1887

Abstract

A novel mesophilic, hydrogenotrophic methanogen, strain CYW5, was isolated from a sediment sample of a piston core collected from submarine mud volcano MV5 located in the offshore area of southwestern Taiwan. Cells of strain CYW5 were irregular coccids, 0.5–1.0 µm in diameter and lysed easily by 0.01 % sodium dodecyl sulphate (SDS) treatment. Strain CYW5utilized formate or hydrogen plus carbon dioxide as catabolic substrates for methanogenesis. The optimal growth conditions were 37 °C, 0.043–0.085 M NaCl and pH 6.02–7.32. The genomic DNA G+C content calculated from the genome sequence of strain CYW5 was 56.2 mol%. The results of phylogenetic analysis of 16S rRNA gene sequences indicated that strain CYW5 represented a member of the family in the order , and was closely related to the members of the genus . The most closely related species was JR1 (94.9 % of 16S rRNA gene sequence identity). The average nucleotide identity and average amino acid identity values between strain CYW5 and members of the family were 74.7–78.5 % and 49.1–64.9%, respectively. Although many of the morphological and physiological characteristics of strain CYW5 and the species of the genus were similar, they were distinguishable by the differences in genomic G+C content and temperature, NaCl and pH ranges for growth. Based on these phenotypic, phylogenetic and genomic results, we propose that strain CYW5 represents a novel species, of a novel genus, named gen. nov., sp. nov. The type strain is CYW5 (=BCRC AR10048=DSM 100756=NBRC 111404).

Funding
This study was supported by the:
  • Sanming University (Award 20YG09)
    • Principle Award Recipient: Sheng-ChungChen
  • Ministry of Science and Technology, Taiwan, R.O.C. (Award MOST 103~107-3113-M-005-001)
    • Principle Award Recipient: Mei-ChinLai
  • Central Geological Survey, Ministry of Economic Affairs (Award 99-5226904000-04-03)
    • Principle Award Recipient: Mei-ChinLai
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.006164
2023-11-08
2024-10-12
Loading full text...

Full text loading...

References

  1. Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS. Methanogens: reevaluation of a unique biological group. Microbiol Rev 1979; 43:260–296 [View Article] [PubMed]
    [Google Scholar]
  2. Paynter MJ, Hungate RE. Characterization of Methanobacterium mobilis, sp. n., isolated from the bovine rumen. J Bacteriol 1968; 95:1943–1951 [View Article] [PubMed]
    [Google Scholar]
  3. Oren A. The Family Methanomicrobiaceae. In Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F. eds The Prokaryotes Berlin, Heidelberg: Springer; 2014 pp 231–246 [View Article]
    [Google Scholar]
  4. Rivard CJ, Smith PH. Isolation and characterization of a thermophilic marine methanogenic bacterium, Methanogenium thermophilicum sp. nov. Int J Syst Evol Microbiol 1982; 32:430–436 [View Article]
    [Google Scholar]
  5. Ollivier BM, Mah RA, Garcia JL, Boone DR. Isolation and characterization of Methanogenium bourgense sp. nov. Int J Syst Evol Microbiol 1986; 36:297–301 [View Article]
    [Google Scholar]
  6. Romesser JA, Wolfe RS, Mayer F, Spiess E, Walther-Mauruschat A. Methanogenium, a new genus of marine methanogenic bacteria, and characterization of Methanogenium cariaci sp. nov. and Methanogenium marisnigri sp. nov. Arch Microbiol 1979; 121:147–153 [View Article]
    [Google Scholar]
