sp. nov., a lanthanide-dependent methylotrophic bacteria isolated from rice field soil Free

Abstract

A new lanthanide (Ln)-dependent methanol-utilizing bacterial strain, La3113, was isolated from rice field soil and its taxonomic position was investigated using polyphasic approaches. The strain was aerobic, Gram-stain-negative, strongly motile, catalase-positive and cytochrome oxidase-positive. It could neither catalyse the hydrolysis of urea nor reduce nitrate to nitrite. Growth was observed within a temperature range of 10–40 °C and a pH range of 6–8, with optimum growth at 28 °C and pH 7. Methylamine was utilized as the single source of energy, carbon and nitrogen, and it was oxidized by methylamine dehydrogenase. C 7, C 6 and C were the dominant cellular fatty acids. Its draft genome (2.67 Mbp and 44.9 mol% G+C content) encodes genes including three Ln-dependent methanol dehydrogenase (XoxF-type MDH) genes, those for formaldehyde assimilation (ribulose monophosphate pathway), formate dehydrogenases and methylamine dehydrogenases, but not Ca-dependent MDH (MxaFI-MDH), which characterizes the species as a Ln-dependent methylotroph. The 16S rRNA gene sequence showed that strain La3113 belongs to the genus and is closely related to JLW8 (98.29 % identity). The digital DNA–DNA hybridization (dDDH) values (less than 30 %) and average nucleotide identity (ANI) values (less than 85 %) between genomes of strain La3113 and related type strains were lower than the thresholds for species delineation (70 % for dDDH and 95–96 % for ANI). On the basis of these polyphasic approaches, we propose a novel species, sp. nov. (type strain La3113=NBRC 111954=DSM 103219).

Funding
This study was supported by the:
  • KAKENHI (Award 15H04476)
  • KAKENHI (Award 18H02129)
  • Yakumo Foundation
  • China Scholarship Council, http://dx.doi.org/10.13039/501100004543
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004098
2020-03-16
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/70/4/2713.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004098&mimeType=html&fmt=ahah

