Environmental Stress Responses of Lactic Acid Bacteria

  • Wei ChenEmail author
  • Wenwei Lu


Lactic acid bacteria (LAB) are often used to produce fermented foods. LAB usually grow in “moderate” environmental conditions and commonly encounter stress conditions like changes in pH, temperature, production, storage, and others (Kim NR, Jeong DW, Ko DS, Shim JH, Intl J Biol Macromol 99:594–599., 1997). These condition changes may lead to poor growth rate or even survival of the bacteria. Stress responses were of great importance for microorganism; they always continually change with temperature and osmotic pressure in the environments (Becker MR, Paster BJ, Leys EJ, Moeschberger ML, Kenyon SG, Galvin JL, Boches SK, Dewhirst FE, Griffen AL, J Clin Microbiol 40(3):1001–1009., 2002). There are various kinds of stress factors, which include physical, chemical, or biological and others. LABs are exposed to these stresses during fermentation, for example, low temperature, high H2O2, and low pH (Kurz M, Saline Syst 4:6., 2008; Burokas A, Arboleya S, Moloney RD, Peterson VL, Murphy K, Clarke G, Stanton C, Dinan TG, Cryan JF, Biol Psychiat 82:472., 2017; Becker MR, Paster BJ, Leys EJ, Moeschberger ML, Kenyon SG, Galvin JL, Boches SK, Dewhirst FE, Griffen AL, J Clin Microbiol 40(3):1001–1009., 2002). LABs have the stress-sensing systems to activate defenses, permitting the bacteria to acclimatize the harsh conditions or environmental changes. In LAB, DNA-repairing mechanisms can be also characterized as responding to oxidative stress and acid stress.


Acid Stress Bile Stress Osmotic Stress Oxidative Stress Cold Stress 


  1. Ahn, Y.T., G.B. Kim, K.S. Lim, Y.J. Baek, and H.U. Kim. 2003. Deconjugation of bile salts by Lactobacillus acidophilus isolates. International Dairy Journal 13 (4): 303–311.CrossRefGoogle Scholar
  2. Ai, Lianzhong, Hao Zhang, Benheng Guo, Wei Chen, Zhengjun Wu, and Wu. Yan. 2008. Preparation, partial characterization and bioactivity of exopolysaccharides from Lactobacillus casei LC2W. Carbohydrate Polymers 74 (3): 353–357.CrossRefGoogle Scholar
  3. Allain, T., S. Chaouch, M. Thomas, I. Vallée, A.G. Buret, P. Langella, P. Grellier, B. Polack, L.G. Bermúdez-Humarán, and I. Florent. 2017. Bile-salt-hydrolases from the probiotic strain Lactobacillus johnsoniiLa1 mediate anti-giardial activityin vitroandin vivo. Frontiers in Microbiology 8: 2707.PubMedCrossRefGoogle Scholar
  4. Axel, C., E. Zannini, A. Coffey, et al. 2012. Ecofriendly control of potato late blight causative agent and the potential role of lactic acid bacteria: A review. Applied Microbiology & Biotechnology 96 (1): 37–48.CrossRefGoogle Scholar
  5. Ayres, J.S. 2016. Cooperative microbial tolerance behaviors in host-microbiota mutualism. Cell 165 (6): 1323–1331. Scholar
  6. Bandyopadhyay, A., and S.P. Moulik. 1988. Interaction of bile salts with a nonionic surfactant and their activation energy for conduction as well as calcium and barium ion tolerance in presence of the nonionic surfactant. Indian Journal of Biochemistry & Biophysics 25 (3): 287.Google Scholar
  7. Beal, C., F. Fonseca, and G. Corrieu. 2001. Resistance to freezing and frozen storage of Streptococcus thermophilus is related to membrane fatty acid composition. Journal of Dairy Science 84 (11): 2347–2356.PubMedCrossRefGoogle Scholar
  8. Beales, N. 2004. Adaptation of microorganisms to cold temperatures, weak acid preservatives, low ph, and osmotic stress: A review. Comprehensive Reviews in Food Science & Food Safety 3 (1): 1–20.CrossRefGoogle Scholar
  9. Beaufils, Sophie, Nicolas Sauvageot, Alain Mazé, Jean Marie Laplace, Yanick Auffray, Josef Deutscher, and Axel Hartke. 2007. The cold shock response of Lactobacillus casei: Relation between HPr phosphorylation and resistance to freeze/thaw cycles. Journal of Molecular Microbiology & Biotechnology 13 (1–3): 65–75.CrossRefGoogle Scholar
