Detection of autotrophic verrucomicrobial methanotrophs in a geothermal environment using stable isotope probing

Frontiers in Microbiology

Volumn 3, Issue AUG, 2012, Pages

  Sharp, Christine E ^a   Stott, Matthew B ^b   Dunfield, Peter F ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b GNS SCIENCE   (New Zealand)

Author keywords

"Methylacidiphilum"; Acidophile; Methane; Methanotroph; Stable isotope probing; Verrucomicrobia

Indexed keywords

EID: 84875776294     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00303     Document Type: Article

References (43)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
2. Barbier, B. A., Dziduch, I., Liebner, S., Ganzert, L., Lantuit, H., Pollard, W., and Wagner, D. (2012). Methane-cycling communities in a permafrost-affected soil on Herschel Island, Western Canadian Arctic: active layer profiling of mcrA and pmoA genes. FEMS Microbiol. Ecol. doi: 10.1111/j.1574-6941.2012. 01332.x. [Epub ahead of print].
3. Benson, C. A., Bizzoco, R. W., Lipson, D. A., and Kelley, S. T. (2011). Microbial diversity in nonsulfur, sulfur and iron geothermal steam vents. FEMS Microbiol. Ecol. 76, 74-88.
4. Bodrossy, L., Kovács, K. L., McDonald, I. R., and Murrell, J. C. (1999). A novel thermophilic methane-oxidising γ-Proteobacterium. FEMS Microbiol. Lett. 170, 335-341.
5. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Pena, A. G., Goodrich, J. K., Gordon, J. I., Huttley, G. A., Kelley, S. T., Knights, D., Koenig, J. E., Ley, R. E., Lozupone, C. A., McDonald, D., Muegge, B. D., Pirrung, M., Reeder, J., Sevinsky, J. R., Turnbaugh, P. J., Walters, W A., Widmann, J., Yatsunenko, T., Zaneveld, J., and Knight, R. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336.
6. Cebron, A., Bodrossy, L., Chen, Y., Singer, A. C., Thompson, I. P., Prosser, J. I., and Murrell, J. C. (2007a). Identity of active methan-otrophs in landfill cover soil as revealed by DNA-stable isotope probing. FEMS Microbiol. Ecol. 62, 12-23.
7. Cebron, A., Bodrossy, L., Stralis-Pavese, N., Singer, A. C., Thompson, I. P., Prosser, J. I., and Murrell, J. C. (2007b). Nutrient amendments in soil DNA stable isotope probing experiments reduce the observed methanotroph diversity. Appl. Environ. Microbiol. 73, 798-807.
8. Costello, E. K., Halloy, S. R., Reed, S. C., Sowell, P., and Schmidt, S. K. (2009). Fumarole-supported islands of biodiversity within a hyperarid, high-elevation landscape on Socompa Volcano, Puna de Atacama, Andes. Appl. Environ. Microbiol. 75, 735-747.
9. Desantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., Huber, T., Dalevi, D., Hu, P., and Andersen, G. L. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069-5072.
10. Dumont, M. G., Pommerenke, B., Casper, P., and Conrad, R. (2011). DNA-, rRNA-, and mRNA-based stable isotope probing of aerobic methanotrophs in lake sediment. Environ. Microbiol. 13, 1153-1167.
11. Dunfield, P. E (2009). "Methanotrophy in Extreme Environments," in Encyclopedia of Life Sciences (ELS). Chichester: John Wiley and Sons, Ltd. Avalibale online at: http://www.els.net. doi: 10.1002/9780470015902.a0021897
12. Dunfield, P. F., Yuryev, A., Senin, P., Smirnova, A. V., Stott, M. B., Hou, S., Ly, B., Saw, J. H., Zhou, Z., Ren, Y., Wang, J., Mountain, B. W., Crowe, M. A., Weatherby, T. M., Bodelier, P. L., Liesack, W., Feng, L., Wang, L., and Alam, M. (2007). Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 450, 879-882.
