described Candidatus ‘Methanofastidiosa’.Ourfindings indicate that we are only beginning to understand methanogen diversity and support an ancient origin for methane metabolism in the Archaea, which is changing our understanding of the global carbon cycle. ethanogenesis performed by anaerobic archaea represents ‘Methanofastidiosa’, which is restricted to methanogenesis the largest biogenic source of methane on Earth1–3. This through methylated thiol reduction10. The hypothesis that Mprocess is a key component of the global carbon cycle methane metabolism originated early in the evolution of the and plays an important role in climate change, owing to the high Euryarchaeota11 has recently been challenged following the discovery warming potential of methane4. Methanogenic archaea are wide- of putative methane metabolism in the archaeal phylum spread in nature and have been detected in a diverse range of Bathyarchaeota (formerly Miscellaneous Crenarchaeota Group)12,13. environments including wetlands, rice agriculture, landfills, hydro- Two near-complete genomes belonging to this phylum contain thermal vents, ruminants and termites1,2. Traditionally, all metha- distant homologues of the genes necessary for hydrogenotrophic nogens belonged to the archaeal phylum Euryarchaeota and until and methylotrophic methanogenesis, including the methyl-coenzyme recently were classified into seven orders1,3,5 (Methanobacteriales, M reductase complex (MCR)12.Thesefindings raise the possibility Methanococcales, Methanomicrobiales, Methanosarcinales, that further divergent methanogenic lineages await discovery. Methanocellales, Methanopyrales and Methanomassiliicoccales). mcrA Substrates for methane production include H2/CO2 (hydro- Discovery of a divergent cluster genotrophic), acetate (acetoclastic) and methylated compounds To enrich for novel methanogenic diversity, triplicate anaerobic (methylotrophic)5. Hydrogenotrophic methanogenesis is the most digesters were inoculated with a mixture of samples sourced from widespread1, being found in all methanogenic orders with the natural (rumen and lake sediment) and engineered (anaerobic diges- exception of Methanomassiliicoccales, and it has been suggested ters and lagoon) environments, and supplied with alpha cellulose. that this is the ancestral form of methane production6. Although The reactors showed stable methane production and were sampled the prevailing source of atmospheric methane is through direct over time. Six metagenomes comprising a total of 111 Gb were gen- acetate cleavage7, only members of the Methanosarcinales are erated and co-assembled14 (Supplementary Table 1), and differential capable of acetoclastic methanogenesis5,7. Methylotrophic methano- coverage binning recovered 68 substantially to near-complete popu- gens are found in the orders Methanosarcinales, Methanobacteriales lation genomes, including four containing mcrA genes. The homo- and Methanomassiliicoccales, and can be classified in two groups logues in three of these genomes are closely related to recognized based on the presence or absence of cytochromes. Methylotrophs methanogenic lineages in the Euryarchaeota (94–99% amino acid without cytochromes are obligately H2-dependent, while those that (aa) identity), while the fourth genome (V1) encodes an mcrA that possess cytochromes (that is, members of the Methanosarcinales), is divergent from extant sequences (∼68% aa identity). This divergent 15 can also oxidize methyl groups to CO2 via a membrane-bound mcrA was used to screen the Sequence Read Archive (SRA) ,and electron transport chain5. closely related mcrA genes (85–100% aa identity, Supplementary Our knowledge of methanogenic substrate utilization and energy Table2)wereidentified in three metagenomic data sets obtained conservation is still incomplete but is rapidly expanding through the from high methane flux habitats: an anaerobic digester treating development of new molecular techniques such as genome-centric palm oil mill effluent (Malaysia)16, an iso-alkane degrading methano- metagenomics. This includes the discovery of hydrogenotrophic genic enrichment culture from tailings ponds (Mildred Lake Settling methanogenesis genes encoded in Methanosaeta8, a genus originally Basin, Canada)17, and formation waters of coalbed methane wells thought to be strictly acetoclastic, the hypothesized mode of energy (CD-8 and PK-28) located within the Surat Basin (Queensland, metabolism in Methanonomassiliiccocales5,9, and the recently Australia)12 (Supplementary Table 1). Subsequent assembly and described sixth class of euryarchaeotal methanogens, Candidatus binning of these data sets led to the recovery of four additional 1Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, Queensland 4072, Australia. 2Advanced Water Management Centre, The University of Queensland, St Lucia, Queensland 4072, Australia. *e-mail: [email protected] NATURE MICROBIOLOGY | VOL 1 | DECEMBER 2016 | www.nature.com/naturemicrobiology 1 © 2016 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. ARTICLES NATURE MICROBIOLOGY DOI: 10.1038/NMICROBIOL.2016.170 Table 1 | Summary statistics of the Verstraetearchaeota genomes. Genome Environment Size Scaffolds N50 Genes GC CD Compl. Cont. Strain aa (Mb) (no.) (bp) (no.) (%) (%) (%) (%) (%) (no.) V1 Cellulose degrading anaerobic 1.6 88 34,490 1,578 58.1 88 90.3 0.9 0 18 digester V2 Palm oil mill effluent degrading 1.7 11 258,701 1,758 57.6 88.5 99.1 0.9 0 18 anaerobic digester V3 Iso-alkane degrading 1.4 86 24,381 1,550 55.4 87.4 99.1 0.9 0 18 enrichment from tailings ponds V4 Formation water from coalbed 1.4 84 20,373 1,423 55.8 87.3 91.6 0.0 0 21 methane well (CD-8) V5 Formation water from coalbed 1.2 295 2,926 1,248 55.4 83.5 60.2 0.0 0 21 methane well (PK-28) Genome ID, habitat, estimated size, number of scaffolds, N50, number of genes, guanine-cytosine (GC) content, coding density (CD), estimated completeness (Compl.), estimated contamination (Cont.), strain heterogeneity (Strain) and estimated number of amino acids (aa) are shown. abMethanobacteriales Methanococcales Methanococcales Methanobacteriales Thaumarchaeota Methanopyrus kandleri C. Methanofastidiosales Korarchaeota Methanomassiliicoccales Methanosarcinales Aigarchaeota V1–V2 Terrestrial Hot Spring Crenarchaeota Group V3 V4 C. Verstraetearchaeota Methanocellales Crenarchaeota V1; mesophilic anaerobic digester degrading cellulose C. Verstraetearchaeota V2; mesophilic anaerobic digester degrading palm oil mill effluent Methanomicrobiales V3; iso-alkane degrading methanogenic enrichment culture from tailings ponds Pav-sed-507, deep sediment (11 cm) of freshwater lake Pavin, TMCG SMS-sludge-13, mesophilic methanogenic granular sludge, TMCG V4; formation water from a coal bed methane well
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