Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Genomic Insight into the Salt Tolerance of Enterococcus faecium, Enterococcus faecalis and Tetragenococcus halophilus

  • Heo, Sojeong (Department of Food and Nutrition, Dongduk Women's University) ;
  • Lee, Jungmin (Department of Food and Nutrition, Dongduk Women's University) ;
  • Lee, Jong-Hoon (Department of Food Science and Biotechnology, Kyonggi University) ;
  • Jeong, Do-Won (Department of Food and Nutrition, Dongduk Women's University)
  • Received : 2019.08.07
  • Accepted : 2019.09.02
  • Published : 2019.10.28
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Abstract

To shed light on the genetic basis of salt tolerance in Enterococcus faecium, Enterococcus faecalis, and Tetragenococcus halophilus, we performed comparative genome analysis of 10 E. faecalis, 11 E. faecium, and three T. halophilus strains. Factors involved in salt tolerance that could be used to distinguish the species were identified. Overall, T. halophilus contained a greater number of potassium transport and osmoprotectant synthesis genes compared with the other two species. In particular, our findings suggested that T. halophilus may be the only one among the three species capable of synthesizing glycine betaine from choline, cardiolipin from glycerol and proline from citrate. These molecules are well-known osmoprotectants; thus, we propose that these genes confer the salt tolerance of T. halophilus.

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References

  1. Lee SS. 1995. Meju fermentation for a raw material of Korean traditional soy products. Kor. J. Mycol. 23: 161-175.
  2. Yoo JY, Kim, HG. 1998. Characteristics of traditional mejus of nation-wide collection. J. Korean Soc. Food Sci. Nutr. 27: 259-267.
  3. Shukla S, Lee JS, Park HK, Yoo JA, Hong SY, Kim JK, et al. 2015. Effect of novel starter culture on reduction of biogenic amines, quality improvement, and sensory properties of doenjang, a traditional Korean soybean fermented sauce variety. J. Food Sci. 80: M1794-1803. https://doi.org/10.1111/1750-3841.12942
  4. Kum SJ, Yang SO, Lee SM, Chang PS, Choi YH, Lee JJ, et al. 2015. Effects of Aspergillus species inoculation and their enzymatic activities on the formation of volatile components in fermented soybean paste (doenjang). J. Agric. Food Chem. 63: 1401-1418. https://doi.org/10.1021/jf5056002
  5. Kim J-W, Doo H-S, Kwon T-H, Kim Y-S, Shin D-H. 2011. Quality characteristics of doenjang meju fermented with Aspergillus species and Bacillus subtilis during fermentation. Korean J. Food Preserv. 18: 397-406. https://doi.org/10.11002/kjfp.2011.18.3.397
  6. Jeong DW, Heo S, Lee B, Lee H, Jeong K, Her JY, et al. 2017. Effects of the predominant bacteria from meju and doenjang on the production of volatile compounds during soybean fermentation. Int. J. Food Microbiol. 262: 8-13. https://doi.org/10.1016/j.ijfoodmicro.2017.09.011
  7. Jeong DW, Lee H, Jeong K, Kim CT, Shim ST, Lee JH. 2019. Effect of starter candidates and NaCl on the production of volatile compounds during soybean fermentation. J. Microbiol. Biotechnol. 29: 191-199. https://doi.org/10.4014/jmb.1811.11012
  8. Cho DH, Lee, WJ. 1970. Microbial studies of Korean native soy-sauce fermentation: a study on the microflora of fermented Korean maeju loaves. J. Korean Agric. Chem. Soc. 13: 35-42.
  9. Kim KM, Lim J, Lee JJ, Hurh BS, Lee I. 2017. Characterization of Aspergillus sojae isolated from Meju, Korean traditional fermented soybean brick. J. Microbiol. Biotechnol. 27: 251-261. https://doi.org/10.4014/jmb.1610.10013
  10. Lee WJ, Cho, DH. 1971. Microbial studies of Korean native soy-sauce fermentation: a study on the microflora changes during Korean native soy-sauce fermentation. J. Korean Agric. Chem. Soc. 14: 137-148.
  11. Kim YS, Jeong, DY, Hwang YT, Uhm T-B. 2011. Bacterial community profiling during the manufacturing process of traditional soybean paste by pyrosequencing method. Korean J. Microbiol. 47: 275-280.
  12. Cho KM, Seo, WT. 2007. Bacterial diversity in Korean traditional soybean fermented foods (doenjang and ganjang) by 16S rRNA gene sequence analysis. Food Sci. Biotechnol. 16: 320-324.
  13. Kim TW, Lee JH, Kim SE, Park MH, Chang HC, Kim HY. 2009. Analysis of microbial communities in doenjang, a Korean fermented soybean paste, using nested PCR-denaturing gradient gel electrophoresis. Int. J. Food Microbiol. 131: 2 65-271. https://doi.org/10.1016/j.ijfoodmicro.2009.03.001
  14. 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. 49: 340-348. https://doi.org/10.1007/s12275-011-0302-3
  15. Lee JH, Kim TW, Lee H, Chang HC, Kim HY. 2010. Determination of microbial diversity in meju, fermented cooked soya beans, using nested PCR-denaturing gradient gel electrophoresis. Lett. Appl. Microbiol. 51: 388-394. https://doi.org/10.1111/j.1472-765X.2010.02906.x
  16. Lee J H, S hin D, Lee B, L ee H , Lee I, Jeong D W. 2017. Genetic diversity and antibiotic resistance of Enterococcus faecalis isolates from traditional Korean fermented soybean foods. J. Microbiol. Biotechnol. 27: 916-924. https://doi.org/10.4014/jmb.1612.12033
  17. Euzeby JP. 2011. Efinitaions and abbreviations. in: List of Bacteria Names with Standing in Nomenclature. (ed.) J.P. Euzeby.
  18. Gardiner GE, Ross RP, Wallace JM, Scanlan FP, Jagers PP, Fitzgerald GF, et al. 1999. Influence of a probiotic adjunct culture of Enterococcus faecium on the quality of cheddar cheese. J. Agric. Food Chem. 47: 4907-4916. https://doi.org/10.1021/jf990277m
  19. Bhardwaj A, Malik RK, Chauhan P. 2008. Functional and safety aspects of enterococci in dairy foods. Indian J. Microbiol. 48: 317-325. https://doi.org/10.1007/s12088-008-0041-2
  20. Santos MM, Piccirillo C, Castro PM, Kalogerakis N, Pintado ME. 2012. Bioconversion of oleuropein to hydroxytyrosol by lactic acid bacteria. World J. Microbiol. Biotechnol. 28: 2435-2440. https://doi.org/10.1007/s11274-012-1036-z
  21. Hanagata H, Shida O, Takagi H. 2003. Taxonomic homogeneity of a salt-tolerant lactic acid bacteria isolated from shoyu mash. J. Gen. Appl. Microbiol. 49: 95-100. https://doi.org/10.2323/jgam.49.95
  22. Bergey DH. 2009. Bergey's Manual of Systematic Bacteriology, pp. 594-623 Ed. Springer-Verlag New York.
  23. 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. https://doi.org/10.4014/jmb.1401.01009
  24. Jeong MR, Jeong DW, Lee JH. 2015. Safety and biotechnological properties of Enterococcus faecalis and Enterococcus faecium isolates from Meju. J. Korean Soc. Appl. Biol. Chem. 58: 813-820. https://doi.org/10.1007/s13765-015-0110-2
  25. Jeong DW, Heo S, Lee JH. 2017. Safety assessment of Tetragenococcus halophilus isolates from doenjang, a Korean high-salt-fermented soybean paste. Food Microbiol. 62: 92-98. https://doi.org/10.1016/j.fm.2016.10.012
  26. Lee JH, Heo S, Jeong K, Lee B, Jeong DW. 2018. Genomic insights into the non-histamine production and proteolytic and lipolytic activities of Tetragenococcus halophilus KUD2 3. FEMS Microbiol. Lett. 365: fnx252.
  27. Facklam RR, Carvalho MG, Teixeira LM. 2002. Enterococcus, pp. 1-54. In Gilmore MS, Clewel DB, Courvalin P, Dunny GM, Murray BE, Rice LB (ed.), The Enterococci: Pathogenesis, Molecular Biology, and Antibiotic Resistance Ed. ASM Press, Washington, DC
  28. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM. 2007. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int. J. Syst. Evol. Microbiol. 57: 81-91. https://doi.org/10.1099/ijs.0.64483-0
  29. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9: 75. https://doi.org/10.1186/1471-2164-9-75
  30. Blom J, Albaum SP, Doppmeier D, Puhler A, Vorholter FJ, Zakrzewski M, et al. 2009. EDGAR: a software framework for the comparative analysis of prokaryotic genomes. BMC Bioinformatics 10: 154. https://doi.org/10.1186/1471-2105-10-154
  31. Wood JM, Bremer E, Csonka LN, Kraemer R, Poolman B, van der Heide T, et al. 2001. Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 130: 437-460. https://doi.org/10.1016/S1095-6433(01)00442-1
  32. Epstein W. 2003. The roles and regulation of potassium in bacteria. Prog. Nucleic Acid Res. Mol. Biol. 75: 293-320. https://doi.org/10.1016/S0079-6603(03)75008-9
  33. Kraegeloh A, Amendt B, Kunte HJ. 2005. Potassium transport in a halophilic member of the bacteria domain: identification and characterization of the K+ uptake systems TrkH and TrkI from Halomonas elongata DSM 2 581T. J. Bacteriol. 187: 1036-1043. https://doi.org/10.1128/JB.187.3.1036-1043.2005
  34. Roberts MF. 2005. Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Systems. 1: 5. https://doi.org/10.1186/1746-1448-1-5
  35. Whatmore AM, Chudek JA, Reed RH. 1990. The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis. J. Gen. Microbiol. 136: 2527-2535. https://doi.org/10.1099/00221287-136-12-2527
  36. Holtmann G, Bakker EP, Uozumi N, Bremer E. 2003. KtrAB and KtrCD: two K+ uptake systems in Bacillus subtilis and their role in adaptation to hypertonicity. J. Bacteriol. 185: 1289-1298. https://doi.org/10.1128/JB.185.4.1289-1298.2003
  37. Schwan WR, Wetzel KJ. 2016. Osmolyte transport in Staphylococcus aureus and the role in pathogenesis. World J. Clin. Infect. Dis. 6: 22-27. https://doi.org/10.5495/wjcid.v6.i2.22
  38. 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. https://doi.org/10.1515/hsz-2016-0265
  39. Chun BH, Han DM, Kim KH, Jeong SE, Park D, Jeon CO. 2019. Genomic and metabolic features of Tetragenococcus halophilus as revealed by pan-genome and transcriptome analyses. Food Microbiol. 83: 36-47. https://doi.org/10.1016/j.fm.2019.04.009
  40. Lin J, Zhu Y, Tang H, Yan J, Luo L. 2019. Identification of a GntR family regulator BusRTha and its regulatory mechanism in the glycine betaine ABC transport system of Tetragenococcus halophilus. Extremophiles 23: 451-460. https://doi.org/10.1007/s00792-019-01096-6
  41. Boch J, Kempf B, Schmid R, Bremer E. 1996. Synthesis of the osmoprotectant glycine betaine in Bacillus subtilis: characterization of the gbsAB genes. J. Bacteriol. 178: 5121-5129. https://doi.org/10.1128/jb.178.17.5121-5129.1996
  42. Romantsov T, Guan Z, Wood JM. 2009. Cardiolipin and the osmotic stress responses of bacteria. Biochim. Biophys. Acta 1788: 2092-2100. https://doi.org/10.1016/j.bbamem.2009.06.010
  43. Kanemasa Y, Yoshioka T, Hayashi H. 1972. Alteration of the phospholipid composition of Staphylococcus aureus cultured in medium containing NaCl. Biochim. Biophys. Acta 280: 444-450. https://doi.org/10.1016/0005-2760(72)90251-2
  44. Tsai M, Ohniwa RL, Kato Y, Takeshita SL, Ohta T, Saito S, et al. 2 011. Staphylococcus aureus requires cardiolipin for survival under conditions of high salinity. BMC Microbiol. 11: 13. https://doi.org/10.1186/1471-2180-11-13
  45. Jeong DW, Heo S, Ryu S, Blom J, Lee JH. 2017. Genomic insights into the virulence and salt tolerance of Staphylococcus equorum. Sci. Rep. 7: 5383. https://doi.org/10.1038/s41598-017-05918-5
  46. He G, Wu C, Huang J, Zhou R. 2017. Effect of exogenous proline on metabolic response of Tetragenococcus halophilus under salt stress. J. Microbiol. Biotechnol. 27: 1682-1691.

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