  7. Maestrojuan GM, Boone DR, Xun L, Mah RA, Zhang L. Transfer of Methanogenium bourgense, Methanogenium marisnigri, Methanogenium olentangyi, and Methanogenium thermophilicum to the genus Methanoculleus gen. nov., emendation of Methanoculleus marisnigri and Methanogenium, and description of new strains of Methanoculleus bourgense and Methanoculleus marisnigri. Int J Syst Evol Microbiol 1990; 40:117–122 [View Article]
    [Google Scholar]
  8. Zellner G, Messner P, Winter J, Stackebrandt E. Methanoculleus palmolei sp. nov., an irregularly coccoid methanogen from an anaerobic digester treating wastewater of a palm oil plant in North-Sumatra, Indonesia. Int J Syst Bacteriol 1998; 48:1111–1117 [View Article] [PubMed]
    [Google Scholar]
  9. Dianou D, Miyaki T, Asakawa S, Morii H, Nagaoka K et al. Methanoculleus chikugoensis sp. nov., a novel methanogenic archaeon isolated from paddy field soil in Japan, and DNA-DNA hybridization among Methanoculleus species. Int J Syst Evol Microbiol 2001; 51:1663–1669 [View Article] [PubMed]
    [Google Scholar]
  10. Mikucki JA, Liu Y, Delwiche M, Colwell FS, Boone DR. Isolation of a methanogen from deep marine sediments that contain methane hydrates, and description of Methanoculleus submarinus sp. nov. Appl Environ Microbiol 2003; 69:3311–3316 [View Article] [PubMed]
    [Google Scholar]
  11. Cheng L, Qiu T-L, Li X, Wang W-D, Deng Y et al. Isolation and characterization of Methanoculleus receptaculi sp. nov. from Shengli oil field, China. FEMS Microbiol Lett 2008; 285:65–71 [View Article]
    [Google Scholar]
  12. Tian J, Wang Y, Dong X. Methanoculleus hydrogenitrophicus sp. nov., a methanogenic archaeon isolated from wetland soil. Int J Syst Evol Microbiol 2010; 60:2165–2169 [View Article] [PubMed]
    [Google Scholar]
  13. Shimizu S, Ueno A, Tamamura S, Naganuma T, Kaneko K. Methanoculleus horonobensis sp. nov., a methanogenic archaeon isolated from a deep diatomaceous shale formation. Int J Syst Evol Microbiol 2013; 63:4320–4323 [View Article] [PubMed]
    [Google Scholar]
  14. Weng C-Y, Chen S-C, Lai M-C, Wu S-Y, Lin S et al. Methanoculleus taiwanensis sp. nov., a methanogen isolated from deep marine sediment at the deformation front area near Taiwan. Int J Syst Evol Microbiol 2015; 65:1044–1049 [View Article] [PubMed]
    [Google Scholar]
  15. Chen S-C, Chen M-F, Lai M-C, Weng C-Y, Wu S-Y et al. Methanoculleus sediminis sp. nov., a methanogen from sediments near a submarine mud volcano. Int J Syst Evol Microbiol 2015; 65:2141–2147 [View Article] [PubMed]
    [Google Scholar]
  16. Franzmann PD, Liu Y, Balkwill DL, Aldrich HC, De Macario EC et al. Methanogenium frigidum sp. nov., a psychrophilic, H2-using methanogen from Ace Lake, Antarctica. Int J Syst Bacteriol 1997; 47:1068–1072 [View Article] [PubMed]
    [Google Scholar]
  17. Chong SC, Liu Y, Cummins M, Valentine DL, Boone DR. Methanogenium marinum sp. nov., a H2-using methanogen from Skan Bay, Alaska, and kinetics of H2 utilization. Antonie van Leeuwenhoek 2002; 81:263–270 [View Article] [PubMed]
    [Google Scholar]
  18. Kendall MM, Wardlaw GD, Tang CF, Bonin AS, Liu Y et al. Diversity of Archaea in marine sediments from Skan Bay, Alaska, including cultivated methanogens, and description of Methanogenium boonei sp. nov. Appl Environ Microbiol 2007; 73:407–414 [View Article] [PubMed]
    [Google Scholar]
