1887

Abstract

Two aerobic methane-oxidizing bacterial strains were isolated from distinct marine environments in Japan. Strains IT-4 and T2-1 were Gram-stain-negative, aerobic, motile, plump short rods or oval-shaped bacteria with a single polar flagellum and type I intracytoplasmic membranes. They were obligate methanotrophs that grew only on methane or methanol. Each strain possessed the particulate methane monooxygenase (pMMO). The ribulose monophosphate pathway was operative for carbon assimilation. The strains grew best at 37 °C, and did not grow at 45 °C. NaCl was required for growth within a concentration range of 1–8 % (w/v). The major phospholipid fatty acids were C, Cω7, and Cω5. The major isoprenoid quinone was MQ-8. The DNA G+C content was 50.9–51.7 mol%. The 16S rRNA gene sequences of the strains showed 99.4 % similarity to each other, and DNA–DNA hybridization analysis indicated that the strains were representatives of the same species. The 16S rRNA gene sequences were highly similar to some marine environmental sequences (94.0–97.7 % similarity), but did not show similarities more than 94 % with sequences of members of other related genera, such as , , and . Phylogenies based on 16S rRNA gene sequences and deduced partial PmoA sequences, and the physiological and chemotaxonomic characteristics revealed that strains IT-4 and T2-1 represent a novel species of a new genus in the family , for which the name gen. nov., sp. nov. is proposed. The type strain is IT-4 ( = JCM 13665 = DSM 18976).

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2013-03-01
2021-10-22
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References

  1. Alfreider A., Vogt C., Hoffmann D., Babel W. ( 2003 ). Diversity of ribulose-1,5-bisphosphate carboxylase/oxygenase large-subunit genes from groundwater and aquifer microorganisms. . Microb Ecol 45, 317328. [View Article] [PubMed]
    [Google Scholar]
  2. Balch W. E., Fox G. E., Magrum L. J., Woese C. R., Wolfe R. S. ( 1979 ). Methanogens: reevaluation of a unique biological group. . Microbiol Rev 43, 260296.[PubMed]
    [Google Scholar]
  3. Beal E. J., House C. H., Orphan V. J. ( 2009 ). Manganese- and iron-dependent marine methane oxidation. . Science 325, 184187. [View Article] [PubMed]
    [Google Scholar]
  4. Boden R., Cunliffe M., Scanlan J., Moussard H., Kits K. D., Klotz M. G., Jetten M. S. M., Vuilleumier S., Han J. & other authors ( 2011 ). Complete genome sequence of the aerobic marine methanotroph Methylomonas methanica MC09. . J Bacteriol 193, 70017002. [View Article] [PubMed]
    [Google Scholar]
  5. Bodrossy L., Holmes E. M., Holmes A. J., Kovács K. L., Murrell J. C. ( 1997 ). Analysis of 16S rRNA and methane monooxygenase gene sequences reveals a novel group of thermotolerant and thermophilic methanotrophs, Methylocaldum gen. nov.. Arch Microbiol 168, 493503. [View Article] [PubMed]
    [Google Scholar]
  6. Bowman J. P., Sly L. I., Nichols P. D., 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, 735753. [View Article]
    [Google Scholar]
  7. Bowman J. P., Sly L. I., Stackebrandt E. ( 1995 ). The phylogenetic position of the family Methylococcaceae . . Int J Syst Bacteriol 45, 182185. [View Article] [PubMed]
    [Google Scholar]
  8. Bowman J. P., McCammon S. A., Skerrat J. H. ( 1997 ). Methylosphaera hansonii gen. nov., sp. nov., a psychrophilic, group I methanotroph from Antarctic marine-salinity, meromictic lakes. . Microbiology 143, 14511459. [View Article] [PubMed]
    [Google Scholar]
  9. Christie W. W. ( 1997 ). Structural analysis of fatty acids. . In Advances in Lipid Methodology – Four, pp. 119169. Edited by Christie W. W. . Dundee:: Oily Press;.
    [Google Scholar]
  10. Collins M. D., Green P. N. ( 1985 ). Isolation and characterization of a novel coenzyme Q from some methane-oxidizing bacteria. . Biochem Biophys Res Commun 133, 11251131. [View Article] [PubMed]
    [Google Scholar]
  11. Csáki R., Bodrossy L., Klem J., Murrell J. C., Kovács K. L. ( 2003 ). Genes involved in the copper-dependent regulation of soluble methane monooxygenase of Methylococcus capsulatus (Bath): cloning, sequencing and mutational analysis. . Microbiology 149, 17851795. [View Article] [PubMed]
    [Google Scholar]
  12. Damm E., Helmke E., Thoms S., Schauer U., Nöthig E., Bakker K., Kiene R. P. ( 2010 ). Methane production in aerobic oligotrophic surface water in the central Arctic Ocean. . Biogeosciences 7, 10991108. [View Article]
    [Google Scholar]
  13. Elsaied H., Naganuma T. ( 2001 ). Phylogenetic diversity of ribulose-1,5-bisphosphate carboxylase/oxygenase large-subunit genes from deep-sea microorganisms. . Appl Environ Microbiol 67, 17511765. [View Article] [PubMed]
    [Google Scholar]
  14. Eshinimaev B. Ts., Medvedkova K. A., Khmelenina V. N., Suzina N. E., Osipov G. A., Lysenko A. M., Trotsenko IuA. ( 2004 ). [New thermophilic methanotrophs of the genus Methylocaldum]. . Mikrobiologiia 73, 530539.[PubMed]
    [Google Scholar]
  15. Ezaki T., Hashimoto Y., Yabuuchi E. ( 1989 ). Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. . Int J Syst Bacteriol 39, 224229. [View Article]
    [Google Scholar]
  16. Fang J., Barcelona M. J., Semrau J. D. ( 2000 ). Characterization of methanotrophic bacteria on the basis of intact phospholipid profiles. . FEMS Microbiol Lett 189, 6772. [View Article] [PubMed]
    [Google Scholar]
  17. Fuse H., Ohta M., Takimura O., Murakami K., Inoue H., Yamaoka Y., Oclarit J. M., Omori T. ( 1998 ). Oxidation of trichloroethylene and dimethyl sulfide by a marine Methylomicrobium strain containing soluble methane monooxygenase. . Biosci Biotechnol Biochem 62, 19251931. [View Article] [PubMed]
    [Google Scholar]
  18. Gascuel O. ( 1997 ). BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. . Mol Biol Evol 14, 685695. [View Article] [PubMed]
    [Google Scholar]
  19. Gouy M., Guindon S., Gascuel O. ( 2010 ). SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. . Mol Biol Evol 27, 221224. [View Article] [PubMed]
    [Google Scholar]
  20. Guindon S., Gascuel O. ( 2003 ). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. . Syst Biol 52, 696704. [View Article] [PubMed]
    [Google Scholar]
  21. Heyer J., Berger U., Hardt M., 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, 18171826. [View Article] [PubMed]
    [Google Scholar]
  22. Hirayama H., Takai K., Inagaki F., Nealson K. H., Horikoshi K. ( 2005 ). Thiobacter subterraneus gen. nov., sp. nov., an obligately chemolithoautotrophic, thermophilic, sulfur-oxidizing bacterium from a subsurface hot aquifer. . Int J Syst Evol Microbiol 55, 467472. [View Article] [PubMed]
    [Google Scholar]
  23. Hirayama H., Sunamura M., Takai K., Nunoura T., Noguchi T., Oida H., Furushima Y., Yamamoto H., Oomori T., Horikoshi K. ( 2007 ). Culture-dependent and -independent characterization of microbial communities associated with a shallow submarine hydrothermal system occurring within a coral reef off Taketomi Island, Japan. . Appl Environ Microbiol 73, 76427656. [View Article] [PubMed]
    [Google Scholar]
  24. Hirayama H., Suzuki Y., Abe M., Miyazaki M., Makita H., Inagaki F., Uematsu K., Takai K. ( 2011 ). Methylothermus subterraneus sp. nov., a moderately thermophilic methanotroph isolated from a terrestrial subsurface hot aquifer. . Int J Syst Evol Microbiol 61, 26462653. [View Article] [PubMed]
    [Google Scholar]
  25. Holmes A. J., Owens N. J. P., Murrell J. C. ( 1995 ). Detection of novel marine methanotrophs using phylogenetic and functional gene probes after methane enrichment. . Microbiology 141, 19471955. [View Article] [PubMed]
    [Google Scholar]
