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INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 73, Issue 5

Physiological and genomic analyses of cobalamin (vitamin B)-auxotrophy of sp. nov., a methionine-auxotrophic chitinolytic bacterium isolated from chitin-treated soil No Access

Abstract

A novel bacterium designated 5-21a, isolated from chitin-treated upland soil, exhibits methionine (Met) auxotrophy and chitinolytic activity. A physiological experiment revealed the cobalamin (synonym, vitamin B)(Cbl)-auxotrophic property of strain 5-21a. The newly determined complete genomic sequence indicated that strain 5-21a possesses only the putative gene for Cbl-dependent Met synthase (MetH) and lacks that for the Cbl-independent one (MetE), which implies the requirement of Cbl for Met-synthesis in strain 5-21a. The set of genes for the upstream (corrin ring synthesis) pathway of Cbl synthesis is absent in the genome of strain 5-21a, which explains the Cbl-auxotrophy of 5-21a. This strain was characterized via a polyphasic approach to determine its taxonomic position. The nucleotide sequences of two copies of the 16S rRNA gene of strain 5-21a indicated the highest similarities to DCY21(99.8 and 99.9 %) and CJ29(98.7 and 98.8 %, respectively), whose Cbl-auxotrophic properties were revealed in this study. The principal respiratory quinone was Q-8. The predominant cellular fatty acids were iso-C, iso-C and iso-C 9. The complete genome sequence of strain 5-21a revealed that the genome size was 4 155 451 bp long and the G+C content was 67.87 mol%. The average nucleotide identity and digital DNA–DNA hybridization values between strain 5-21a and its most closely phylogenetic relative DCY21 were 88.8 and 36.5%, respectively. Based on genomic, chemotaxonomic, phenotypic and phylogenetic data, strain 5-21a represents a novel species in the genus , for which the name sp. nov. is proposed. The type strain is 5-21a (=NBRC 115507=LMG 32660).

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  • Accepted:
  • Published Online:
Keyword(s): auxotroph , cobalamin , Lysobacter , methionine and vitamin B12
Funding
This study was supported by the:
  • KAKENHI (Award 21K05331)
    • Principle Award Recipient: AkihiroSaito
  • KAKENHI (Award 16K07648)
    • Principle Award Recipient: AkihiroSaito
© 2023 The Authors
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2023-05-19
2024-04-25
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References