  19. Rivard CJ, Henson JM, Thomas MV, Smith PH. Isolation and characterization of Methanomicrobium paynteri sp. nov., a mesophilic methanogen isolated from marine sediments. Appl Environ Microbiol 1983; 46:484–490 [View Article] [PubMed]
    [Google Scholar]
  20. Widdel F, Rouviere PE, Wolfe RS. Classification of secondary alcohol-utilizing methanogens including a new thermophilic isolate. Arch Microbiol 1988; 150:477–481 [View Article]
    [Google Scholar]
  21. Zellner G, Messner P, Kneifel H, Tindall BJ, Winter J et al. Methanolacinia gen. nov., incorporating Methanomicrobium paynteri as Methanolacinia paynteri comb. nov. J Gen Appl Microbiol 1989; 35:185–202 [View Article]
    [Google Scholar]
  22. Ollivier B, Cayol JL, Patel BK, Magot M, Fardeau ML et al. Methanoplanus petrolearius sp. nov., a novel methanogenic bacterium from an oil-producing well. FEMS Microbiol Lett 1997; 147:51–56 [View Article] [PubMed]
    [Google Scholar]
  23. Wildgruber G, Thomm M, König H, Ober K, Richiuto T et al. Methanoplanus limicola, a plate-shaped methanogen representing a novel family, the Methanoplanaceae. Arch Microbiol 1982; 132:31–36 [View Article]
    [Google Scholar]
  24. van Bruggen JJA, Zwart KB, Hermans JGF, van Hove EM, Stumm CK. Isolation and characterization of Methanoplanus endosymbiosus sp. nov., an endosymbiont of the marine sapropelic ciliate Metopus contortus Quennerstedt. Arch Microbiol 1986; 144:367–374 [View Article]
    [Google Scholar]
  25. Zellner G, Boone DR, Keswani J, Whitman WB, Woese CR et al. Reclassification of Methanogenium tationis and Methanogenium liminatans as Methanofollis tationis gen. nov., comb. nov. and Methanofollis liminatans comb. nov. and description of a new strain of Methanofollis liminatans. Int J Syst Evol Microbiol 1999; 49:247–255 [View Article] [PubMed]
    [Google Scholar]
  26. Imachi H, Sakai S, Nagai H, Yamaguchi T, Takai K. Methanofollis ethanolicus sp. nov., an ethanol-utilizing methanogen isolated from a lotus field. Int J Syst Evol Microbiol 2009; 59:800–805 [View Article] [PubMed]
    [Google Scholar]
  27. Wu S-Y, Chen S-C, Lai M-C. Methanofollis formosanus sp. nov., isolated from a fish pond. Int J Syst Evol Microbiol 2005; 55:837–842 [View Article] [PubMed]
    [Google Scholar]
  28. Lai MC, Chen SC. Methanofollis aquaemaris sp. nov., a methanogen isolated from an aquaculture fish pond. Int J Syst Evol Microbiol 2001; 51:1873–1880 [View Article] [PubMed]
    [Google Scholar]
  29. Zellner G, Sleytr UB, Messner P, Kneifel H, Winter J. Methanogenium liminatans spec. nov., a new coccoid, mesophilic methanogen able to oxidize secondary alcohols. Arch Microbiol 1990; 153:287–293 [View Article]
    [Google Scholar]
  30. Zabel H, König H, Winter J. Isolation and characterization of a new coccoid methanogen, Methanogenium tatii spec. nov. from a solfataric field on Mount Tatio. Arch Microbiol 1984; 137:308–315 [View Article]
    [Google Scholar]
  31. Göker M, Lu M, Fiebig A, Nolan M, Lapidus A et al. Genome sequence of the mud-dwelling archaeon Methanoplanus limicola type strain (DSM 2279T), reclassification of Methanoplanus petrolearius as Methanolacinia petrolearia and emended descriptions of the genera Methanoplanus and Methanolacinia. Stand Genomic Sci 2014; 9:1076–1088 [View Article] [PubMed]
    [Google Scholar]
  32. Brambilla E, Djao ODN, Daligault H, Lapidus A, Lucas S et al. Complete genome sequence of Methanoplanus petrolearius type strain (SEBR 4847T). Stand Genomic Sci 2010; 3:203–211 [View Article] [PubMed]
    [Google Scholar]
  33. Chen S-C, Hsu S-K, Wang Y, Chung S-H, Chen P-C et al. Distribution and characters of the mud diapirs and mud volcanoes off southwest Taiwan. J Asian Earth Sci 2014; 92:201–214 [View Article]
    [Google Scholar]
  34. Sowers K, Noll K. Techniques for anaerobic growth. In Archaea: A Laboratory Manual vol 2 Cold Spring Harbor Laboratory Press; 1995 pp 15–48
    [Google Scholar]
  35. Wolin E, Wolin MJ, Wolfe R. Formation of methane by bacterial extracts. J Biol Chem 1963; 238:2882–2886 [View Article] [PubMed]
    [Google Scholar]
  36. Ferguson TJ, Mah RA. Isolation and characterization of an H2-oxidizing thermophilic methanogen. Appl Environ Microbiol 1983; 45:265–274 [View Article] [PubMed]
    [Google Scholar]
  37. DeLong EF. Archaea in coastal marine environments. Proc Natl Acad Sci USA 1992; 89:5685–5689 [View Article] [PubMed]
    [Google Scholar]
  38. Utsumi M, Belova SE, King GM, Uchiyama H. Phylogenetic comparison of methanogen diversity in different wetland soils. J Gen Appl Microbiol 2003; 49:75–83 [View Article] [PubMed]
    [Google Scholar]
  39. Gray JP, Herwig RP. Phylogenetic analysis of the bacterial communities in marine sediments. Appl Environ Microbiol 1996; 62:4049–4059 [View Article] [PubMed]
    [Google Scholar]
  40. Turner S, Pryer KM, Miao VP, Palmer JD. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 1999; 46:327–338 [View Article] [PubMed]
    [Google Scholar]
  41. Lai MC, Shih CJ. Characterization of Methanococcus voltaei strain P2F9701a: a new methanogen isolated from estuarine environment. Curr Microbiol 2001; 42:432–437 [View Article] [PubMed]
    [Google Scholar]
  42. Konig H. Isolation and analysis of cell walls from methanogenic archaea. In Archaea: A Laboratory Manual vol 2 Cold Spring Harbor Laboratory Press; 1995 pp 315–328
    [Google Scholar]
  43. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680–685 [View Article] [PubMed]
    [Google Scholar]
  44. Wu S-Y, Lai M-C. Methanogenic archaea isolated from Taiwan’s Chelungpu fault. Appl Environ Microbiol 2011; 77:830–838 [View Article] [PubMed]
    [Google Scholar]
  45. Jarrell KF, Faguy D, Hebert AM, Kalmokoff ML. A general method of isolating high molecular weight DNA from methanogenic archaea (archaebacteria). Can J Microbiol 1992; 38:65–68 [View Article] [PubMed]
    [Google Scholar]
  46. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article] [PubMed]
    [Google Scholar]
  47. Liu Y. Taxonomy of methanogens. In Handbook of Hydrocarbon and Lipid Microbiology Springer; 2010 [View Article]
    [Google Scholar]
  48. Haft DH, DiCuccio M, Badretdin A, Brover V, Chetvernin V et al. RefSeq: an update on prokaryotic genome annotation and curation. Nucleic Acids Res 2018; 46:D851–D860 [View Article] [PubMed]
    [Google Scholar]
  49. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article] [PubMed]
    [Google Scholar]
  50. 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]
  51. 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 [View Article] [PubMed]
    [Google Scholar]
  52. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Microbe 2014; 9:111–118 [View Article]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.006164
Loading
/content/journal/ijsem/10.1099/ijsem.0.006164
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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