Skip to content
1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo International Journal of Systematic and Evolutionary Microbiology

Volume 73, Issue 6

sp. nov., a type II methane-oxidizing bacterium from surface soil of a rice paddy field in Japan, and emended description of the genus ( Whittenbury . 1970) Bowman . 1993 No Access

Abstract

A novel methane-oxidizing bacterial strain SS37A-Re was isolated from surface soil of a rice paddy field in Japan. Cells were Gram-stain-negative, motile rods with single polar flagellum and type II intracytoplasmic membrane arrangement. The strain grew on methane or methanol as the sole carbon and energy source. It grew at 15–37 °C (optimum 25–30 °C), pH 6.0–9.0 (optimum 7.0–8.0) and with 0–0.1 % (w/w) NaCl (no growth at 0.5 % or above). Cells formed cysts, but not exospores. The results of sequence analysis of the 16S rRNA gene indicated that SS37A-Re represented a member of the family , with the highest similarity (98.9 %) to corrig. OBBP. Phylogenetic analysis of and genes and core genes in the genome indicated that the strain was closely related to the members of the genus , while the analysis of the gene indicated the close relationships with the genus . The values of genome relatedness between SS37A-Re and species of the genera and were 78.6–82.5% and 21.7–24.9 % estimated by the average nucleotide identity and digital DNA–DNA hybridisation, respectively, showing the highest values with LMG 27198. The DNA G+C content was 63.2 mol% (genome). The major quinone and fatty acids were Q-8 and, C (Cω8 and Cω8) and C, respectively. On the basis of the phenotypic and phylogenetic features, the strain represents a novel species of the genus , for which the name sp. nov. is proposed. The type strain is SS37A-Re (=JCM 34278 =NBRC 114996=KCTC 82710).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Flagella , Methylocystis iwaonis , motility , rice paddy field , surface soil and type II methane-oxidizing bacteria
Funding
This study was supported by the:
  • New Energy and Industrial Technology Development Organization (Award JPNP18016)
    • Principle Award Recipient: SusumuAsakawa
  • Matsumae International Foundation (Award 18G11)
    • Principle Award Recipient: MohammadSaiful Alam
  • University Nazi BONI
    • Principle Award Recipient: JosephBenewindé Sawadogo
  • Public Foundation of Chubu Science and Technology Center (Award Greater Nagoya Invitation Fellowship for Foreign Researchers in the Field of Environment)
    • Principle Award Recipient: DayériDianou
  • ESPEC Foundation (Award Global Environment Research and Technology (Charitable Trust))
    • Principle Award Recipient: SusumuAsakawa
  • Japan Society for the Promotion of Science (Award JSPS Invitation Fellowship for Foreign Researchers)
    • Principle Award Recipient: DayériDianou
© 2023 The Authors
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005925
2023-06-06
2025-01-26
Loading full text...

Full text loading...