References

  1. Anthony C. The Biochemistry of Methylotrophs London, UK: Academic Press; 1982
    [Google Scholar]
  2. Keltjens JT, Pol A, Reimann J, Op den Camp HJM. Pqq-Dependent methanol dehydrogenases: rare-earth elements make a difference. Appl Microbiol Biotechnol 2014; 98:6163–6183 [View Article]
    [Google Scholar]
  3. Hibi Y, Asai K, Arafuka H, Hamajima M, Iwama T et al. Molecular structure of La3+-induced methanol dehydrogenase-like protein in Methylobacterium radiotolerans . J Biosci Bioeng 2011; 111:547–549 [View Article]
    [Google Scholar]
  4. Chistoserdova L. Modularity of methylotrophy, revisited. Environ Microbiol 2011; 13:2603–2622 [View Article]
    [Google Scholar]
  5. Taubert M, Grob C, Howat AM, Burns OJ, Dixon JL et al. XoxF encoding an alternative methanol dehydrogenase is widespread in coastal marine environments. Environ Microbiol 2015; 17:3937–3948 [View Article]
    [Google Scholar]
  6. Ramachandran A, Walsh DA. Investigation of XoxF methanol dehydrogenases reveals new methylotrophic bacteria in pelagic marine and freshwater ecosystems. FEMS Microbiol Ecol 2015; 91:fiv105 [View Article]
    [Google Scholar]
  7. Vekeman B, Speth D, Wille J, Cremers G, De Vos P et al. Genome characteristics of two novel type I methanotrophs enriched from North Sea sediments containing exclusively a lanthanide-dependent XoxF5-Type methanol dehydrogenase. Microb Ecol 2016; 72:503–509 [View Article]
    [Google Scholar]
  8. Del Rocío Bustillos-Cristales M, Corona-Gutierrez I, Castañeda-Lucio M, Águila-Zempoaltécatl C, Seynos-García E et al. Culturable facultative methylotrophic bacteria from the cactus Neobuxbaumia macrocephala possess the locus xoxF and consume methanol in the presence of Ce3+ and Ca2 . Microbes Environ 2017; 32:244–251 [View Article]
    [Google Scholar]
  9. Lv H, Masuda S, Fujitani Y, Sahin N, Tani A. Oharaeibacter diazotrophicus gen. nov., sp. nov., a diazotrophic and facultatively methylotrophic bacterium, isolated from rice rhizosphere. Int J Syst Evol Microbiol 2017; 67:576–582 [View Article]
    [Google Scholar]
  10. Lv H, Sahin N, Tani A. Isolation and genomic characterization of Novimethylophilus kurashikiensis gen. nov. sp. nov., a new lanthanide-dependent methylotrophic species of Methylophilaceae . Environ Microbiol 2018; 20:1204–1223 [View Article]
    [Google Scholar]
  11. Kalyuzhnaya MG, Bowerman S, Lara JC, Lidstrom ME, Chistoserdova L. Methylotenera mobilis gen. nov., sp. nov., an obligately methylamine-utilizing bacterium within the family Methylophilaceae . Int J Syst Evol Microbiol 2006; 56:2819–2823 [View Article]
    [Google Scholar]
  12. Kalyuzhnaya MG, Beck DAC, Vorobev A, Smalley N, Kunkel DD et al. Novel methylotrophic isolates from lake sediment, description of Methylotenera versatilis sp. nov. and emended description of the genus Methylotenera . Int J Syst Evol Microbiol 2012; 62:106–111 [View Article]
    [Google Scholar]
  13. Beck DAC, McTaggart TL, Setboonsarng U, Vorobev A, Kalyuzhnaya MG et al. The expanded diversity of Methylophilaceae from lake Washington through cultivation and genomic sequencing of novel ecotypes. PLoS One 2014; 9:e102458 [View Article]
    [Google Scholar]
  14. Whittenbury R, Phillips KC, Wilkinson JF, Enrichment WJF. Enrichment, isolation and some properties of methane-utilizing bacteria. J Gen Microbiol 1970; 61:205–218 [View Article]
    [Google Scholar]
  15. Gerhardt P, Murray RGE, Wood WA, Krieg NR. Methods for General and Molecular Bacteriology Washington, DC: American Society for Microbiology; 1994
    [Google Scholar]
  16. Smibert RM, Krieg NR. Phenotypic characterization. In Gerhardt P. editor Methods for General and Molecular Bacteriology Washington, DC: American Society for Microbiology; 1994 pp 607–.654
    [Google Scholar]
  17. Eckert B, Weber OB, Kirchhof G, Halbritter A, Stoffels M et al. Azospirillum doebereinerae sp. nov., a nitrogen-fixing bacterium associated with the C4-grass Miscanthus . Int J Syst Evol Microbiol 2001; 51:17–26 [View Article]
    [Google Scholar]
  18. Kalyuzhnaya MG, Stolyar SM, Auman AJ, Lara JC, Lidstrom ME et al. Methylosarcina lacus sp. nov., a methanotroph from Lake Washington, Seattle, USA, and emended description of the genus Methylosarcina . Int J Syst Evol Microbiol 2005; 55:2345–2350 [View Article]
    [Google Scholar]
  19. Tani A, Sahin N, Matsuyama Y, Enomoto T, Nishimura N et al. High-throughput identification and screening of novel Methylobacterium species using whole-cell MALDI-TOF/MS analysis. PLoS One 2012; 7:e40784 [View Article]
    [Google Scholar]
  20. 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]
    [Google Scholar]
  21. 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]
    [Google Scholar]
  22. Lee I, Ouk Kim Y, Park S-C, Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article]
    [Google Scholar]
  23. 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]
    [Google Scholar]
  24. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009; 106:19126–19131 [View Article]
    [Google Scholar]
  25. 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]
  26. 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 [View Article]
    [Google Scholar]
  27. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W et al. Silva: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 2007; 35:7188–7196 [View Article]
    [Google Scholar]
  28. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article]
    [Google Scholar]
  29. McTaggart TL, Benuska G, Shapiro N, Woyke T, Chistoserdova L. Draft genome sequences of five new strains of Methylophilaceae isolated from lake Washington sediment. Genome Announc 2015; 3:e01511-14 [View Article]
    [Google Scholar]
  30. Na S-I, Kim YO, Yoon S-H, Ha S-M, Baek I et al. UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 2018; 56:280–285 [View Article]
    [Google Scholar]
  31. Taubert M, Grob C, Howat AM, Burns OJ, Dixon JL et al. XoxF encoding an alternative methanol dehydrogenase is widespread in coastal marine environments. Environ Microbiol 2015; 17:3937–3948 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004098
Loading
/content/journal/ijsem/10.1099/ijsem.0.004098
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed