Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Deficiency in Opu Systems Imparts Salt-Sensitivity to Weizmannia coagulans

  • Tao Kim (Department of Food and Nutrition, Dongduk Women's University) ;
  • Sojeong Heo (Department of Food and Nutrition, Dongduk Women's University) ;
  • Jong-Hoon Lee (Department of Food Science and Biotechnology, Kyonggi University) ;
  • Do-Won Jeong (Department of Food and Nutrition, Dongduk Women's University)
  • Received : 2024.04.09
  • Accepted : 2024.05.20
  • Published : 2024.07.28
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Abstract

Weizmannia coagulans can be used as a starter strain in fermented foods or as a probiotic. However, it is salt-sensitive. Here, W. coagulans genomes were compared with the genomes of strains of Bacillus species (B. licheniformis, B. siamensis, B. subtilis, and B. velezensis) that were isolated from fermented foods and show salt tolerance, to identify the basis for the salt-sensitivity of W. coagulans. Osmoprotectant uptake (Opu) systems transport compatible solutes into cells to help them tolerate osmotic stress. B. siamensis, B. subtilis, and B. velezensis each possess five Opu systems (OpuA, OpuB, OpuC, OpuD, and OpuE); B. licheniformis has all except OpuB. However, W. coagulans only has the OpuC system. Based on these findings, the opuA and opuB operons, and the opuD and opuE genes, were amplified from B. velezensis. Expression of each of these systems, respectively, in W. coagulans increased salt-tolerance. W. coagulans expressing B. velezensis opuA, opuD, or opuE grew in 10.5% NaCl (w/v), whereas wild-type W. coagulans could not grow in 3.5% NaCl. The salt resistance of B. subtilis was also increased by overexpression of B. velezensis opuA, opuB, opuD, or opuE. These results indicate that the salt-susceptibility of W. coagulans arises because it is deficient in Opu systems.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) [NRF-2022M3A9I3082364].

References

  1. Hammer BW. 1915. Bacteriological studies on the coagulation of evaporated milk (Vol. 17). Agricultural Experiment Station, Iowa State College of Agriculture and Mechanic Arts. 
  2. Gupta RS, Patel S, Saini N, Chen S. 2020. Robust demarcation of 17 distinct Bacillus species clades, proposed as novel Bacillaceae genera, by phylogenomics and comparative genomic analyses: description of Robertmurraya kyonggiensis sp. nov. and proposal for an emended genus Bacillus limiting it only to the members of the Subtilis and Cereus clades of species. Int. J. Syst. Evol. Microbiol. 70: 5753-5798. 
  3. Konuray G, Erginkaya Z. 2018. Potential use of Bacillus coagulans in the food industry. Foods 7: 92. 
  4. Jager R, Shields KA, Lowery RP, De Souza EO, Partl JM, Hollmer C, et al. 2016. Probiotic Bacillus coagulans GBI-30, 6086 reduces exercise-induced muscle damage and increases recovery. Peer J. 4: e2276. 
  5. Majeed M, Majeed S, Nagabhushanam K, Natarajan S, Sivakumar A, Ali F. 2016. Evaluation of the stability of Bacillus coagulans MTCC 5856 during processing and storage of functional foods. Int. J. Food Sci. Technol. 51: 894-901. 
  6. Ratna Sudha, M Yelikar, KA, Deshpande S. 2012. Clinical study of Bacillus coagulans unique IS-2 (ATCC PTA-11748) in the treatment of patients with bacterial vaginosis. Indian J. Microbiol. 52: 396-399. 
  7. Elshaghabee FMF, Rokana N, Gulhane RD, Sharma C, Panwar H. 2017. Bacillus as potential probiotics: status, concerns, and future perspectives. Front. Microbiol. 8: 1490. 
  8. Maity C, Gupta AK, Saroj DB, Biyani A, Bagkar P, Kulkarni J, et al. 2021. Impact of a gastrointestinal stable probiotic supplement Bacillus coagulans LBSC on human gut microbiome modulation. J. Diet. Suppl. 18: 577-596. 
