1887

Abstract

A Gram-stain-negative, aerobic, non-motile and coccoid methanotroph, strain IM1, was isolated from hot spring soil. Cells of strain IM1 were catalase-negative, oxidase-positive and displayed a characteristic intracytoplasmic membrane arrangement of type I methanotrophs. The strain possessed genes encoding both membrane-bound and soluble methane monooxygenases and grew only on methane or methanol. The strain was capable of growth at temperatures between 15 and 48 °C (optimum, 30–45 °C) and pH values between pH 4.8 and 8.2 (optimum, pH 6.2–7.0). Based on phylogenetic analysis of 16S rRNA gene and PmoA sequences, strain IM1 was demonstrated to be affiliated to the genus . The 16S rRNA gene sequence of this strain was most closely related to the sequences of an uncultured bacterium clone FD09 (100 %) and a partially described cultured sp. GDS2.4 (99.78 %). The most closely related taxonomically described strains were Texas (97.92 %), Bath (97.86 %) and 73a (94.21 %). Strain IM1 shared average nucleotide identity values of 85.93 and 85.62 % with strains Texas and Bath, respectively. The digital DNA–DNA hybridization value with the closest type strain was 29.90 %. The DNA G+C content of strain IM1 was 63.3 mol% and the major cellular fatty acids were C (39.0 %), C 7 (24.0 %), C 6 (13.6 %) and C 5 (12.0 %). The major ubiquinone was methylene-ubiquinone-8. On the basis of phenotypic, genetic and phylogenetic data, strain IM1 represents a novel species of the genus for which the name sp. nov. is proposed, with strain IM1 (=JCM 33941=KCTC 72677) as the type strain.

Funding
This study was supported by the:
  • Not Applicable , Ministry of Oceans and Fisheries, Korea , (Award 20170411)
  • Sung-Keun Rhee , National Institute of Biological Resources , (Award NIBR201902111)
  • Sung-Keun Rhee , National Research Foundation , (Award 2015M3D3A1A01064881)
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004442
2020-09-10
2020-11-30
Loading full text...

Full text loading...

References

  1. Bowman JP. Methylococcus. In Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J et al. (editors) Bergey's Manual of Systematics of Archaea and Bacteria John Wiley & Sons, Inc; 2015 pp 1–10
    [Google Scholar]
  2. Bowman JP, Sly LI, Nichols PD, Hayward AC. 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 Evol Microbiol 1993; 43:735–753
    [Google Scholar]
  3. Foster JW, Davis RH. A methane-dependent coccus, with notes on classification and nomenclature of obligate, methane-utilizing bacteria. J Bacteriol 1966; 91:1924–1931 [CrossRef][PubMed]
    [Google Scholar]
  4. Malashenko IR, Romanovskaia VA, Bogachenko VN, Shved AD. Thermophilic and thermotolerant bacteria that assimilate methane. Mikrobiologiia 1975; 44:855–862[PubMed]
    [Google Scholar]
  5. Romanovskaya V, Malashenko YR, Bogachenko V. Corrected diagnosis of genera and species of methane-utilizing bacteria. Microbiology 1978; 47:96–103
    [Google Scholar]
  6. Hazeu W, Batenburg-van der Vegte WH, de Bruyn JC. Some characteristics of Methylococcus mobilis sp. nov. Archives of Microbiology 1980; 124:211–220
    [Google Scholar]
  7. Skerman VBD, McGowan V, Sneath PHA. Approved Lists of bacterial names. Int J Syst Evol Microbiol 1980; 30:225–420
    [Google Scholar]
  8. Whittenbury R, Phillips KC, Wilkinson JF. Enrichment, isolation and some properties of methane-utilizing bacteria. J Gen Microbiol 1970; 61:205–218 [CrossRef][PubMed]
    [Google Scholar]
  9. Yarza P, Spröer C, Swiderski J, Mrotzek N, Spring S et al. Sequencing orphan species initiative (SOS): filling the gaps in the 16S rRNA gene sequence database for all species with validly published names. Syst Appl Microbiol 2013; 36:69–73 [CrossRef][PubMed]
    [Google Scholar]
  10. Bodrossy L, Holmes EM, Holmes AJ, Kovács KL, Murrell JC. Analysis of 16S rRNA and methane monooxygenase gene sequences reveals a novel group of thermotolerant and thermophilic methanotrophs, Methylocaldum gen. nov. Arch Microbiol 1997; 168:493–503 [CrossRef][PubMed]
    [Google Scholar]
