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Complete Genome of Bacillus subtilis subsp. subtilis KCTC 3135T and Variation in Cell Wall Genes of B. subtilis Strains

  • Ahn, Seonjoo (Department of Biomedical Sciences, Seoul National University College of Medicine) ;
  • Jun, Sangmi (Convergent Research Center for Emerging Virus Infection, Korea Research Institute of Chemical Technology) ;
  • Ro, Hyun-Joo (Convergent Research Center for Emerging Virus Infection, Korea Research Institute of Chemical Technology) ;
  • Kim, Ju Han (Department of Biomedical Sciences, Seoul National University College of Medicine) ;
  • Kim, Seil (Division of Chemical and Medical Metrology, Center for Bioanalysis, Korea Research Institute of Standards and Science)
  • Received : 2017.12.06
  • Accepted : 2018.08.27
  • Published : 2018.10.28

Abstract

The type strain Bacillus subtilis subsp. subtilis KCTC $3135^T$ was deeply sequenced and annotated, replacing a previous draft genome in this study. The tar and tag genes were involved in synthesizing wall teichoic acids (WTAs), and these genes and their products were previously regarded as the distinguishing difference between B. s. subtilis and B. s. spizizenii. However, a comparative genomic analysis of B. subtilis spp. revealed that both B. s. subtilis and B. s. spizizenii had various types of cell walls. These tar and tag operons were mutually exclusive and the tar genes from B. s. spizizenii were very similar to the genes from non-Bacillus bacteria, unlike the tag genes from B. s. subtilis. The results and previous studies suggest that the tar genes and the tag genes are not inherited after subspecies speciation. The phylogenetic tree based on whole genome sequences showed that each subspecies clearly formed a monophyletic group, while the tree based on tar genes showed that monophyletic groups were formed according to the cell wall type rather than the subspecies. These findings indicate that the tar genes and the presence of ribitol as a cell-wall constituent were not the distinguishing difference between the subspecies of B. subtilis and that the description of subspecies B. s. spizizenii should be updated.