  9. Bang WY, Ban OH, Lee BS, Oh S, Park C, Park MK, et al. 2021. Genomic-, phenotypic-, and toxicity-based safety assessment and probiotic potency of Bacillus coagulans IDCC 1201 isolated from green malt. J. Ind. Microbiol. Biotechnol. 48: kuab026.
  10. Lee B, Lee H, Jeong DW, Lee JH. 2015. A rapid isolation method for Bacillus coagulans from rice straw. Microbiol. Biotechnol. Lett. 43: 401-404. 
  11. Shudong P, Guo C, Wu S, Cui H, Suo H, Duan Z. 2022. Bioactivity and metabolomics changes of plant-based drink fermented by Bacillus coagulans VHProbi C08. LWT - Food Sci. Technol. 153: 113030. 
  12. Babu KR, Satyanarayana T. 1995. α-Amylase production by thermophilic Bacillus coagulans in solid state fermentation. Process Biochem. 30: 305-309. 
  13. Olajuyigbe FM, Ehiosun KI. 2013. Production of thermostable and organic solvent-tolerant alkaline protease from Bacillus coagulans PSB-07 under different submerged fermentation conditions. Afr. J. Biotechnol. 12: 3341-3350. 
  14. Le Marrec C, Hyronimus B, Bressollier P, Verneuil B, Urdaci MC. 2000. Biochemical and genetic characterization of coagulin, a new antilisterial bacteriocin in the pediocin family of bacteriocins, produced by Bacillus coagulans I4. Appl. Environ. Microbiol. 66: 5213-5220. 
  15. EFSA. 2007. Introduction of a qualified presumption of safety (QPS) approach for assessment of selected microorganisms referred to EFSA. EFSA J. 587: 1-16. 
  16. Heo S, Kim T, Na HE, Lee G, Park JH, Park HJ, et al. Safety assessment systems for microbial starters derived from fermented foods. J. Microbiol. Biotechnol. 32: 1227-1233. 
  17. Kim YS, Lee J, Heo S, Lee JH, Jeong DW. 2021. Technology and safety evaluation of Bacillus coagulans exhibiting antimicrobial activity for starter development. LWT - Food Sci. Technol. 137: 110464. 
  18. Jeong DW, Lee B, Lee J H. 2018. Complete genome sequence of Bacillus licheniformis 14ADL4 exhibiting resistance to clindamycin. Korean J. Microbiol. 54: 169-170. 
  19. Heo S, Kim JH, Kwak MS, Jeong DW, Sung MH. 2021. Functional genomic insights into probiotic Bacillus siamensis strain B28 from traditional Korean fermented kimchi. Foods 10: 1906. 
  20. Lee MH, Song JJ, Choi YH, Hong SP, Rha E, Kim HK, et al. 2003. High-level expression and secretion of Bacillus pumilus lipase B26 in Bacillus subtilis Chungkookjang. J. Microbiol. Biotechnol. 13: 892-896. 
  21. Ji Y, Marra A, Rosenberg M, Woodnutt G. 1999. Regulated antisense RNA eliminates alpha-toxin virulence in Staphylococcus aureus infection. J. Bacteriol. 181: 6585-6590. 
  22. Johnson SL, Bishop-Lilly KA, Ladner JT, Daligault HE, Davenport KW, Jaissle J, et al. 2015. Complete genome sequences for 59 Burkholderia isolates, both pathogenic and near neighbor. Genome Announc. 3. e00159-15. 
  23. Lee J, Heo S, Kim Y S, Lee JH, Jeong DW. 2020. Complete genome sequence of Bacillus coagulans strain ASRS217, a potential food fermentation starter culture. Korean J. Microbiol. 56: 321-323. 
  24. Yao G, Gao P, Zhang W. 2016. Complete genome sequence of probiotic Bacillus coagulans HM-08: a potential lactic acid producer. J. Biotechnol. 228: 71-72. 