  11. Zillig W, Stetter KO, Wunderl S, Schulz W, Priess H et al. Validation of the publication of new names and new combinations previously effectively published outside the IJSB. Int J Syst Evol Microbiol 1980; 30:676–677
    [Google Scholar]
  12. Wise MG, McArthur JV, Shimkets LJ. Methylosarcina fibrata gen. nov., sp. nov. and Methylosarcina quisquiliarum sp.nov., novel type 1 methanotrophs. Int J Syst Evol Microbiol 2001; 51:611–621 [CrossRef][PubMed]
    [Google Scholar]
  13. Bowman JP. The Family Methylococcaceae . In Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F. (editors) The Prokaryotes: Gammaproteobacteria Berlin, Heidelberg: Springer Berlin Heidelberg; 2014 pp 411–440
    [Google Scholar]
  14. Lin L-H, Hall J, Onstott TC, Gihring T, Lollar BS et al. Planktonic microbial communities associated with fracture-derived groundwater in a deep gold mine of South Africa. Geomicrobiol J 2006; 23:475–497 [CrossRef]
    [Google Scholar]
  15. Borgonie G, Linage-Alvarez B, Ojo AO, Mundle SOC, Freese LB et al. Eukaryotic opportunists dominate the deep-subsurface biosphere in South Africa. Nat Commun 2015; 6:8952 [CrossRef][PubMed]
    [Google Scholar]
  16. Rattanachomsri U, Kanokratana P, Eurwilaichitr L, Igarashi Y, Champreda V. Culture-Independent phylogenetic analysis of the microbial community in industrial sugarcane bagasse feedstock piles. Biosci Biotechnol Biochem 2011; 75:232–239 [CrossRef][PubMed]
    [Google Scholar]
  17. Kato S, Kikuchi S, Kashiwabara T, Takahashi Y, Suzuki K et al. Prokaryotic abundance and community composition in a freshwater iron-rich microbial mat at circumneutral pH. Geomicrobiol J 2012; 29:896–905 [CrossRef]
    [Google Scholar]
  18. Takashima C, Kano A, Naganuma T, Tazaki K. Laminated iron texture by iron-oxidizing bacteria in a calcite travertine. Geomicrobiol J 2008; 25:193–202 [CrossRef]
    [Google Scholar]
  19. Park SS, Yun ST, Chae GT, Hutcheon I, Koh YK et al. Temperature evaluation of the Bugok geothermal system, South Korea. Geothermics 2006; 35:448–469
    [Google Scholar]
  20. Koh YK, Yun ST, Kim CS, Bae DS, Park SS. Geochemical evolution and deep environment of the geothermal waters in the Bugok area: reconsideration on the origin of sulfate-type geothermal water. Economic and Environmental Geology 2001; 34:329–343
    [Google Scholar]
  21. Widdel F, Bak F, Schleifer K-H. Gram-negative mesophilic sulfate-reducing bacteria. In Balows A, Trüper HG, Dworkin M, Harder W. (editors) The Prokaryotes: A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications New York, NY: Springer New York; 1992 pp 3352–3378
    [Google Scholar]
  22. Nguyen N-L, Yu W-J, Gwak J-H, Kim S-J, Park S-J et al. Genomic insights into the acid adaptation of novel methanotrophs enriched from acidic forest soils. Front Microbiol 2018; 9:9 [CrossRef][PubMed]
    [Google Scholar]
  23. Hirayama H, Suzuki Y, Abe M, Miyazaki M, Makita H et al. Methylothermus subterraneus sp. nov., a moderately thermophilic methanotroph isolated from a terrestrial subsurface hot aquifer. Int J Syst Evol Microbiol 2011; 61:2646–2653 [CrossRef][PubMed]
    [Google Scholar]
  24. de Bruyn JC, Boogerd FC, Bos P, Kuenen JG. Floating filters, a novel technique for isolation and enumeration of fastidious, acidophilic, iron-oxidizing, autotrophic bacteria. Appl Environ Microbiol 1990; 56:2891–2894 [CrossRef][PubMed]
    [Google Scholar]
  25. Nguyen N-L, Yu W-J, Yang H-Y, Kim J-G, Jung M-Y et al. A novel methanotroph in the genus Methylomonas that contains a distinct clade of soluble methane monooxygenase. J Microbiol 2017; 55:775–782 [CrossRef][PubMed]
    [Google Scholar]
  26. Hucker GJ. A new modification and application of the Gram stain. J Bacteriol 1921; 6:395–397 [CrossRef][PubMed]
    [Google Scholar]
  27. Brown AE, Smith H. Benson's Microbiological Applications, Laboratory Manual in General Microbiology. Short Version McGraw-Hill Education; 2014
    [Google Scholar]
  28. Nowak E, Brousseau R, Garrett J, Masson L, Maynard C et al. Characterization of formulated microbial products by denaturing gradient gel electrophoresis, total cellular fatty acid analysis, and DNA microarray analysis. Can J Microbiol 2008; 54:380–390 [CrossRef][PubMed]