References

  1. Ciais P, Sabine C, Bala G, Bopp L, Brovkin V et al. Carbon and other biogeochemical cycles. In Stocker TF, Qin D, Plattner GK, Tignor M et al. eds Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change Cambridge: Cambridge University Press; 2013 pp 465–570
     [Google Scholar]
  2. Hanson RS, Hanson TE. Methanotrophic bacteria. Microbiol Rev 1996; 60:439–471 [View Article] [PubMed]
     [Google Scholar]
  3. Bowman JP. The methanotrophs—The families Methylococcaceae and Methylocystaceae. In Dworkin M, Falkow S, Rosenberg E, Schleifer K-H. eds The Prokaryotes: A Handbook on the Biology of BacteriaProteobacteria: Alpha and Beta Sublcalssses, 3rd ed. vol 5 Springer; 2006 pp 266–289 [View Article]
     [Google Scholar]
  4. Dedysh SN, Knief C. Diversity and phylogeny of described aerobic methanotrophs. In Kalyuzhnaya MG, Xing X-H. eds Methane Biocatalysis: Paving the Way to Sustainability Springer; 2018 pp 17–42 [View Article]
     [Google Scholar]
  5. 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 [View Article] [PubMed]
     [Google Scholar]
  6. Ogiso T, Ueno C, Dianou D, Huy TV, Katayama A et al. Methylomonas koyamae sp. nov., a type I methane-oxidizing bacterium from floodwater of a rice paddy field. Int J Syst Evol Microbiol 2012; 62:1832–1837 [View Article] [PubMed]
     [Google Scholar]
  7. 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 [View Article] [PubMed]
     [Google Scholar]
  8. 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 [View Article] [PubMed]
     [Google Scholar]
  9. Pandit PS, Rahalkar MC. Renaming of ‘Candidatus Methylocucumis oryzae’ as Methylocucumis oryzae gen. nov., sp. nov., a novel Type I methanotroph isolated from India. Antonie van Leeuwenhoek 2019; 112:955–959 [View Article]
     [Google Scholar]
  10. Asakawa S. Ecology of methanogenic and methane-oxidizing microorganisms in paddy soil ecosystem. Soil Sci Plant Nutr 2021; 67:520–526 [View Article]
     [Google Scholar]
  11. Le Mer J, Escoffier S, Chessel C, Roger PA. Microbiological aspects of methane emission in a ricefield soil from the Camargue (France): 2. methanotrophy and related microflora. Eur J Soil Biol 1996; 32:71–80
     [Google Scholar]
  12. Gilbert B, Aßmus B, Hartmann A, Frenzel P. In situ localization of two methanotrophic strains in the rhizosphere of rice plants. FEMS Microbiol Ecol 1998; 25:117–128 [View Article]
     [Google Scholar]
  13. Takeda K, Suzuki S, Neko K, Tomiyama Y, Fujita T et al. Enumeration and characterization of methanotrophs in paddy soils and rice roots. Jpn J Soil Sci Plant Nutr 1998; 69:570–575 [View Article]
     [Google Scholar]
  14. Dianou D, Adachi K. Characterization of methanotrophic bacteria isolated from a subtropical paddy field. FEMS Microbiol Lett 1999; 173:163–173 [View Article]
     [Google Scholar]
  15. van Bodegom P, Stams F, Mollema L, Boeke S, Leffelaar P. Methane oxidation and the competition for oxygen in the rice rhizosphere. Appl Environ Microbiol 2001; 67:3586–3597 [View Article] [PubMed]
     [Google Scholar]
  16. Takeda K, Tonouchi A, Takada M, Suko T, Suzuki S et al. Characterization of cultivable methanotrophs from paddy soils and rice roots. Soil Sci Plant Nutr 2008; 54:876–885 [View Article]
     [Google Scholar]
  17. Bao Z, Shinoda R, Minamisawa K. Draft genome sequence of Methylosinus sp. strain 3S-1, an isolate from rice root in a low-nitrogen paddy field. Genome Announc 2016; 4:e00932-16 [View Article] [PubMed]
     [Google Scholar]
  18. Pandit PS, Rahalkar MC, Dhakephalkar PK, Ranade DR, Pore S et al. Deciphering community structure of methanotrophs dwelling in rice rhizospheres of an Indian rice field using cultivation and cultivation-independent approaches. Microb Ecol 2016; 71:634–644 [View Article]
     [Google Scholar]
  19. Rahalkar MC, Patil S, Dhakephalkar PK, Bahulikar RA. Cultivated methanotrophs associated with rhizospheres of traditional rice landraces from Western India belong to Methylocaldum and Methylocystis. 3 Biotech 2018; 8:281 [View Article]
     [Google Scholar]
  20. 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 Bacteriol 1993; 43:735–753 [View Article]
     [Google Scholar]
  21. Bowman JP. Methylocystis. In Trujillo ME, Dedysh S, DeVos P, Hedlund B, Kämpfer P et al. eds Bergey’s Manual of Systematics of Archaea and Bacteria John Wiley & Sons; 2015 [View Article]
     [Google Scholar]
