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Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia

Nature volume 450, pages 879–882 (2007)Cite this article

Abstract

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.

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Figure 1: Vertical profiles of methane partial pressures (open circles), O 2 partial pressures (open triangles) and temperature (filled diamonds) in a geothermal soil.
Figure 2: D 600 (open diamonds), methane consumption (open circles), and O 2 consumption (open triangles) of isolate V4 growing in liquid medium at pH 1.5 and 50 °C.
Figure 3: Growth rate constant based on D 600 (open circles) and average methane consumption rates (filled circles) of isolate V4 at a range of pH values.
Figure 4: Transmission electron micrographs of internal membrane structures observed in some cells of Verrucomicrobia isolate V4.
Figure 5: Phylogenetic tree constructed from derived PmoA and AmoA sequences (subunits of particulate methane monooxygenase or ammonia monooxygenase), showing the relative positions of the three sequences from Verrucomicrobia isolate V4.

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Acknowledgements

We thank S. Dedysh, J. C. Murrell and J. Euzéby for comments; A. Malahoff for supporting this research programme; and the Tikitere Trust for permission to sample at Hell’s Gate. This work was supported in part by the Wairakei Environmental Mitigation Charitable Trust (P.D.). The genome analysis was funded by the US Department of Defense (M.A.). Gene sequences referenced in this paper are deposited DDBJ/EMBL/GenBank under accession numbers AM900833–AM900834 and EU223838–EU223931.

Author Contributions P.F.D., B.W.M., M.A.C. and M.B.S. performed field sampling, methane measurement and molecular 16S rRNA analyses. P.F.D. and M.B.S. isolated and characterized the culture. S.H., B.L., J.H.S., Z.Z., Y.R., J.W., L.F., M.B.S., L.W., W.L. and M.A. conducted genome sequencing. P.F.D., P.S., A.Y., A.V.S., J.S., P.S. and M.A. conducted genome analyses. T.M.W. and M.B.S. performed electron microscopy. P.B. undertook phospholipid fatty-acid analysis.

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  1. Peter F. Dunfield

    Present address: Present address: Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, Alberta, T2N 1N4, Canada.,

Authors and Affiliations

  1. GNS Science, Extremophile Research Group, Private Bag 2000, Taupo, New Zealand ,

    Peter F. Dunfield, Angela V. Smirnova, Matthew B. Stott, Bruce W. Mountain & Michelle A. Crowe

  2. Ariadne Genomics, Inc., 9430 Key West Avenue no. 113, Rockville, Maryland 20850, USA ,

    Anton Yuryev

  3. Department of Microbiology, University of Hawaii, Snyder Hall no. 207, 2538 The Mall, Honolulu, Hawaii 96822, USA,

    Pavel Senin, Shaobin Hou, Binh Ly, Jimmy H. Saw & Maqsudul Alam

  4. Advanced Studies in Genomics, Proteomics and Bioinformatics, College of Natural Sciences, Keller Hall 319, 2565 McCarthy Mall, Honolulu, Hawaii 96822, USA ,

    Pavel Senin, Shaobin Hou, Binh Ly & Maqsudul Alam

  5. TEDA School of Biological Sciences and Biotechnology, Nankai University, 23 HongDa Street, Tianjin 300457, China ,

    Zhemin Zhou, Yan Ren, Jianmei Wang, Lu Feng & Lei Wang

  6. Biological Electron Microscopy Facility, Pacific Biosciences Research Center, University of Hawaii at Manoa, Snyder Hall no. 118, Honolulu, Hawaii 96822, USA ,

    Tina M. Weatherby

  7. Department of Microbial Wetland Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Centre for Limnology, Rijksstraatweg 6, 3631 AC, Nieuwersluis, The Netherlands,

    Paul L. E. Bodelier

  8. Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Strasse, 35043 Marburg, Germany ,

    Werner Liesack

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Correspondence to Peter F. Dunfield, Lei Wang or Maqsudul Alam.

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Supplementary information

Supplementary Information

The file contains Supplementary Figure 1 with Legend and Supplementary Tables 1-3. The Supplementary Figure 1 shows phylogenetic 16S rRNA gene tree showing the position of isolate V4 relative to other members of the phylum Verrucomicrobia and to proteobacterial methanotrophs. The Supplementary Table 1 illustrates putative genes involved in one-carbon metabolism in Verrucomicrobia isolate V4. The Supplementary Table 2 illustrates identities of partial segments (165 amino acids) of derived PmoA sequences in isolate V4 to PmoA and AmoA sequences of selected bacterial nitrifiers and methanotrophs, and the occurrence of proposed "signature" amino acid residues for either PmoA or AmoA. The Supplementary Table 3 illustrates phospholipid fatty acid profile of isolate V4. (PDF 479 kb)

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Dunfield, P., Yuryev, A., Senin, P. et al. Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 450, 879–882 (2007). https://doi.org/10.1038/nature06411

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