    [Google Scholar]
  29. Hu HY, Fujie K, Urano K. Development of a novel solid phase extraction method for the analysis of bacterial quinones in activated sludge with a higher reliability. J Biosci Bioeng 1999; 87:378–382 [CrossRef][PubMed]
    [Google Scholar]
  30. Minnikin DE, O'Donnell AG, Goodfellow M, Alderson G, Athalye M et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 1984; 2:233–241 [CrossRef]
    [Google Scholar]
  31. Zhou J, Bruns MA, Tiedje JM. DNA recovery from soils of diverse composition. Appl Environ Microbiol 1996; 62:316–322 [CrossRef][PubMed]
    [Google Scholar]
  32. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991; 173:697–703 [CrossRef][PubMed]
    [Google Scholar]
  33. Hutchens E, Radajewski S, Dumont MG, McDonald IR, Murrell JC. Analysis of methanotrophic bacteria in Movile cave by stable isotope probing. Environ Microbiol 2004; 6:111–120 [CrossRef][PubMed]
    [Google Scholar]
  34. Roosaare M, Puustusmaa M, Möls M, Vaher M, Remm M. PlasmidSeeker: identification of known plasmids from bacterial whole genome sequencing reads. PeerJ 2018; 6:e4588 [CrossRef][PubMed]
    [Google Scholar]
  35. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [CrossRef][PubMed]
    [Google Scholar]
  36. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL. Improved microbial gene identification with glimmer. Nucleic Acids Res 1999; 27:4636–4641 [CrossRef][PubMed]
    [Google Scholar]
  37. Lowe TM, Chan PP. tRNAscan-SE on-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 2016; 44:W54–W57 [CrossRef][PubMed]
    [Google Scholar]
  38. Lagesen K, Hallin P, Rødland EA, Staerfeldt H-H, Rognes T et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100–3108 [CrossRef][PubMed]
    [Google Scholar]
  39. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [CrossRef][PubMed]
    [Google Scholar]
  40. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [CrossRef][PubMed]
    [Google Scholar]
  41. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [CrossRef][PubMed]
    [Google Scholar]
  42. Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012; 28:1823–1829 [CrossRef][PubMed]
    [Google Scholar]
  43. Thompson JD, Higgins DG, Gibson TJ. clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22:4673–4680 [CrossRef][PubMed]
    [Google Scholar]
  44. Hall TA. BioEdit : A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999; 41:95–98
    [Google Scholar]
  45. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. mega X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [CrossRef][PubMed]
    [Google Scholar]
  46. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [CrossRef][PubMed]
    [Google Scholar]
  47. Kumar S, Stecher G, Tamura K. mega7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [CrossRef][PubMed]
    [Google Scholar]
  48. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [CrossRef][PubMed]
    [Google Scholar]
  49. Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 1992; 8:275–282 [CrossRef][PubMed]
    [Google Scholar]
  50. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically United database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [CrossRef][PubMed]
    [Google Scholar]
  51. Hanson RS, Hanson TE. Methanotrophic bacteria. Microbiol Rev 1996; 60:439–471[PubMed]
    [Google Scholar]
  52. Khadem AF, van Teeseling MCF, van Niftrik L, Jetten MSM, Op den Camp HJM et al. Genomic and physiological Analysis of carbon storage in the verrucomicrobial Methanotroph "Ca. Methylacidiphilum Fumariolicum" SolV. Front Microbiol 2012; 3:345 [CrossRef][PubMed]
    [Google Scholar]
  53. van Teeseling MCF, Pol A, Harhangi HR, van der Zwart S, Jetten MSM et al. Expanding the verrucomicrobial methanotrophic world: description of three novel species of Methylacidimicrobium gen. nov. Appl Environ Microbiol 2014; 80:6782–6791 [CrossRef][PubMed]
    [Google Scholar]
  54. Linton JD, Cripps RE. The occurrence and identification of intracellular polyglucose storage granules in Methylococcus NCIB 11083 grown in chemostat culture on methane. Arch Microbiol 1978; 117:41–48 [CrossRef][PubMed]
    [Google Scholar]