  22. Wartiainen I, Hestnes AG, McDonald IR, Svenning MM. Methylocystis rosea sp. nov., a novel methanotrophic bacterium from Arctic wetland soil, Svalbard, Norway (78º N). Int J Syst Evol Microbiol 2006; 56:541–547 [View Article] [PubMed]
     [Google Scholar]
  23. Dedysh SN, Belova SE, Bodelier PLE, Smirnova KV, Khmelenina VN et al. Methylocystis heyeri sp. nov., a novel type II methanotrophic bacterium possessing ‘signature’ fatty acids of type I methanotrophs. Int J Syst Evol Microbiol 2007; 57:472–479 [View Article] [PubMed]
     [Google Scholar]
  24. Lindner AS, Pacheco A, Aldrich HC, Costello Staniec A, Uz I et al. Methylocystis hirsuta sp. nov., a novel methanotroph isolated from a groundwater aquifer. Int J Syst Evol Microbiol 2007; 57:1891–1900 [View Article] [PubMed]
     [Google Scholar]
  25. Belova SE, Kulichevskaya IS, Bodelier PLE, Dedysh SN. Methylocystis bryophila sp. nov., a facultatively methanotrophic bacterium from acidic Sphagnum peat, and emended description of the genus Methylocystis (ex Whittenbury et al. 1970) Bowman et al. 1993. Int J Syst Evol Microbiol 2013; 63:1096–1104 [View Article] [PubMed]
     [Google Scholar]
  26. Tikhonova EN, Grouzdev DS, Avtukh AN, Kravchenko IK. Methylocystis silviterrae sp.nov., a high-affinity methanotrophic bacterium isolated from the boreal forest soil. Int J Syst Evol Microbiol 2021; 71:005166 [View Article] [PubMed]
     [Google Scholar]
  27. Dianou D, Ueno C, Ogiso T, Kimura M, Asakawa S. Diversity of cultivable methane-oxidizing bacteria in microsites of a rice paddy field: investigation by cultivation method and fluorescence in situ hybridization (FISH). Microbes Environ 2012; 27:278–287 [View Article] [PubMed]
     [Google Scholar]
  28. Whittenbury R, Phillips KC, Wilkinson JF. Enrichment, isolation and some properties of methane-utilizing bacteria. J Gen Microbiol 1970; 61:205–218 [View Article]
     [Google Scholar]
  29. Bosse U, Frenzel P. Activity and distribution of methane-oxidizing bacteria in flooded rice soil microcosms and in rice plants (Oryza sativa). Appl Environ Microbiol 1997; 63:1199–1207 [View Article] [PubMed]
     [Google Scholar]
  30. Leadbetter ER, Foster JW. Studies on some methane-utilizing bacteria. Arch Mikrobiol 1958; 30:91–118 [View Article] [PubMed]
     [Google Scholar]
  31. Sowers KR. Isolation of chromosomal and plasmid DNAs from methanogenic archaea. In Sowers KR, Schreier HI. eds Archaea: A Laboratory Manual:Methanogens Cold Spring Harbor Laboratory Press; 1995 pp 369–378
     [Google Scholar]
  32. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991; 173:697–703 [View Article] [PubMed]
     [Google Scholar]
  33. Holmes AJ, Costello A, Lidstrom ME, Murrell JC. Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol Lett 1995; 132:203–208 [View Article]
     [Google Scholar]
  34. Costello AM, Lidstrom ME. Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 1999; 65:5066–5074 [View Article]
     [Google Scholar]
  35. 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 [View Article] [PubMed]
     [Google Scholar]
  36. McDonald IR, Kenna EM, Murrell JC. Detection of methanotrophic bacteria in environmental samples with the PCR. Appl Environ Microbiol 1995; 61:116–121 [View Article] [PubMed]
     [Google Scholar]
  37. Neufeld JD, Schäfer H, Cox MJ, Boden R, McDonald IR et al. Stable-isotope probing implicates Methylophaga spp and novel Gammaproteobacteria in marine methanol and methylamine metabolism. ISME J 2007; 1:480–491 [View Article]
     [Google Scholar]
  38. 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 [View Article]
     [Google Scholar]
  39. Lemoine F, Correia D, Lefort V, Doppelt-Azeroual O, Mareuil F et al. NGPhylogeny.fr: new generation phylogenetic services for non-specialists. Nucleic Acids Res 2019; 47:W260–W265 [View Article] [PubMed]
     [Google Scholar]
  40. Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010; 27:221–224 [View Article] [PubMed]
     [Google Scholar]
  41. Heyer J, Galchenko VF, Dunfield PF. Molecular phylogeny of type II methane-oxidizing bacteria isolated from various environments. Microbiology 2002; 148:2831–2846 [View Article] [PubMed]
     [Google Scholar]
  42. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
     [Google Scholar]
  43. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
     [Google Scholar]
  44. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
     [Google Scholar]
  45. Bayliss SC, Thorpe HA, Coyle NM, Sheppard SK, Feil EJ. PIRATE: a fast and scalable pangenomics toolbox for clustering diverged orthologues in bacteria. Gigascience 2019; 8:giz119 [View Article] [PubMed]
