Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia
Huub J. M. Op den Camp
Department of Microbiology, IWWR, Radboud University Nijmegen, Toernooiveld 1, NL-6525 ED Nijmegen, The Netherlands.
Search for more papers by this authorTajul Islam
Department of Biology and Centre for Geobiology, University of Bergen, P.O. Box 7800, N-5020 Bergen, Norway.
Search for more papers by this authorMatthew B. Stott
GNS Science, Extremophile Research Group, Private Bag 2000, 3352 Taupo, New Zealand.
Search for more papers by this authorHarry R. Harhangi
Department of Microbiology, IWWR, Radboud University Nijmegen, Toernooiveld 1, NL-6525 ED Nijmegen, The Netherlands.
Search for more papers by this authorAlexander Hynes
Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, AB, Canada, T2N 1N4.
Search for more papers by this authorStefan Schouten
NIOZ Royal Netherlands Institute for Sea Research, Department of Marine Organic Biogeochemistry, P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands.
Search for more papers by this authorMike S. M. Jetten
Department of Microbiology, IWWR, Radboud University Nijmegen, Toernooiveld 1, NL-6525 ED Nijmegen, The Netherlands.
Search for more papers by this authorNils-Kåre Birkeland
Department of Biology and Centre for Geobiology, University of Bergen, P.O. Box 7800, N-5020 Bergen, Norway.
Search for more papers by this authorArjan Pol
Department of Microbiology, IWWR, Radboud University Nijmegen, Toernooiveld 1, NL-6525 ED Nijmegen, The Netherlands.
Search for more papers by this authorCorresponding Author
Peter F. Dunfield
Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, AB, Canada, T2N 1N4.
E-mail [email protected]; Tel: (+1) 403 220 2469; Fax (+1) 403 289 9311.Search for more papers by this authorHuub J. M. Op den Camp
Department of Microbiology, IWWR, Radboud University Nijmegen, Toernooiveld 1, NL-6525 ED Nijmegen, The Netherlands.
Search for more papers by this authorTajul Islam
Department of Biology and Centre for Geobiology, University of Bergen, P.O. Box 7800, N-5020 Bergen, Norway.
Search for more papers by this authorMatthew B. Stott
GNS Science, Extremophile Research Group, Private Bag 2000, 3352 Taupo, New Zealand.
Search for more papers by this authorHarry R. Harhangi
Department of Microbiology, IWWR, Radboud University Nijmegen, Toernooiveld 1, NL-6525 ED Nijmegen, The Netherlands.
Search for more papers by this authorAlexander Hynes
Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, AB, Canada, T2N 1N4.
Search for more papers by this authorStefan Schouten
NIOZ Royal Netherlands Institute for Sea Research, Department of Marine Organic Biogeochemistry, P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands.
Search for more papers by this authorMike S. M. Jetten
Department of Microbiology, IWWR, Radboud University Nijmegen, Toernooiveld 1, NL-6525 ED Nijmegen, The Netherlands.
Search for more papers by this authorNils-Kåre Birkeland
Department of Biology and Centre for Geobiology, University of Bergen, P.O. Box 7800, N-5020 Bergen, Norway.
Search for more papers by this authorArjan Pol
Department of Microbiology, IWWR, Radboud University Nijmegen, Toernooiveld 1, NL-6525 ED Nijmegen, The Netherlands.
Search for more papers by this authorCorresponding Author
Peter F. Dunfield
Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, AB, Canada, T2N 1N4.
E-mail [email protected]; Tel: (+1) 403 220 2469; Fax (+1) 403 289 9311.Search for more papers by this authorThe GenBank/EMBL/DDBJ accession numbers for the pmoA sequences of strain Kam1 are FJ462788-FJ462791; and for the xoxF gene of strain SolV: FJ477305.