  55. Tavormina PL, Kellermann MY, Antony CP, Tocheva EI, Dalleska NF et al. Starvation and recovery in the deep-sea methanotroph Methyloprofundus sedimenti . Mol Microbiol 2017; 103:242–252 [CrossRef][PubMed]
    [Google Scholar]
  56. Frindte K, Maarastawi SA, Lipski A, Hamacher J, Knief C. Characterization of the first rice paddy cluster I isolate, Methyloterricola oryzae gen. nov., sp. nov. and amended description of Methylomagnum ishizawai . Int J Syst Evol Microbiol 2017; 67:4507–4514 [CrossRef][PubMed]
    [Google Scholar]
  57. Pieja AJ, Rostkowski KH, Criddle CS. Distribution and selection of poly-3-hydroxybutyrate production capacity in methanotrophic Proteobacteria . Microb Ecol 2011; 62:564–573 [CrossRef][PubMed]
    [Google Scholar]
  58. Collins MD, Green PN. Isolation and characterization of a novel coenzyme Q from some methane-oxidizing bacteria. Biochem Biophys Res Commun 1985; 133:1125–1131 [CrossRef][PubMed]
    [Google Scholar]
  59. Eshinimaev BT, Medvedkova KA, Khmelenina VN, Suzina NE, Osipov GA et al. New thermophilic methanotrophs of the genus Methylocaldum . Mikrobiologiia 2004; 73:448–456[PubMed]
    [Google Scholar]
  60. Makula RA. Phospholipid composition of methane-utilizing bacteria. J Bacteriol 1978; 134:771–777 [CrossRef][PubMed]
    [Google Scholar]
  61. Houghton KM, Stewart LC. Temperature-gradient incubation isolates multiple competitive species from a single environmental sample. Access Microbiology 2019
    [Google Scholar]
  62. Ward N, Larsen Øivind, Sakwa J, Bruseth L, Khouri H et al. Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2004; 2:e303 [CrossRef][PubMed]
    [Google Scholar]
  63. Chan JZ-M, Halachev MR, Loman NJ, Constantinidou C, Pallen MJ. Defining bacterial species in the genomic era: insights from the genus Acinetobacter . BMC Microbiol 2012; 12:302 [CrossRef][PubMed]
    [Google Scholar]
  64. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [CrossRef][PubMed]
    [Google Scholar]
  65. Ghashghavi M, Belova SE, Bodelier PLE, Dedysh SN, Kox MAR et al. Methylotetracoccus oryzae strain C50C1 is a novel type Ib gammaproteobacterial methanotroph adapted to freshwater environments. mSphere 2019; 4:e00631–00618 [CrossRef][PubMed]
    [Google Scholar]
  66. Hoefman S, van der Ha D, Iguchi H, Yurimoto H, Sakai Y et al. Methyloparacoccus murrellii gen. nov., sp. nov., a methanotroph isolated from pond water. Int J Syst Evol Microbiol 2014; 64:2100–2107 [CrossRef][PubMed]
    [Google Scholar]
  67. Geymonat E, Ferrando L, Tarlera SE. Methylogaea oryzae gen. nov., sp. nov., a mesophilic methanotroph isolated from a rice paddy field. Int J Syst Evol Microbiol 2011; 61:2568–2572 [CrossRef][PubMed]
    [Google Scholar]
  68. Kleiveland CR, Hult LTO, Kuczkowska K, Jacobsen M, Lea T et al. Draft genome sequence of the methane-oxidizing bacterium Methylococcus capsulatus (Texas). J Bacteriol 2012; 194:6626 [CrossRef][PubMed]
    [Google Scholar]
  69. Takeuchi M, Kamagata Y, Oshima K, Hanada S, Tamaki H et al. Methylocaldum marinum sp. nov., a thermotolerant, methane-oxidizing bacterium isolated from marine sediments, and emended description of the genus Methylocaldum . Int J Syst Evol Microbiol 2014; 64:32403246 [CrossRef][PubMed]
    [Google Scholar]
  70. Takeuchi M, Ozaki H, Hiraoka S, Kamagata Y, Sakata S et al. Possible cross-feeding pathway of facultative methylotroph Methyloceanibacter caenitepidi Gela4 on methanotroph Methylocaldum marinum S8. PLoS One 2019; 14:e0213535 [CrossRef][PubMed]
    [Google Scholar]
  71. Frindte K, Kalyuzhnaya MG, Bringel F, Dunfield PF, Jetten MSM et al. Draft genome sequences of two gammaproteobacterial methanotrophs isolated from rice ecosystems. Genome Announc 2017; 5:e00526–00517 [CrossRef][PubMed]
    [Google Scholar]
  72. Khalifa A, Lee CG, Ogiso T, Ueno C, Dianou D et al. Methylomagnum ishizawai gen. nov., sp. nov., a mesophilic type I methanotroph isolated from rice rhizosphere. Int J Syst Evol Microbiol 2015; 65:3527–3534 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004442
Loading
/content/journal/ijsem/10.1099/ijsem.0.004442
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error