13. Ettwig, K. F., Van Alen, T., Van De Pas-Schoonen, K. T., Jetten, M. S. M., and Strous, M. (2009). Enrichment and molecular detection of denitrifying methanotrophic bacteria of the NC10 phylum. Appl. Environ. Microbiol. 75, 3656-3662.
14. Giggenbach, W O. (1994). Variations in the chemical and isotopic composition of fluids discharged from the Taupo Volcanic Zone, New Zealand. J. Volcanol. Geotherm. Res. 68,89-116.
15. Gilles, A., Meglecz, E., Pech, N., Ferreira, S., Malausa, T., and Martin, J.-F. (2011). Accuracy and quality assessment of 454 GS-FLX Titanium pyrosequencing. BMC Genomics 12, 245.
16. Graef, C., Hestnes, A. G., Svenning, M. M., and Frenzel, P. (2011). The active methanotrophic community in a wetland from the High Arctic. Environ. Microbiol. Rep. 3, 466-472.
17. Haas, B. J., Gevers, D., Earl, A. M., Feldgarden, M., Ward, D. V., Giannoukos, G., Ciulla, D., Tabbaa, D., Highlander, S. K., Sodergren, E., Methe, B., Desantis, T. Z., Petrosino, J. F., Knight, R., and Birren, B. W. (2011). Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21,494-504.
18. Hallam, S. J., Mincer, T. J., Schleper, C., Preston, C. M., Roberts, K., Richardson, P. M., and Delong, E. F. (2006). Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol. 4:e95. doi: 10.1371/ journal.pbio.0040095
19. Hanson, R. S., and Hanson, T. E. (1996). Methanotrophic bacteria. Microbiol. Rev. 60, 439-471.
20. Hou, S., Makarova, K. S., Saw, J. H., Senin, P., Ly, B. V., Zhou, Z., Ren, Y., Wang, J., Galperin, M. Y., Omelchenko, M. V., Wolf, Y I., Yutin, N., Koonin, E. V., Stott, M. B., Mountain, B. W., Crowe, M. A., Smirnova, A. V., Dunfield, P. F., Feng, L., Wang, L., and Alam, M. (2008). Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biol. Direct 3,26.
21. Hutchens, E., Radajewski, S., Dumont, M. G., McDonald, I. R., and Murrell, J. C. (2004). Analysis of methanotrophic bacteria in Movile Cave by stable isotope probing. Environ. Microbiol. 6, 111-120.
22. Islam, T., Jensen, S., Reigstad, L. J., Larsen, O., and Birkeland, N. K. (2008). Methane oxidation at 55 degrees C and pH 2 by a ther-moacidophilic bacterium belonging to the Verrucomicrobia phylum. Proc. Natl. Acad. Sci. U.S.A. 105, 300-304.
23. Khadem, A. F., Pol, A., Wieczorek, A., Mohammadi, S. S., Francoijs, K. J., Stunnenberg, H. G., Jetten, M. S. M., and Op den Camp, H. J. M. (2011). Autotrophic methanotrophy in Verrucomicrobia: Methylacidiphilum fumariolicum SolV uses the Calvin-Benson-Bassham Cycle for carbon dioxide fixation. J. Bacteriol. 193, 4438-4446.
24. Kip, N., Van Winden, J. F., Pan, Y., Bodrossy, L., Reichart, G.-J., Smolders, A. J. P., Jetten, M. S. M., Sinninghe Damste, J. S., and Op den Camp, H. J. M. (2010). Global prevalence of methane oxidation by symbiotic bacteria in peat-moss ecosystems. Nat. Geosci. 3, 617-621.
25. Knief, C., Lipski, A., and Dunfield, P. E (2003). Diversity and activity of methanotrophic bacteria in different upland soils. Appl. Environ. Microbiol. 69, 6703-6714.
26. Knittel, K., and Boetius, A. (2009). Anaerobic oxidation of methane: progress with an unknown process. Annu. Rev. Microbiol. 63, 311-334.
27. Kolb, S., Knief, C., Stubner, S., and Conrad, R. (2003). Quantitative detection of methanotrophs in soil by novel pmoA-targeted realtime PCR assays. Appl. Environ. Microbiol. 69, 2423-2429.