  25. Maas RH, Bakker RR, Jansen ML, Visser D, Jong E, Eggink G, et al. 2008. Lactic acid production from lime-treated wheat straw by Bacillus coagulans: neutralization of acid by fed-batch addition of alkaline substrate. Appl. Microbiol. Biotechnol. 78: 751-758. 
  26. Rey MW, Ramaiya P, Nelson BA, Brody-Karpin SD, Zaretsky EJ, Tang M, et al. 2004. Complete genome sequence of the industrial bacterium Bacillus licheniformis and comparisons with closely related Bacillus species. Genome Biol. 5: R77. 
  27. Jeong DW, Lee B, Heo S, Jang M, Lee JH. 2018. Complete genome sequence of Bacillus licheniformis strain 0DA23-1, a potential starter culture candidate for soybean fermentation. Korean J. Microbiol. 54: 453-455. 
  28. Rohith HS, Halami PM. 2021. The combined effect of potential probiotic Bacillus licheniformis MCC 2514 and Bifidobacterium breve NCIM 5671 towards anti-inflammatory activity on HT-29 cell lines. Probiotics Antimicrob. Proteins 15: 351-362. 
  29. Yuan F, Li K, Zhou C, Zhou H, Liu H, Chai H, et al. 2020. Identification of two novel highly inducible promoters from Bacillus licheniformis by screening transcriptomic data. Genom 112: 1866-1871. 
  30. Jeong H, Jeong DE, Kim SH, Song GC, Park SY, Ryu CM, et al. 2012. Draft genome sequence of the plant growth-promoting bacterium Bacillus siamensis KCTC 13613T. J. Bacteriol. 194: 4148-4149. 
  31. Pan H, Tian X, Shao M, Xie Y, Huang H, Hu J et al. 2019. Genome mining and metabolic profiling illuminate the chemistry driving diverse biological activities of Bacillus siamensis SCSIO 05746. Appl. Microbiol. Biotechnol. 103: 4153-4165. 
  32. Nye TM, Schroeder JW, Kearns DB, Simmons LA. 2017. Complete genome sequence of undomesticated Bacillus subtilis strain NCIB 3610. Genome Announc. 5: e00364-17. 
  33. Iqbal S, Ullah N, Janjua HA. 2021. In vitro evaluation and genome mining of Bacillus subtilis strain RS10 reveals its biocontrol and plant growth-promoting potential. Agriculture 11: 1273. 
  34. Grela A, Jamrozek I, Hubisz M, Iwanicki A, Hinc K, Kazmierkiewicz R, et al. 2018. Positions 299 and 302 of the GerAA subunit are important for function of the GerA spore germination receptor in Bacillus subtilis. PLoS One 13: e0198561. 
  35. Heo J, Kim JS, Hong SB, Park BY, Kim SJ, Kwon SW. 2019. Genetic marker gene, recQ, differentiating Bacillus subtilis and the closely related Bacillus species. FEMS Microbiol. Lett. 366: fnz172. 
  36. Dunlap CA, Kim SJ, Kwon SW, Rooney AP. 2016. Bacillus velezensis is not a later heterotypic synonym of Bacillus amyloliquefaciens; Bacillus methylotrophicus, Bacillus amyloliquefaciens subsp. plantarum and 'Bacillus oryzicola' are laterheterotypic synonyms of Bacillus velezensis based on phylogenomics. Int. J. Syst. Evol. Microbiol. 66: 1212-1217. 
  37. Na HE, Heo S, Kim T, Lee G, Lee JH, Jeong DW. 2023. ComQXPA quorum-sensing systems contribute to enhancing the protease activity of Bacillus velezensis DMB05 from fermented soybeans. Int. J. Food Microbiol. 401: 110294. 
  38. Na HE, Heo S, Kim YS, Kim T, Lee G, Lee JH, et al. 2022. The safety and technological properties of Bacillus velezensis DMB06 used as a starter candidate were evaluated by genome analysis. LWT - Food Sci. Technol. 161: 113398. 