  10. Becker, M.R., B.J. Paster, E.J. Leys, M.L. Moeschberger, S.G. Kenyon, J.L. Galvin, S.K. Boches, F.E. Dewhirst, and A.L. Griffen. 2002. Molecular analysis of bacterial species associated with childhood caries. Journal of Clinical Microbiology 40 (3): 1001–1009. Scholar
  11. Begley, M., C.G. Gahan, and C. Hill. 2005. The interaction between bacteria and bile. Fems Microbiology Reviews 29 (4): 625–651.PubMedCrossRefGoogle Scholar
  12. Bender, G.R., S.V. Sutton, and R.E. Marquis. 1986. Acid tolerance, proton permeabilities, and membrane ATPases of oral streptococci. Infection & Immunity 53 (2): 331.Google Scholar
  13. Bermúdezhumarán, L.G., N.G. Cortesperez, S. Ahleung, F. Lefèvre, G. Yang, Q. Pang, C. Wu, Y. Zeng, K. Adelpatient, and P. Langella. 2008. Current prophylactic and therapeutic uses of a recombinant Lactococcus lactis strain secreting biologically active interleukin-12. Journal of Molecular Microbiology & Biotechnology 14 (1–3): 80–89.CrossRefGoogle Scholar
  14. Biswas, Indranil, Laura Drake, Dasha Erkina, and Saswati Biswas. 2008. Involvement of sensor kinases in the stress tolerance response of Streptococcus mutans. Journal of Bacteriology 190 (1): 68.PubMedCrossRefGoogle Scholar
  15. Boels, I.C., M. Kleerebezem, and W.M. de Vos. 2003. Engineering of carbon distribution between glycolysis and sugar nucleotide biosynthesis in Lactococcus lactis. Applied and Environmental Microbiology 69 (2): 1129–1135.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Brennan, M., B. Wanismail, M.C. Johnson, and B. Ray. 1986. Cellular damage in dried Lactobacillus acidophilus. Journal of Food Protection 49 (1): 47–53.CrossRefGoogle Scholar
  17. Budin-Verneuil, A., V. Pichereau, Y. Auffray, D.S. Ehrlich, and E. Maguin. 2006. Proteomic characterization of the acid tolerance response in Lactococcus lactis MG1363. 5 (18): 4794–4807.Google Scholar
  18. Budin-Verneuil, A., V. Pichereau, Y. Auffray, D. Ehrlich, and E. Maguin. 2007. Proteome phenotyping of acid stress-resistant mutants of Lactococcus lactis MG1363. Proteomics 7 (12): 2038–2046.PubMedCrossRefGoogle Scholar
  19. Burokas, A., S. Arboleya, R.D. Moloney, V.L. Peterson, K. Murphy, G. Clarke, C. Stanton, T.G. Dinan, and J.F. Cryan. 2017. Targeting the microbiota-gut-brain axis: Prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biological Psychiatry 82: 472. Scholar
  20. Caldas, T., N. Demont-Caulet, A. Ghazi, and G. Richarme. 1999. Thermoprotection by glycine betaine and choline. Microbiology 145 (Pt 9): 2543.PubMedCrossRefGoogle Scholar
  21. Champomier Vergès, M.C., M. Zuñiga, F. Morel-Deville, G. Pérez-Martínez, M. Zagorec, and S.D. Ehrlich. 1999. Relationships between arginine degradation, pH and survival in Lactobacillus sakei. Fems Microbiology Letters 180 (2): 297.PubMedCrossRefGoogle Scholar
  22. Chen, Pm, Hc Chen, Ct Ho, Ht Cjlien Jung, Jy Chen, and Js Chia. 2008. The two-component system ScnRK of Streptococcus mutans affects hydrogen peroxide resistance and murine macrophage killing. Microbes & Infection 10 (3): 293.CrossRefGoogle Scholar
  23. Chong, P., L. Drake, and I. Biswas. 2008. LiaS regulates virulence factor expression in Streptococcus mutans. Infection & Immunity 76 (76): 3093–3099.CrossRefGoogle Scholar
  24. Chu-Ky, S., R. Tourdot-Marechal, P.A. Marechal, and J. Guzzo. 2005. Combined cold, acid, ethanol shocks in Oenococcus oeni: Effects on membrane fluidity and cell viability. Biochimica Et Biophysica Acta 1717 (2): 118–124.PubMedCrossRefGoogle Scholar
  25. Crow, V., B. Curry, and M. Hayes. 2001. The ecology of non-starter lactic acid bacteria (NSLAB) and their use as adjuncts in New Zealand Cheddar.[J]. International Dairy Journal 11 (4): 275–283.CrossRefGoogle Scholar