Summary
Aerobic methanotrophic bacteria are capable of utilizing methane as their sole energy source. They are commonly found at the oxic/anoxic interfaces of environments such as wetlands, aquatic sediments, and landfills, where they feed on methane produced in anoxic zones of these environments. Until recently, all known species of aerobic methanotrophs belonged to the phylum Proteobacteria, in the classes Gammaproteobacteria and Alphaproteobacteria. However, in 2007–2008 three research groups independently described the isolation of thermoacidophilic methanotrophs that represented a distinct lineage within the bacterial phylum Verrucomicrobia. Isolates were obtained from geothermal areas in Italy, New Zealand and Russia. They are by far the most acidophilic methanotrophs known, with a lower growth limit below pH 1. Here we summarize the properties of these novel methanotrophic Verrucomicrobia, compare them with the proteobacterial methanotrophs, propose a unified taxonomic framework for them and speculate on their potential environmental significance. New genomic and physiological data are combined with existing information to allow detailed comparison of the three strains. We propose the new genus Methylacidiphilum to encompass all three newly discovered bacteria.
Supporting Information
Fig. S1. Comparison of the verrucomicrobial methane monooxygenases based on ligands to Cu and Zn.
Fig. S2. Phylogenetic relationship among deduced PmoB and AmoB proteins.
Fig. S3. Phylogenetic relationship among deduced PmoC and AmoC proteins.
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References
- Baani, M., and Liesack, W. (2008) Two isozymes of particulate methane monooxygenase with different methane oxidation kinetics are found in Methylocystis sp. strain SC2. Proc Natl Acad Sci USA 105: 10203–10208.
- Boschker, H.T.S., Nold, S.C., Wellsbury, P., Bos, D., de Graaf, W., Pel, R., et al. (1998) Direct linking of microbial populations to specific biogeochemical processes by 13C labelling of biomarkers. Nature 392: 801–805.
- Bowman, J.P., Sly, L.I., Nichols, P.D., and Hayward, A.C. (1993) Revised taxonomy of the methanotrophs: description of Methylobacter gen. nov., emendation of Methylococcus, validation of Methylosinus and Methylocystis species, and a proposal that the family Methylococcaceae includes only the group I methanotrophs. Int J Syst Bacteriol 43: 735–753.
- Cardellini, C., Chiodinib, G., Frondinia, F., Granierib, D., Lewickic, J., and Peruzzia L. (2003) Accumulation chamber measurements of methane fluxes: application to volcanic-geothermal areas and landfills. Appl Geochem 18: 45–54.
- Castaldi, S., and Tedesco, D. (2005) Methane production and consumption in an active volcanic environment of southern Italy. Chemosphere 58: 131–139.
- Chen, Y., Dumont, M.G., McNamara, N.P., Chamberlain, P.M., Bodrossy, L., Stralis-Pavese, N., and Murrell, J.C. (2008) Diversity of the active methanotrophic community in acidic peatlands as assessed by mRNA and SIP-PLFA analyses. Environ Microbiol 10: 446–459.
- Chistoserdova, L., Chen, S.W., Lapidus, A., and Lidstrom, M.E. (2003) Methylotrophy in Methylobacterium extorquens AM1 from a genomic point of view. J Bacteriol 185: 2980–2987.
- Conrad, R. (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol Rev 60: 609–640.
- Crossman, Z.M., Abraham, F., and Evershed, R.P. (2004) Stable isotope pulse-chasing and compound specific stable carbon isotope analysis of phospholipid fatty acids to assess methane oxidizing bacterial populations in landfill cover soils. Environ Sci Technol 38: 1359–1367.
- Crossman, Z.M., Ineson, P., and Evershed, R.P. (2005) The use of 13C labelling of bacterial lipids in the characterisation of ambient methane-oxidising bacteria in soils. Org Geochem 36: 769–778.
- Dedysh, S.N., Liesack, W., Khmelenina, V.N., Suzina, N.E., Trotsenko, Y.A., Semrau, J.D., et al. (2000) Methylocella palustris gen. nov., sp. nov., a new methane-oxidizing acidophilic bacterium from peat bogs, representing a novel subtype of serine-pathway methanotrophs. Int J Syst Evol Microbiol 50: 955–969.
- Dedysh, S.N., Derakshani, M., and Liesack, W. (2001) Detection and enumeration of methanotrophs in acidic Sphagnum peat by 16S rRNA fluorescence in situ hybridization, including the use of newly developed oligonucleotide probes for Methylocella palustris. Appl Environ Microbiol 67: 4850–4857.