  39. Heo S, Kim JH, Kwak MS, Sung MH, Jeong DW. 2021. Functional annotation genome unravels potential probiotic Bacillus velezensis strain KMU01 from traditional Korean fermented kimchi. Foods 10: 563. 
  40. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genom. 9: 75. 
  41. Darzi Y, Letunic I, Bork P, Yamada T. 2018. iPath3.0: interactive pathways explorer v3. Nucleic Acids Res. 46: W510-W513. 
  42. Abbas BA, Khudor MH, Saeed BMS. 2014. Detection of hbl, nhe and bceT toxin genes in Bacillus cereus isolates by multiplex PCR. Int. J. Curr. Microbiol. Appl. Sci. 3: 1009-1016. 
  43. Hanahan D, Meselson M. 1983. Plasmid screening at high colony density. Methods Enzymol. 100: 333-342. 
  44. Kraemer GR, Iandolo JJ. 1990. High-frequency transformation of Staphylococcus aureus by electroporation. Curr. Microbiol. 21: 373-376. 
  45. Jeong DW, Kim HR, Jung G, Han S, Kim CT, Lee JH. 2014. Bacterial community migration in the ripening of doenjang, a traditional Korean fermented soybean food. J. Microbiol. Biotechnol. 24: 648-660. 
  46. Jeong DW, Jeong M, Lee JH. 2017. Antibiotic susceptibilities and characteristics of Bacillus licheniformis isolates from traditional Korean fermented soybean foods. LWT - Food Sci. Technol. 75: 565-568. 
  47. Kim T, Heo S, Na HE, Lee G, Kim JH, Kwak MS, et al. 2022. Bacterial community of galchi-baechu kimchi based on culture-dependent and -independent investigation and selection of starter candidates. J. Microbiol. Biotechnol. 32: 341-347. 
  48. Kim YS, Kim MC, Kwon SW, Kim SJ, Park IC, Ka JO, et al. 2011. Analyses of bacterial communities in meju, a Korean traditional fermented soybean bricks, by cultivation-based and pyrosequencing methods. J. Microbiol. Biotechnol. 49: 340-348.
  49. Jeon HH, Jung JY, Chun BH, Kim MD, Baek SY, Moon JY, et al. 2016. Screening and characterization of potential Bacillus starter cultures for fermenting low-salt soybean paste (Doenjang). J. Microbiol. Biotechnol. 26: 666-674. 
  50. Lee MY, Park SY, Jung KO, Park KY, Kim SD. 2005. Quality and functional characteristics of chungkukjang prepared with various Bacillus sp. isolated from traditional chungkukjang. J. Food Sci. 70: M191-M196. 
  51. Hoffmann T, Bremer E. 2017. Guardians in a stressful world: the Opu family of compatible solute transporters from Bacillus subtilis. Biol. Chem. 398: 193-214. 
  52. Heo S, Lee J, Lee JH, Jeong DW. 2019. Genomic insight into the salt tolerance of Enterococcus faecium, Enterococcus faecalis and Tetragenococcus halophilus. J. Microbiol. Biotechnol. 29: 151-1602. 
  53. Peterbauer C, Maischberger T, Haltrich D. 2011. Food-grade gene expression in lactic acid bacteria. Biotechnol. J. 6: 1147-1161. 
  54. Wang L, Xue Z, Zhao B, Yu B, Xu P, Ma Y. 2013. Jerusalem artichoke powder: a useful material in producing high-optical-purity L-lactate using an efficient sugar-utilizing thermophilic Bacillus coagulans strain. Bioresour. Technol. 130: 174-180. 
  55. Xing SC, Chen JY, Lv N, Mi JD, Chen WL, Liang JB, et al. 2018. Biosorption of lead (Pb2+) by the vegetative and decay cells and spores of Bacillus coagulans R11 isolated from lead mine soil. Chemosphere 211: 804-816.