Original Article

The ISME Journal (2016) 10, 2478–2487; doi:10.1038/ismej.2016.33; published online 4 March 2016

Chasing the elusive Euryarchaeota class WSA2: genomes reveal a uniquely fastidious methyl-reducing methanogen

Masaru Konishi Nobu1,2, Takashi Narihiro2, Kyohei Kuroda1,3, Ran Mei1 and Wen-Tso Liu1

  1. 1Department of Civil and Environmental Engineering, University of Illinois, Urbana-Champaign, Urbana, IL, USA
  2. 2Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, Japan
  3. 3Department of Environmental Systems Engineering, Nagaoka University of Technology, Nagaoka, Japan

Correspondence: W-T Liu, Department of Civil and Environmental Engineering, University of Illinois, Urbana-Champaign, 205N. Mathews Ave., Urbana, IL 61801, USA. E-mail: wtliu@illinois.edu

Received 22 October 2015; Revised 22 January 2016; Accepted 29 January 2016
Advance online publication 4 March 2016

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Abstract

The ecophysiology of one candidate methanogen class WSA2 (or Arc I) remains largely uncharacterized, despite the long history of research on Euryarchaeota methanogenesis. To expand our understanding of methanogen diversity and evolution, we metagenomically recover eight draft genomes for four WSA2 populations. Taxonomic analyses indicate that WSA2 is a distinct class from other Euryarchaeota. None of genomes harbor pathways for CO2-reducing and aceticlastic methanogenesis, but all possess H2 and CO oxidation and energy conservation through H2-oxidizing electron confurcation and internal H2 cycling. As the only discernible methanogenic outlet, they consistently encode a methylated thiol coenzyme M methyltransferase. Although incomplete, all draft genomes point to the proposition that WSA2 is the first discovered methanogen restricted to methanogenesis through methylated thiol reduction. In addition, the genomes lack pathways for carbon fixation, nitrogen fixation and biosynthesis of many amino acids. Acetate, malonate and propionate may serve as carbon sources. Using methylated thiol reduction, WSA2 may not only bridge the carbon and sulfur cycles in eutrophic methanogenic environments, but also potentially compete with CO2-reducing methanogens and even sulfate reducers. These findings reveal a remarkably unique methanogen ‘Candidatus Methanofastidiosum methylthiophilus’ as the first insight into the sixth class of methanogens ‘Candidatus Methanofastidiosa’.