  26. Iguchi H., Yurimoto H., Sakai Y. ( 2011 ). Methylovulum miyakonense gen. nov., sp. nov., a type I methanotroph isolated from forest soil. . Int J Syst Evol Microbiol 61, 810815. [View Article] [PubMed]
    [Google Scholar]
  27. Kalyuzhnaya M. G., Khmelenina V. N., Kotelnikova S., Holmquist L., Pedersen K., Trotsenko Y. A. ( 1999 ). Methylomonas scandinavica sp. nov., a new methanotrophic psychrotrophic bacterium isolated from deep igneous rock ground water of Sweden. . Syst Appl Microbiol 22, 565572. [View Article] [PubMed]
    [Google Scholar]
  28. Kalyuzhnaya M. G., Khmelenina V., Eshinimaev B., Sorokin D., Fuse H., Lidstrom M., Trotsenko Y. ( 2008 ). Classification of halo(alkali)philic and halo(alkali)tolerant methanotrophs provisionally assigned to the genera Methylomicrobium and Methylobacter and emended description of the genus Methylomicrobium . . Int J Syst Evol Microbiol 58, 591596. [View Article] [PubMed]
    [Google Scholar]
  29. Karl D. M., Beversdorf L., Bjorkman K. M., Church M. J., Martinez A., Delong E. F. ( 2008 ). Aerobic production of methane in the sea. . Nat Geosci 1, 473478. [View Article]
    [Google Scholar]
  30. Koh S.-C., Bowman J. P., Sayler G. S. ( 1993 ). Soluble methane monooxygenase production and trichloroethylene degradation by a type I methanotroph, Methylomonas methanica 68–1. . Appl Environ Microbiol 59, 960967.[PubMed]
    [Google Scholar]
  31. Komagata K., Suzuki K. ( 1987 ). Lipid and cell-wall analysis in bacterial systematics. . Methods Microbiol 19, 161207. [View Article]
    [Google Scholar]
  32. Large P. J., Quayle J. R. ( 1963 ). Microbial growth on C1 compounds. 5. Enzyme activities in extracts of Pseudomonas AM1. . Biochem J 87, 386396.[PubMed]
    [Google Scholar]
  33. Lees V., Owens N. J. P., Murrell J. C. ( 1991 ). Nitrogen metabolism in marine methanotrophs. . Arch Microbiol 157, 6065. [View Article]
    [Google Scholar]
  34. Lidstrom M. E. ( 1988 ). Isolation and characterization of marine methanotrophs. . Antonie van Leeuwenhoek 54, 189199. [View Article] [PubMed]
    [Google Scholar]
  35. Ludwig W., Strunk O., Westram R., Richter L., Meier H., Yadhukumar, Buchner A., Lai T., Steppi S. & other authors ( 2004 ). ARB: a software environment for sequence data. . Nucleic Acids Res 32, 13631371. [View Article] [PubMed]
    [Google Scholar]
  36. Maeda N., Kanai T., Atomi H., Imanaka T. ( 2002 ). The unique pentagonal structure of an archaeal Rubisco is essential for its high thermostability. . J Biol Chem 277, 3165631662. [View Article] [PubMed]
    [Google Scholar]
  37. McDonald I. R., Kenna E. M., Murrell J. C. ( 1995 ). Detection of methanotrophic bacteria in environmental samples with the PCR. . Appl Environ Microbiol 61, 116121.[PubMed]
    [Google Scholar]
  38. Mehta M. P., Butterfield D. A., Baross J. A. ( 2003 ). Phylogenetic diversity of nitrogenase (nifH) genes in deep-sea and hydrothermal vent environments of the Juan de Fuca Ridge. . Appl Environ Microbiol 69, 960970. [View Article] [PubMed]
    [Google Scholar]
  39. Miguez C. B., Bourque D., Sealy J. A., Greer C. W., Groleau D. ( 1997 ). Detection and isolation of methanotrophic bacteria possessing soluble methane monooxygenase (sMMO) genes using the polymerase chain reaction (PCR). . Microb Ecol 33, 2131. [View Article] [PubMed]
    [Google Scholar]
  40. Minnikin D. E., O'Donnell A. G., Goodfellow M., Alderson G., Athalye M., Schaal A., Parlett J. H. ( 1984 ). An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. . J Microbiol Methods 2, 233241. [View Article]
    [Google Scholar]
  41. Nakamura T., Hoaki T., Hanada S., Maruyama A., Kamagata Y., Fuse H. ( 2007 ). Soluble and particulate methane monooxygenase gene clusters in the marine methanotroph Methylomicrobium sp. strain NI. . FEMS Microbiol Lett 277, 157164. [View Article] [PubMed]
    [Google Scholar]
  42. Nanba K., Takeda K., Higashihara T., Ohwada K. ( 1999 ). Distribution of methanotrophic bacteria in the coastal marine sediments. . Fish Sci 65, 531536.
