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Nature 450, 879-882 (6 December 2007) | doi:10.1038/nature06411; Received 13 August 2007; Accepted 24 October 2007; Published online 14 November 2007

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Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia

Peter F. Dunfield1,9, Anton Yuryev2, Pavel Senin3,4, Angela V. Smirnova1, Matthew B. Stott1, Shaobin Hou3,4, Binh Ly3,4, Jimmy H. Saw3, Zhemin Zhou5, Yan Ren5, Jianmei Wang5, Bruce W. Mountain1, Michelle A. Crowe1, Tina M. Weatherby6, Paul L. E. Bodelier7, Werner Liesack8, Lu Feng5, Lei Wang5 & Maqsudul Alam3,4

  1. GNS Science, Extremophile Research Group, Private Bag 2000, Taupo, New Zealand
  2. Ariadne Genomics, Inc., 9430 Key West Avenue no. 113, Rockville, Maryland 20850, USA
  3. Department of Microbiology, University of Hawaii, Snyder Hall no. 207, 2538 The Mall, Honolulu, Hawaii 96822, USA
  4. Advanced Studies in Genomics, Proteomics and Bioinformatics, College of Natural Sciences, Keller Hall 319, 2565 McCarthy Mall, Honolulu, Hawaii 96822, USA
  5. TEDA School of Biological Sciences and Biotechnology, Nankai University, 23 HongDa Street, Tianjin 300457, China
  6. Biological Electron Microscopy Facility, Pacific Biosciences Research Center, University of Hawaii at Manoa, Snyder Hall no. 118, Honolulu, Hawaii 96822, USA
  7. Netherlands Institute of Ecology (NIOO-KNAW), Centre for Limnology, Department of Microbial Wetland Ecology, Rijksstraatweg 6, 3631 AC, Nieuwersluis, The Netherlands
  8. Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Strasse, 35043 Marburg, Germany
  9. Present address: Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, Alberta, T2N 1N4, Canada.

Correspondence to: Peter F. Dunfield1,9Lei Wang5Maqsudul Alam3,4 Correspondence and requests for materials should be addressed to P.D. (Email: p.dunfield@gns.cri.nz), M.A. (Email: alam@hawaii.edu) or L.W. (Email: wanglei@nankai.edu.cn).

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Aerobic methanotrophic bacteria consume methane as it diffuses away from methanogenic zones of soil and sediment1. They act as a biofilter to reduce methane emissions to the atmosphere, and they are therefore targets in strategies to combat global climate change. No cultured methanotroph grows optimally below pH 5, but some environments with active methane cycles are very acidic2, 3. Here we describe an extremely acidophilic methanotroph that grows optimally at pH 2.0–2.5. Unlike the known methanotrophs, it does not belong to the phylum Proteobacteria but rather to the Verrucomicrobia, a widespread and diverse bacterial phylum that primarily comprises uncultivated species with unknown genotypes. Analysis of its draft genome detected genes encoding particulate methane monooxygenase that were homologous to genes found in methanotrophic proteobacteria. However, known genetic modules for methanol and formaldehyde oxidation were incomplete or missing, suggesting that the bacterium uses some novel methylotrophic pathways. Phylogenetic analysis of its three pmoA genes (encoding a subunit of particulate methane monooxygenase) placed them into a distinct cluster from proteobacterial homologues. This indicates an ancient divergence of Verrucomicrobia and Proteobacteria methanotrophs rather than a recent horizontal gene transfer of methanotrophic ability. The findings show that methanotrophy in the Bacteria is more taxonomically, ecologically and genetically diverse than previously thought, and that previous studies have failed to assess the full diversity of methanotrophs in acidic environments.