     [Google Scholar]
  46. Dunfield PF, Khmelenina VN, Suzina NE, Trotsenko YA, Dedysh SN. Methylocella silvestris sp. nov., a novel methanotroph isolated from an acidic forest cambisol. Int J Syst Evol Microbiol 2003; 53:1231–1239 [View Article] [PubMed]
     [Google Scholar]
  47. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article] [PubMed]
     [Google Scholar]
  48. 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 [View Article] [PubMed]
     [Google Scholar]
  49. Whittenbury R, Dalton H. The methylotrophic bacteria. In Starr MP, Stolp H, Trüper HG, Balows A et al. eds The Prokaryotes: A Handbook on Habitats, Isolation, and Identification of Bacteria vol 1 Springer-Verlag; 1981 pp 894–902 [View Article]
     [Google Scholar]
  50. Whittenbury R, Davies SL, Davey JF. Exospores and cysts formed by methane-utilizing bacteria. J Gen Microbiol 1970; 61:219–226 [View Article] [PubMed]
     [Google Scholar]
  51. Cleenwerck I, Vandemeulebroecke K, Janssens D, Swings J. Re-examination of the genus Acetobacter, with descriptions of Acetobacter cerevisiae sp. nov. and Acetobacter malorum sp. nov. Int J Syst Evol Microbiol 2002; 52:1551–1558 [View Article] [PubMed]
     [Google Scholar]
  52. Brusseau GA, Tsien H-C, Hanson RS, Wackett LP. Optimization of trichloroethylene oxidation by methanotrophs and the use of a colorimetric assay to detect soluble methane monooxygenase activity. Biodegradation 1990; 1:19–29 [View Article] [PubMed]
     [Google Scholar]
  53. Koh S-C, Bowman JP, Sayler GS. Soluble methane monooxygenase production and trichloroethylene degradation by a type I methanotroph, Methylomonas methanica 68-1. Appl Environ Microbiol 1993; 59:960–967 [View Article] [PubMed]
     [Google Scholar]
  54. Nichols PD, Guckert JB, White DC. Determination of monounsaturated fatty acid double-bond position and geometry for microbial monocultures and complex consortia by capillary GC–MS of their dimethyl disulphide adducts. J Microbiol Methods 1986; 5:49–55 [View Article]
     [Google Scholar]
  55. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959; 37:911–917 [View Article] [PubMed]
     [Google Scholar]
  56. Bowman JP. Family V. Methylocystaceae fam. nov. In Brenner DJ, Krieg NR, Staley JT, Garrity GM. eds Bergey’s Manual of Systematic Bacteriology: The Proteobacteria, Part C, the Alpha-, Beta-, Delta-, and Epsilonbacteria, 2nd ed. vol 2 New York: Springer; 2005 pp 411–422
     [Google Scholar]
  57. Hördt A, López MG, Meier-Kolthoff JP, Schleuning M, Weinhold L-M et al. Analysis of 1,000+ type-strain genomes substantially improves taxonomic classification of Alphaproteobacteria.. Front Microbiol 2020; 11:468 [View Article] [PubMed]
     [Google Scholar]
  58. Romanovskaya VA, Malashenko YR, Bogachenko VN. Corrected diagnosis of the genera and species of methane-utilizing bacteria. Microbiology 1978; 47:96–103
     [Google Scholar]
  59. Oshkin IY, Miroshnikov KK, Grouzdev DS, Dedysh SN. Pan-genome-based analysis as a framework for demarcating two closely related methanotroph genera Methylocystis and Methylosinus.. Microorganisms 2020; 8:768 [View Article] [PubMed]
     [Google Scholar]
  60. Bodelier PLE, Gillisen M-JB, Hordijk K, Damsté JSS, Rijpstra WIC et al. A reanalysis of phospholipid fatty acids as ecological biomarkers for methanotrophic bacteria. ISME J 2009; 3:606–617 [View Article] [PubMed]
     [Google Scholar]
  61. Bowman JP, Skerratt JH, Nichols PD, Sly LI. Phospholipid fatty acid and lipopolysaccharide fatty acid signature lipids in methane-utilizing bacteria. FEMS Microbiol Ecol 1991; 85:15–22 [View Article]
     [Google Scholar]
  62. Gal’chenko VF, Shishkina VN, Suzina NE, Trotsenko A. Isolation and properties of new strains of obligate methanotrophs. Microbiology 1978; 46:723–728
     [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.005925
Loading
Methylocystis iwaonis sp. nov., a type II methane-oxidizing bacterium from surface soil of a rice paddy field in Japan, and emended description of the genus Methylocystis (ex Whittenbury et al. 1970) Bowman et al. 1993
Int J Syst Evol Microbiol 73, 005925 (2023); https://doi.org/10.1099/ijsem.0.005925
/content/journal/ijsem/10.1099/ijsem.0.005925
/content/journal/ijsem/10.1099/ijsem.0.005925
Loading

Data & Media loading...

Supplements

Loading data from figshare Loading data from figshare

Most cited 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