28. Kravchenko, I. K. (2002). Methane oxidation in boreal peat soils treated with various nitrogen compounds. Plant Soil242, 157-162.
29. Lee, S.-Y., Lee, S. H., Jang, J. K., and Cho, K.-S. (2011). Comparison of methanotrophic community and methane oxidation between rhizo-spheric and non-rhizospheric soils. Geomicrobiol. J. 28, 676-685.
30. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, Buchner, A., Lai, T., Steppi, S., Jobb, G., Forster, W., Brettske, I., Gerber, S., Ginhart, A. W., Gross, O., Grumann, S., Hermann, S., Jost, R., Konig, A., Liss, T., Lussmann, R., May, M., Nonhoff, B., Reichel, B., Strehlow, R., Stamatakis, A., Stuckmann, N., Vilbig, A., Lenke, M., Ludwig, T., Bode, A., and Schleifer, K. H. (2004). ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363-1371.
31. Marakushev, S., and Belonogova, O. (2010). Evolution of carbon dioxide archaic chemoautotrophic fixation system in hydrothermal systems. Dokl. Biochem. Biophys. 433, 168-174.
32. Martineau, C., Whyte, L. G., and Greer, C. W (2010). Stable isotope probing analysis of the diversity and activity of methanotrophic bacteria in soils from the Canadian high Arctic. Appl. Environ. Microbiol. 76, 5773-5784.
33. 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.
34. Neufeld, J. D., Schäfer, H., Cox, M. J., Boden, R., McDonald, I. R., and Murrell, J. C. (2007a). Stable-isotope probing implicates Methylophaga spp and novel Gammaproteobacteria in marine methanol and methylamine metabolism. ISMEJ. 1,480-491.
35. Neufeld, J. D., Vohra, J., Dumont, M. G., Lueders, T., Manefield, M., Friedrich, M. W., and Murrell, J. C. (2007b). DNA stable-isotope probing. Nat. Protoc. 2, 860-866.
36. Nicol, G. W., and Schleper, C. (2006). Ammonia-oxidising Crenarchaeota: important players in the nitrogen cycle? Trends Microbiol. 14, 207-212.
37. Op den Camp, H. J. M., Islam, T., Stott, M. B., Harhangi, H. R., Hynes, A., Schouten, S., Jetten, M. S. M., Birkeland, N. K., Pol, A., and Dunfield, P. F. (2009). Environmental, genomic and tax-anomic perspectives on methan-otrophic Verrucomicrobia. Environ. Microbiol. Rep. 1, 293-306.
38. Pol, A., Heijmans, K., Harhangi, H. R., Tedesco, D., Jetten, M. S. M., and Op den Camp, H. J. M. (2007). Methanotrophy below pH 1 by a new Verrucomicrobia species. Nature 450, 874-878.
39. Ramos-Padron, E., Bordenave, S., Lin, S., Bhaskar, I. M., Dong, X., Sensen, C. W., Fournier, J., Voordouw, G., and Gieg, L. M. (2011). Carbon and sulfur cycling by microbial communities in a gypsum-treated oil sands tailings pond. Environ. Sci. Technol. 45, 439-446.
40. Redmond, M. C., Valentine, D. L., and Sessions, A. L. (2010). Identification of novel methane-, ethane-, and propane-oxidizing bacteria at marine hydrocarbon seeps by stable isotope probing. Appl. Environ. Microbiol. 76, 6412-6422.
41. 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.
42. Stott, M. B., Crowe, M. A., Mountain, B. W., Smirnova, A. V., Hou, S., Alam, M., and Dunfield, P. F. (2008). Isolation of novel bacteria, including a candidate division, from geothermal soils in New Zealand. Environ. Microbiol. 10, 2030-2041.
43. Wagner, D., Lipski, A., Embacher, A., and Gattinger, A. (2005). Methane fluxes in permafrost habitats of the Lena Delta: effects of microbial community structure and organic matter quality. Environ. Microbiol. 7, 1582-1592.