Keywords

References

  1. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, et al. 1997. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390: 249-256. https://doi.org/10.1038/36786
  2. Nazina TN, Tourova TP, Poltaraus AB, Novikova EV, Grigoryan AA, Ivanova AE, et al. 2001. Taxonomic study of aerobic thermophilic bacilli: descriptions of Geobacillus subterraneus gen. nov., sp. nov. and Geobacillus uzenensis sp. nov. from petroleum reservoirs and transfer of Bacillus stearothermophilus, Bacillus thermocatenulatus, Bacillus thermoleovorans, Bacillus kaustophilus, Bacillus thermoglucosidasius and Bacillus thermodenitrificans to Geobacillus as the new combinations G. stearothermophilus, G. thermocatenulatus, G. thermoleovorans, G. kaustophilus, G. thermoglucosidasius and G. thermodenitrificans. Int. J. Syst. Evol. Microbiol. 51: 433-446. https://doi.org/10.1099/00207713-51-2-433
  3. Porwal S, Lal S, Cheema S, Kalia VC. 2009. Phylogeny in aid of the present and novel microbial lineages: diversity in Bacillus. PLoS One 4: e4438. https://doi.org/10.1371/journal.pone.0004438
  4. Harwood CR. 1992. Bacillus subtilis and its relatives: molecular biological and industrial workhorses. Trends Biotechnol. 10: 247-256. https://doi.org/10.1016/0167-7799(92)90233-L
  5. Earl AM, Losick R, Kolter R. 2008. Ecology and genomics of Bacillus subtilis. Trends Microbiol. 16: 269-275. https://doi.org/10.1016/j.tim.2008.03.004
  6. Schallmey M, Singh A, Ward OP. 2004. Developments in the use of Bacillus species for industrial production. Can. J. Microbiol. 50: 1-17. https://doi.org/10.1139/w03-076
  7. Jin P, Zhang L, Yuan P, Kang Z, Du G, Chen J. 2016. Efficient biosynthesis of polysaccharides chondroitin and heparosan by metabolically engineered Bacillus subtilis. Carbohydr. Polym. 140: 424-432. https://doi.org/10.1016/j.carbpol.2015.12.065
  8. Deshmukh AN, Nipanikar-Gokhale P, Jain R. 2016. Engineering of Bacillus subtilis for the Production of 2,3-Butanediol from Sugarcane Molasses. Appl. Biochem. Biotechnol. 179: 321-331. https://doi.org/10.1007/s12010-016-1996-9
  9. Nakamura LK, Roberts MS, Cohan FM. 1999. Relationship of Bacillus subtilis clades associated with strains 168 and W23: a proposal for Bacillus subtilis subsp. subtilis subsp. nov. and Bacillus subtilis subsp. spizizenii subsp. nov. Int. J. Syst. Bacteriol. 49: 1211-1215. https://doi.org/10.1099/00207713-49-3-1211
  10. Rooney AP, Price NP, Ehrhardt C, Swezey JL, Bannan JD. 2009. Phylogeny and molecular taxonomy of the Bacillus subtilis species complex and description of Bacillus subtilis subsp. inaquosorum subsp. nov. Int. J. Syst. Evol. Microbiol. 59: 2429-2436. https://doi.org/10.1099/ijs.0.009126-0
  11. Swoboda JG, Campbell J, Meredith TC, Walker S. 2010. Wall teichoic acid function, biosynthesis, and inhibition. ChemBioChem. 11: 35-45.
  12. Brown S, Santa Maria JP Jr, Walker S. 2013. Wall teichoic acids of gram-positive bacteria. Annu. Rev. Microbiol. 67: 313-336. https://doi.org/10.1146/annurev-micro-092412-155620
  13. Lazarevic V, Abellan FX, Moller SB, Karamata D, Mauel C. 2002. Comparison of ribitol and glycerol teichoic acid genes in Bacillus subtilis W23 and 168: identical function, similar divergent organization, but different regulation. Microbiology 148: 815-824. https://doi.org/10.1099/00221287-148-3-815
  14. Mauel C, Young M, Karamata D. 1991. Genes concerned with synthesis of poly(glycerol phosphate), the essential teichoic acid in Bacillus subtilis strain 168, are organized in two divergent transcription units. J. Gen. Microbiol. 137: 929-941. https://doi.org/10.1099/00221287-137-4-929
  15. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. 2012. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19: 455-477. https://doi.org/10.1089/cmb.2012.0021
  16. Nawrocki EP, Eddy SR. 2013. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29: 2933-2935. https://doi.org/10.1093/bioinformatics/btt509
  17. Nawrocki EP, Burge SW, Bateman A, Daub J, Eberhardt RY, Eddy SR, et al. 2015. Rfam 12.0: updates to the RNA families database. Nucleic Acids Res. 43: D130-D137. https://doi.org/10.1093/nar/gku1063
  18. Edgar RC. 2007. PILER-CR: Fast and accurate identification of CRISPR repeats. BMC Bioinformatics 8: 18. https://doi.org/10.1186/1471-2105-8-18
  19. Bland C, Ramsey TL, Sabree F, Lowe M, Brown K, Kyrpides NC, et al. 2007. CRISPR Recognition Tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinformatics 8: 209. https://doi.org/10.1186/1471-2105-8-209
  20. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119. https://doi.org/10.1186/1471-2105-11-119
  21. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. 2014. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 42: D199-D205. https://doi.org/10.1093/nar/gkt1076
  22. Chen C, Huang H, Wu CH. 2017. Protein bioinformatics databases and resources. Methods Mol. Biol. 1558: 3-39.
  23. Powell S, Forslund K, Szklarczyk D, Trachana K, Roth A, Huerta-Cepas J, et al. 2014. eggNOG v4.0: nested orthology inference across 3686 organisms. Nucleic Acids Res. 42: D231-D239. https://doi.org/10.1093/nar/gkt1253
  24. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, et al. 2005. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 33: 5691-5702. https://doi.org/10.1093/nar/gki866
  25. Mistry J, Finn RD, Eddy SR, Bateman A, Punta M. 2013. Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res. 41: e121-e121. https://doi.org/10.1093/nar/gkt263
  26. Gibson MK, Forsberg KJ, Dantas G. 2015. Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology. ISME J. 9: 207-216. https://doi.org/10.1038/ismej.2014.106
  27. Caspi R, Billington R, Ferrer L, Foerster H, Fulcher CA, Keseler IM, et al. 2016. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 44: D471-480. https://doi.org/10.1093/nar/gkv1164