  1. Christensen P. Lysobacter. In Trujillo ME, Dedysh S, DeVos P, Hedlund B, Kämpfer P et al. eds Bergey’s Manual of Systematics of Archaea and Bacteria 2015 p gbm01232
     [Google Scholar]
  2. Xie Y, Wright S, Shen Y, Du L. Bioactive natural products from Lysobacter. Nat Prod Rep 2012; 29:1277–1287 [View Article] [PubMed]
     [Google Scholar]
  3. Panthee S, Hamamoto H, Paudel A, Sekimizu K. Lysobacter species: a potential source of novel antibiotics. Arch Microbiol 2016; 198:839–845 [View Article] [PubMed]
     [Google Scholar]
  4. Puopolo G, Tomada S, Pertot I. The impact of the omics era on the knowledge and use of Lysobacter species to control phytopathogenic micro-organisms. J Appl Microbiol 2018; 124:15–27 [View Article] [PubMed]
     [Google Scholar]
  5. Kumeta Y, Inami K, Ishimaru K, Yamazaki Y, Sameshima-Saito R et al. Thermogravimetric evaluation of chitin degradation in soil: implication for the enhancement of ammonification of native organic nitrogen by chitin addition. Soil Sci Plant Nutr 2018; 64:512–519 [View Article]
     [Google Scholar]
  6. Iwasaki Y, Ichino T, Saito A. Transition of the bacterial community and culturable chitinolytic bacteria in chitin-treated upland soil: from Streptomyces to methionine-auxotrophic Lysobacter and other genera. Microb Environ 2020; 35: [View Article]
     [Google Scholar]
  7. Choi JH, Seok JH, Cha JH, Cha CJ. Lysobacter panacisoli sp. nov., isolated from ginseng soil. Int J Syst Evol Microbiol 2014; 64:2193–2197 [View Article] [PubMed]
     [Google Scholar]
  8. Choi J-H, Seok J-H, Cha J-H, Cha C-J. Lysobacter panacisoli sp. nov., isolated from ginseng soil. Int J Syst Evol Microbiol 2014; 64:2193–2197 [View Article] [PubMed]
     [Google Scholar]
  9. González JC, Peariso K, Penner-Hahn JE, Matthews RG. Cobalamin-independent methionine synthase from Escherichia coli: a zinc metalloenzyme. Biochemistry 1996; 35:12228–12234 [View Article] [PubMed]
     [Google Scholar]
  10. Shelton AN, Seth EC, Mok KC, Han AW, Jackson SN et al. Uneven distribution of cobamide biosynthesis and dependence in bacteria predicted by comparative genomics. ISME J 2019; 13:789–804 [View Article] [PubMed]
     [Google Scholar]
  11. Bretscher AP, Kaiser D. Nutrition of Myxococcus xanthus, a fruiting myxobacterium. J Bacteriol 1978; 133:763–768 [View Article] [PubMed]
     [Google Scholar]
  12. Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 2005; 438:90–93 [View Article] [PubMed]
     [Google Scholar]
  13. Roth JR, Lawrence JG, Bobik TA. Cobalamin (coenzyme B12): synthesis and biological significance. Annu Rev Microbiol 1996; 50:137–181 [View Article] [PubMed]
     [Google Scholar]
  14. Perruchon C, Vasileiadis S, Papadopoulou ES, Karpouzas DG. Genome-based metabolic reconstruction unravels the key role of B12 in methionine auxotrophy of an ortho-phenylphenol-degrading Sphingomonas haloaromaticamans. Front Microbiol 2019; 10:3009 [View Article] [PubMed]
     [Google Scholar]
  15. Schlochtermeier A, Walter S, Schröder J, Moorman M, Schrempf H. The gene encoding the cellulase (Avicelase) Cel1 from Streptomyces reticuli and analysis of protein domains. Mol Microbiol 1992; 6:3611–3621 [View Article] [PubMed]
     [Google Scholar]
  16. Weon H-Y, Kim B-Y, Kim M-K, Yoo S-H, Kwon S-W et al. Lysobacter niabensis sp. nov. and Lysobacter niastensis sp. nov., isolated from greenhouse soils in Korea. Int J Syst Evol Microbiol 2007; 57:548–551 [View Article]
     [Google Scholar]
  17. Fang B-Z, Xie Y-G, Zhou X-K, Zhang X-T, Liu L et al. Lysobacter prati sp. nov., isolated from a plateau meadow sample. Antonie van Leeuwenhoek 2020; 113:763–772 [View Article]
     [Google Scholar]
  18. Kim KR, Kim KH, Khan SA, Kim HM, Han DM et al. Lysobacter arenosi sp. nov. and Lysobacter solisilvae sp. nov. isolated from soil. J Microbiol 2021; 59:709–717 [View Article] [PubMed]
     [Google Scholar]
  19. Saito A, Mitsui H, Hattori R, Minamisawa K, Hattori T. Slow-growing and oligotrophic soil bacteria phylogenetically close to Bradyrhizobium japonicum. FEMS Microbiol Ecol 1998; 25:277–286 [View Article]
     [Google Scholar]
  20. Barnett DW, Garrison EK, Quinlan AR, Strömberg MP, Marth GT. BamTools: a C++ API and toolkit for analyzing and managing BAM files. Bioinformatics 2011; 27:1691–1692 [View Article] [PubMed]
     [Google Scholar]
  21. Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol 2019; 37:540–546 [View Article] [PubMed]
     [Google Scholar]
  22. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [View Article] [PubMed]
     [Google Scholar]
  23. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
     [Google Scholar]
  24. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv 2013arXiv:1303.3997
     [Google Scholar]
  25. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article] [PubMed]
     [Google Scholar]
  26. Tanizawa Y, Fujisawa T, Nakamura Y. DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 2018; 34:1037–1039 [View Article] [PubMed]
     [Google Scholar]
  27. Lomsadze A, Gemayel K, Tang SYY, Borodovsky M. Modeling leaderless transcription and atypical genes results in more accurate gene prediction in prokaryotes. Genome Res 2018; 28:1079–1089 [View Article] [PubMed]
     [Google Scholar]
  28. Noguchi H, Taniguchi T, Itoh T. MetaGeneAnnotator: detecting species-specific patterns of ribosomal binding site for precise gene prediction in anonymous prokaryotic and phage genomes. DNA Res 2008; 15:387–396 [View Article] [PubMed]
     [Google Scholar]
  29. 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 [View Article] [PubMed]
     [Google Scholar]
  30. Chan PP, Lin BY, Mak AJ, Lowe TM. tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes. Nucleic Acids Res 2021; 49:9077–9096 [View Article] [PubMed]
     [Google Scholar]
  31. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A 2005; 102:2567–2572 [View Article] [PubMed]
     [Google Scholar]
  32. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article] [PubMed]
     [Google Scholar]
  33. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
     [Google Scholar]
  34. Tamura K, Stecher G, Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article] [PubMed]
     [Google Scholar]
  35. Na S-I, Kim YO, Yoon S-H, Ha S, 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]
  36. Barrow GI, Feltham RKA. eds Cowan and Steel’s Manual for the Identification of Medical Bacteria, 3rd edn. Cambridge: Cambridge University Press; 1993 [View Article]
     [Google Scholar]
  37. Sasser M. Technical Note 101: Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids Newark, DE: MIDI; 1990
     [Google Scholar]
  38. Kaleta C, Schäuble S, Rinas U, Schuster S. Metabolic costs of amino acid and protein production in Escherichia coli. Biotechnol J 2013; 8:1105–1114 [View Article]
     [Google Scholar]
  39. Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS. Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes. J Biol Chemist 2003; 278:41148–41159 [View Article]
     [Google Scholar]
  40. Lu X, Heal KR, Ingalls AE, Doxey AC, Neufeld JD. Metagenomic and chemical characterization of soil cobalamin production. ISME J 2020; 14:53–66 [View Article]
     [Google Scholar]
  41. Perlman D. Microbial synthesis of cobamides. Adv Appl Microbiol 1959; 1:87–122 [View Article] [PubMed]
     [Google Scholar]
  42. Martens JH, Barg H, Warren MJ, Jahn D. Microbial production of vitamin B12. Appl Microbiol Biotechnol 2002; 58:275–285 [View Article] [PubMed]
     [Google Scholar]
  43. Bae HS, Im WT, Lee ST. Lysobacter concretionis sp. nov., isolated from anaerobic granules in an upflow anaerobic sludge blanket reactor. Int J Syst Evol Microbiol 2005; 55:1155–1161 [View Article] [PubMed]
     [Google Scholar]
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Physiological and genomic analyses of cobalamin (vitamin B12)-auxotrophy of Lysobacter auxotrophicus sp. nov., a methionine-auxotrophic chitinolytic bacterium isolated from chitin-treated soil
Int J Syst Evol Microbiol 73, 005899 (2023); https://doi.org/10.1099/ijsem.0.005899
/content/journal/ijsem/10.1099/ijsem.0.005899
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