- Dedysh, S.N., Khmelenina, V.N., Suzina, N.E., Trotsenko, Y.A., Semrau, J.D., Liesack, W., and Tiedje, J.M. (2002) Methylocapsa acidiphila gen. nov., sp. nov., a novel methane-oxidizing and dinitrogen-fixing acidophilic bacterium from Sphagnum bog. Int J Syst Evol Microbiol 52: 251–261.
- Dedysh, S.N., Dunfield, P.F., Derakshani, M., Stubner, S., Heyer, J., and Liesack, W. (2003) Differential detection of type II methanotrophic bacteria in acidic peatlands using newly developed 16S rRNA-targeted fluorescent oligonucleotide probes. FEMS Microbiol Ecol 43: 299–308.
- Dedysh, S.N., Berestovskaya, Y.Y., Vasylieva, L.V., Belova, S.E., Khmelenina, V.N., Suzina, N.E., et al. (2004) Methylocella tundrae sp. nov., a novel methanotrophic bacterium from acidic tundra peatlands. Int J Syst Evol Microbiol 54: 151–156.
- Dedysh, S.N., Belova, S.E., Bodelier, P.L.E., Smirnova, K.V., Khmelenina, V.N., Chidthaisong, A., et al. (2007) Methylocystis heyeri sp. nov., a novel type II methanotrophic bacterium possessing the ‘signature’ fatty acid of type I methanotrophs. Int J Syst Evol Microbiol 57: 472–479.
- Dunfield, P.F. (2006) The soil methane sink. In Greenhouse Gas Sinks. D. Reay, C.N. Hewitt, K. Smith, and J. Grace (eds). Wallingford, UK: CABI Publishing, pp. 152–170.
- Dunfield, P.F., Khmelenina, V.N., Suzina, N.E., Trotsenko, Y.A., and Dedysh, S.N. (2003) Methylocella silvestris sp. nov., a novel methanotrophic bacterium isolated from an acidic forest cambisol. Int J Syst Evol Microbiol 53: 1231–1239.
- Dunfield, P.F., Yuryev, A., Senin, P., Smirnova, A.V., Stott, M.B., Hou, S., et al. (2007) Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 450: 879–882.
- Etiope, G., and Klusman, R.W. (2002) Geologic emissions of methane to the atmosphere. Chemosphere 49: 777–789.
- Fiebig, J., Woodland, A.B., Spangenberg, J., and Oschmann, W. (2007) Natural evidence for rapid abiogenic hydrothermal generation of CH4. Geochim Cosmochim Acta 71: 3028–3039.
- Giggenbach, W. (1995) Variations in the chemical and isotopic composition of fluids discharged from the Taupo Volcanic Zone, New Zealand. J Volcanol Geotherm Res 68: 89–116.
- Goris, J., Konstantinidis, K.T., Klappenbach, J.A., Coenye, T., Vandamme, P., and Tiedje, J.M. (2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57: 81–91.
- Guckert, J.B., Antworth, C.P., Nichols, P.D., and White, D.C. (1985) Phospholipid, ester-linked fatty-acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiol Lett 31: 147–158.
- Hakemian, A.S., and Rosenzweig, A.C. (2007) The biochemistry of methane oxidation. Ann Rev Biochem 76: 223–241.
- Hanson, R.S., and Hanson, T.E. (1996) Methanotrophic bacteria. Microbiol Rev 60: 439–471.
- Hernandez, P.A., Perez, N.M., Salazar, J.M., Nakai, S., Notsu, K., and Wakita, H. (1998) Diffuse emission of carbon dioxide, methane and helium-3 from Teide volcano, Tenerife, Canary Island. Geophys Res Lett 25: 3311–3314.
- Heyer, J., Berger, U., Hardt, M., and Dunfield, P.F. (2005) Methylohalobius crimeensis gen. nov., sp. nov., a moderately halophilic, methanotrophic bacterium isolated from hypersaline lakes of Crimea. Int J Syst Evol Microbiol 55: 1817–1826.
- Horita, J., and Berndt M.E. (1999) Abiogenic methane formation and isotopic fractionation under hydrothermal conditions. Science 285: 1055–1057.
- Hou, S., Makarova, K.S., Saw, J.H.W., Senin, P., Ly, B.V., Zhou, Z., et al. (2008) Complete genome sequence of the extremely acidophilic methanotroph isolate V4, ‘Methylacidiphilum infernorum’, a representative of the bacterial phylum Verrucomicrobia. Biol Direct 3: 26.
- Hugenholtz, P., Goebel, B.M., and Pace, N.R. (1998) Impact of culture independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180: 4765–4774.
- Islam, T., Jensen, S., Reigstad, L.J., Larsen, O., and Birkeland, N.K. (2008) Methane oxidation at 55°C and pH 2 by a thermoacidophilic bacterium belonging to the Verrucomicrobia phylum. Proc Natl Acad Sci USA 105: 300–304.
- Janssen, P.H. (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72: 1719–1728.
- Kalyuzhnaya, M., Khmelenina, V., Eshinimaev, B., Suzina, N., Nikitin, D., Solonin, A., et al. (2001) Taxonomic characterization of new alkaliphilic and alkalitolerant methanotrophs from soda lakes of the southeastern Transbaikal region and description of Methylomicrobium buryatense sp. nov. Syst Appl Microbiol 24: 166–176.
- Kalyuzhnaya, M.G., Hristova, K.R., Lidstrom, M.E., and Chistoserdova, L. (2008a) Characterization of a novel methanol dehydrogenase in representatives of Burkholderiales: implications for environmental detection of methylotrophy and evidence for convergent evolution. J Bacteriol 190: 3817–3823.
- Kalyuzhnaya, M.G., Lidstrom, M.E., and Chistoserdova, L. (2008b) Real-time detection of actively metabolizing microbes by redox sensing as applied to methylotroph populations in Lake Washington. ISME J 2: 696–706.
- Kalyuzhnaya, M.G., Lapidus, A., Ivanova, N., Copeland, A.C., McHardy, A.C., Szeto, E., et al. (2008c) High-resolution metagenomics targets specific functional types in complex microbial communities. Nat Biotechnol 26: 1029–1034.
- Klusman, R.W., Moore, J.N., and LeRoy, M.P. (2000) Potential for surface gas flux measurements in exploration and surface evaluation of geothermal resources. Geothermics 29: 637–670.
- Knief, C., Lipski, A., and Dunfield, P.F. (2003) Diversity and activity of methanotrophic bacteria in different upland soils. Appl Environ Microbiol 69: 6703–6714.
- Knief, C., Kolb, S., Bodelier, P.L.E., Lipski, A., and Dunfield P.F. (2006) The active methanotrophic community in hydromorphic soils changes in response to changing methane concentration. Environ Microbiol 8: 321–333.
- Kvenvolden, K.A., and Rogers, B.W. (2005) Gaia's breath – global methane exhalations. Mar Petrol Geol 22: 579–590.
- Lin, J.L., Radajewski, S., Eshinimaev, B.T., Trotsenko, Y.A., McDonald, I.R., and Murrell, J.C. (2004) Molecular diversity of methanotrophs in Transbaikal soda lake sediments and identification of potentially active populations by stable isotope probing. Environ Microbiol 6: 1049–1060.
- Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, B., et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363–1371.
- McDonald, I.R., Bodrossy, L., Chen, Y., and Murrell, J.C. (2008) Molecular ecology techniques for the study of aerobic methanotrophs. Appl Environ Microbiol 74: 1305–1315.
- Morris, S.A., Radajewski, S., Willison, T.W., and Murrell, J.C. (2002) Identification of the functionally active methanotroph population in a peat soil microcosm by stable isotope probing. Appl Environ Microbiol 68: 1446–1453.
- Nold, S.C., Boschker, H.T.S., Pel, R., and Laanbroek, H.J. (1999) Ammonium addition inhibits 13C-methane incorporation into methanotroph membrane lipids in a freshwater sediment. FEMS Microbiol Ecol 29: 81–89.
- Pol, A., Heijmans, K., Harhangi, H.R., Tedesco, D., and Jetten, M.S.M. (2007), Methanotrophy below pH 1 by a new Verrucomicrobia species. Nature 450: 874–878.
- Rahalkar, M., Bussman, I., and Schink, B. (2007) Methylosoma difficile gen. nov., a novel methanotroph enriched by gradient cultivation from littoral sediment of Lake Constance. Int J Sys Evol Microbiol 57: 1073–1080.
- Schmidt, H.A., Strimmer, K., Vingron, M., and von Haeseler, A. (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502–504.
- Segers, R. (1998) Methane production and methane consumption: a review of processes underlying wetland methane fluxes. Biogeochemistry 41: 23–51.
- Snyder, G., Poreda, R., Fehn, U., and Hunt, A. (2003) Sources of nitrogen and methane in Central American geothermal settings: noble gas and 129I evidence for crustal and magmatic volatile components. Geochem Geophys 4: ARTN 9001.
- Stoecker, K., Bendinger, B., Schöning, B., Nielsen, P.H., Nielsen, J.L., Baranyi, C., et al. (2006) Cohn's Crenothrix is a filamentous methane oxidizer with an unusual methane monooxygenase. Proc Natl Acad Sci USA 7: 2363–2367.
- Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599.
- Tchawa Yimga, M., Dunfield, P.F., Ricke, P., Heyer, J., and Liesack, W. (2003) Wide distribution of a novel pmoA-like gene copy among type II methanotrophs, and its expression in Methylocystis strain SC2. Appl Environ Microbiol 69: 5593–5602.
10.1128/AEM.69.9.5593-5602.2003 Google Scholar
- Trotsenko, Y.A., and Khmelenina, V.N. (2002) Biology of extremophilic and extremotolerant methanotrophs. Arch Microbiol 177: 123–131.
- Tsubota, J., Eshinimaev, B.T., Khmelenina, V.N., and Trotsenko, Y.A. (2005) Methylothermus thermalis gen. nov., sp. nov., a novel moderately thermophilic obligate methanotroph from a hot spring in Japan. Int J Syst Evol Microbiol 55: 1877–1884.
- Van Niftrik, L., Geerts, W.J., van Donselaar, E.G., Humbel, B.M., Yakushevska, A., Verkleij, A.J., et al. (2008) Combined structural and chemical analysis of the anammoxosome: a membrane-bounded intracytoplasmic compartment in anammox bacteria. J Struct Biol 161: 401–410.
- Wagner, M., and Horn, M. (2006) The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr Opin Biotechnol 17: 241–249.
- Wise, M.G., McArthur, J.V., and Shimkets, L.J. (2001) Methylosarcina fibrata gen. nov., sp. nov. and Methylosarcina quisquiliarum sp. nov., novel type I methanotrophs. Int J Syst Evol Microbiol 51: 611–621.
- Yang, Z. (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591.
- Yang, Z., and Nielsen, R. (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17: 2–43.
- Yoon, J., Yasumoto-Hirose, M., Katsuta, A., Sekiguchi, H., Matsuda, S., Kasai, H., and Yokota, A. (2007) Coraliomargarita akajimensis gen. nov., sp. nov., a novel member of the phylum ‘Verrucomicrobia’ isolated from seawater in Japan. Int J Syst Evol Microbiol 57: 959–963.
- Yoon, J., Matsuo, Y., Adachi, K., Nozawa, M., Matsuda, S., Kasai, H., and Yokota, A. (2008) Description of Persicirhabdus sediminis gen. nov., sp. nov., Roseibacillus ishigakijimensis gen. nov., sp. nov., Roseibacillus ponti sp. nov., Roseibacillus persicicus sp. nov., Luteolibacter pohnpeiensis gen. nov., sp. nov. and Luteolibacter algae sp. nov., six marine members of the phylum ‘Verrucomicrobia’, and emended descriptions of the class Verrucomicrobiae, the order Verrucomicrobiales and the family Verrucomicrobiaceae. Int J Syst Evol Microbiol 58: 998–1007.