  28. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, et al. 2017. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int. J. Syst. Evol. Microbiol. 67: 1613-1617. https://doi.org/10.1099/ijsem.0.001755
  29. Zhu Q, Kosoy M, Dittmar K. 2014. HGTector: an automated method facilitating genome-wide discovery of putative horizontal gene transfers. BMC Genomics 15: 717. https://doi.org/10.1186/1471-2164-15-717
  30. Jolley KA, Maiden MC. 2010. BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11: 595. https://doi.org/10.1186/1471-2105-11-595
  31. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10: 421. https://doi.org/10.1186/1471-2105-10-421
  32. Maiden MCJ, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, et al. 1998. Multilocus sequence typing: A portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 95: 3140-3145. https://doi.org/10.1073/pnas.95.6.3140
  33. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792-1797. https://doi.org/10.1093/nar/gkh340
  34. Tamura K, Nei M, Kumar S. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. USA 101: 11030-11035. https://doi.org/10.1073/pnas.0404206101
  35. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
  36. Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870-1874. https://doi.org/10.1093/molbev/msw054
  37. Lee I, Kim YO, Park SC, Chun J. 2016. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int. J. Syst. Evol. Microbiol. 66: 1100-1103. https://doi.org/10.1099/ijsem.0.000760
  38. Kim S, Gong G, Woo HM, Kim Y, Um Y. 2016. Burkholderia jirisanensis sp. nov., isolated from forest soil. Int. J. Syst. Evol. Microbiol. 66: 1260-1267. https://doi.org/10.1099/ijsem.0.000867
  39. Yun SH, Lee SY, Choi CW, Lee H, Ro HJ, Jun S, et al. 2017. Proteomic characterization of the outer membrane vesicle of the halophilic marine bacterium Novosphingobium pentaromativorans US6-1. J. Microbiol. 55: 56-62. https://doi.org/10.1007/s12275-017-6581-6
  40. Garcia-Vallvé S, Romeu A, Palau J. 2000. Horizontal gene transfer in bacterial and archaeal complete genomes. Genome Res. 10: 1719-1725. https://doi.org/10.1101/gr.130000
  41. Zuniga M, Comas I, Linaje R, Monedero V, Yebra MJ, Esteban CD, et al. 2005. Horizontal gene transfer in the molecular evolution of mannose PTS transporters. Mol. Biol. Evol. 22: 1673-1685. https://doi.org/10.1093/molbev/msi163
  42. Comas I, Gonzalez-Candelas F, Zuniga M. 2008. Unraveling the evolutionary history of the phosphoryl-transfer chain of the phosphoenolpyruvate: phosphotransferase system through phylogenetic analyses and genome context. BMC Evol. Biol. 8: 147. https://doi.org/10.1186/1471-2148-8-147
  43. Young M, Mauel C, Margot P, Karamata D. 1989. Pseudo-allelic relationship between non-homologous genes concerned with biosynthesis of polyglycerol phosphate and polyglycerol phosphate teichoic acids in Bacillus subtilis strains 168 and W23. Mol. Microbiol. 3: 1805-1812. https://doi.org/10.1111/j.1365-2958.1989.tb00166.x
  44. Yi H, Chun J, Cha CJ. 2014. Genomic insights into the taxonomic status of the three subspecies of Bacillus subtilis. Syst. Appl. Microbiol. 37: 95-99. https://doi.org/10.1016/j.syapm.2013.09.006
  45. Halling SM, Burtis K, Doi R. 1977. Reconstitution studies show that rifampicin resistance is determined by the largest polypeptide of Bacillus subtilis RNA polymerase. J. Biol. Chem. 252: 9024-9031.
  46. Goldstein BP. 2014. Resistance to rifampicin: a review. J. Antibiot. 67: 625. https://doi.org/10.1038/ja.2014.107
  47. Sigle S, Steblau N, Wohlleben W, Muth G. 2016. Polydiglycosylphosphate transferase PdtA (SCO2578) of Streptomyces coelicolor A3 (2) is crucial for proper sporulation and apical tip extension under stress conditions. Appl. Environ. Microbiol. 82: 5661-5672. https://doi.org/10.1128/AEM.01425-16
  48. Sharma D, Cukras AR, Rogers EJ, Southworth DR, Green R. 2007. Mutational analysis of S12 protein and implications for the accuracy of decoding by the ribosome. J. Mol. Biol. 374: 1065-1076. https://doi.org/10.1016/j.jmb.2007.10.003
  49. Nguyen-Distèche M, Leyh-Bouille M, Ghuysen J-M. 1982. Isolation of the membrane-bound 26 000-Mr penicillin-binding protein of Streptomyces strain K15 in the form of a penicillin-sensitive D-alanyl-D-alanine-cleaving transpeptidase. Biochem. J. 207: 109-115. https://doi.org/10.1042/bj2070109
  50. Gordon E, Mouz N, Duee E, Dideberg O. 2000. The crystal structure of the penicillin-binding protein 2x from Streptococcus pneumoniae and its acyl-enzyme form: implication in drug resistance. J. Mol. Biol. 299: 477-485. https://doi.org/10.1006/jmbi.2000.3740
  51. Lowy FD. 2003. Antimicrobial resistance: the example of Staphylococcus aureus. J. Clin. Invest. 111: 1265-1273. https://doi.org/10.1172/JCI18535
  52. Drawz SM, Bonomo RA. 2010. Three decades of $\beta$-lactamase inhibitors. Clin. Microbiol. Rev. 23: 160-201. https://doi.org/10.1128/CMR.00037-09
  53. Farha MA, Leung A, Sewell EW, D'Elia MA, Allison SE, Ejim L, et al. 2012. Inhibition of WTA synthesis blocks the cooperative action of PBPs and sensitizes MRSA to $\beta$-lactams. ACS Chem. Biol. 8: 226-233.
  54. Roberts MC. 2005. Update on acquired tetracycline resistance genes. FEMS Microbiol. Lett. 245: 195-203. https://doi.org/10.1016/j.femsle.2005.02.034
  55. Bhavsar AP, Beveridge TJ, Brown ED. 2001. Precise deletion of tagD and controlled depletion of its product, glycerol 3-phosphate cytidylyltransferase, leads to irregular morphology and lysis of Bacillus subtilis grown at physiological temperature. J. Bacteriol. 183: 6688-6693. https://doi.org/10.1128/JB.183.22.6688-6693.2001
  56. D'Elia MA, Millar KE, Beveridge TJ, Brown ED. 2006. Wall teichoic acid polymers are dispensable for cell viability in Bacillus subtilis. J. Bacteriol. 188: 8313-8316. https://doi.org/10.1128/JB.01336-06

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