    [Google Scholar]
  43. Nanba K., King G. M., Dunfield K. ( 2004 ). Analysis of facultative lithotroph distribution and diversity on volcanic deposits by use of the large subunit of ribulose 1,5-bisphosphate carboxylase/oxygenase. . Appl Environ Microbiol 70, 22452253. [View Article] [PubMed]
    [Google Scholar]
  44. Sieburth J. N., Johnson P. W., Eberhardt M. A., Sieracki M. E., Lidstrom M., Laux D. ( 1987 ). The first methane-oxidizing bacterium from the upper mixing layer of the deep ocean: Methylomonas pelagica sp. nov.. Curr Microbiol 14, 285293. [View Article]
    [Google Scholar]
  45. Sieburth J. M., Johnson P. W., Church V. M., Laux D. C. ( 1993 ). C1 bacteria in the water column of Chesapeake Bay, USA. III. Immunologic relationships of the type species of marine monomethylamine- and methane-oxidizing bacteria to wild estuarine and oceanic cultures. . Mar Ecol Prog Ser 95, 91102. [View Article]
    [Google Scholar]
  46. Smith K. S., Costello A. M., Lidstrom M. E. ( 1997 ). Methane and trichloroethylene oxidation by an estuarine methanotroph, Methylobacter sp. strain BB5.1. . Appl Environ Microbiol 63, 46174620.[PubMed]
    [Google Scholar]
  47. Spiekermann P., Rehm B. H. A., Kalscheuer R., Baumeister D., Steinbüchel A. ( 1999 ). A sensitive, viable-colony staining method using Nile red for direct screening of bacteria that accumulate polyhydroxyalkanoic acids and other lipid storage compounds. . Arch Microbiol 171, 7380. [View Article] [PubMed]
    [Google Scholar]
  48. Tamaoka J., Komagata K. ( 1984 ). Determination of DNA base composition by reversed-phase high-performance liquid chromatography. . FEMS Microbiol Lett 25, 125128. [View Article]
    [Google Scholar]
  49. Tsubota J., Eshinimaev B. Ts., Khmelenina V. N., 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, 18771884. [View Article] [PubMed]
    [Google Scholar]
  50. Wartiainen I., Hestnes A. G., McDonald I. R., Svenning M. M. ( 2006 ). Methylobacter tundripaludum sp. nov., a methane-oxidizing bacterium from Arctic wetland soil on the Svalbard islands, Norway (78° N). . Int J Syst Evol Microbiol 56, 109113. [View Article] [PubMed]
    [Google Scholar]
  51. Whittenbury R., Phillips K. C., Wilkinson J. F. ( 1970 ). Enrichment, isolation and some properties of methane-utilizing bacteria. . J Gen Microbiol 61, 205218. [View Article] [PubMed]
    [Google Scholar]
  52. Zehr J. P., McReynolds L. A. ( 1989 ). Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii . . Appl Environ Microbiol 55, 25222526.[PubMed]
    [Google Scholar]
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