  26. Cui, Y., W. Liu, X. Qu, Z. Chen, X. Zhang, T. Liu, and L. Zhang. 2012. A two component system is involved in acid adaptation of Lactobacillus delbrueckii subsp.bulgaricus. Microbiological Research 167 (5): 253–261.PubMedCrossRefGoogle Scholar
  27. Davis, C.R., D.J. Wibowo, T.H. Lee, and G.H. Fleet. 1986. Growth and metabolism of lactic acid bacteria during and after malolactic fermentation of wines at different pH. Applied & Environmental Microbiology 51 (3): 539.Google Scholar
  28. De Angelis, M., and M. Gobbetti. 2004. Environmental stress responses in Lactobacillus: A review. Proteomics 4 (1): 106–122.PubMedCrossRefPubMedCentralGoogle Scholar
  29. Derzelle, Sylviane, Bernard Hallet, Thierry Ferain, Jean Delcour, and Pascal Hols. 2002. Cold shock induction of the cspL gene in Lactobacillus plantarum involves transcriptional regulation. Journal of Bacteriology 184 (19): 5518–5523.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Derzelle, Sylviane, Bernard Hallet, Theirry Ferain, Jean Delcour, and Pascal Hols. 2003. Improved adaptation to cold-shock, stationary-phase, and freezing stresses in Lactobacillus plantarum overproducing cold-shock proteins. Applied & Environmental Microbiology 69 (7): 4285.CrossRefGoogle Scholar
  31. Dumont, F., P.A. Marechal, and P. Gervais. 2004. Cell size and water permeability as determining factors for cell viability after freezing at different cooling rates. Applied & Environmental Microbiology 70 (1): 268.CrossRefGoogle Scholar
  32. Duwat, P., S. Sourice, B. Cesselin, G. Lamberet, K. Vido, P. Gaudu, Y. Le Loir, F. Violet, P. Loubière, and A. Gruss. 2001. Respiration capacity of the fermenting bacterium Lactococcus lactis and its positive effects on growth and survival. Journal of Bacteriology 183 (15): 4509–4516.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Erny, D., A.L. Hrabe de Angelis, D. Jaitin, P. Wieghofer, O. Staszewski, E. David, H. Keren-Shaul, T. Mahlakoiv, K. Jakobshagen, T. Buch, V. Schwierzeck, O. Utermohlen, E. Chun, W.S. Garrett, K.D. McCoy, A. Diefenbach, P. Staeheli, B. Stecher, I. Amit, and M. Prinz. 2015. Host microbiota constantly control maturation and function of microglia in the CNS. Nature Neuroscience 18 (7): 965–977. Scholar
  34. Fang, L., W. Jiang, W. Bae, and M. Inouye. 1997. Promoter-independent cold-shock induction of cspA and its derepression at 37 degrees C by mRNA stabilization. Molecular Microbiology 23 (2): 355.PubMedCrossRefGoogle Scholar
  35. Fetissov, S.O. 2017. Role of the gut microbiota in host appetite control: Bacterial growth to animal feeding behaviour. Nature Reviews. Endocrinology 13 (1): 11–25. Scholar
  36. Fiocco, D., V. Capozzi, P. Goffin, P. Hols, and G. Spano. 2007. Improved adaptation to heat, cold, and solvent tolerance in Lactobacillus plantarum. Applied Microbiology & Biotechnology 77 (4): 909–915.CrossRefGoogle Scholar
  37. Flahaut, S., Abdellah Benachour, Jean Christophe Giard, Philippe Boutibonnes, and Yanick Auffray. 1996. Defense against lethal treatments and de novo protein synthesis induced by NaCl in Enterococcus faecalis ATCC 19433. Archives of Microbiology 165 (5): 317–324.PubMedCrossRefPubMedCentralGoogle Scholar
  38. Fonseca, F., C. Béal, and G. Corrieu. 2001. Operating conditions that affect the resistance of lactic acid bacteria to freezing and frozen storage. Cryobiology 43 (3): 189–198.PubMedCrossRefPubMedCentralGoogle Scholar
  39. Fonseca, F., C. Beal, F. Mihoub, M. Marin, and G. Corrieu. 2003. Improvement of cryopreservation of Lactobacillus delbrueckii subsp. bulgaricus CFL1 with additives displaying different protective effects. International Dairy Journal 13 (11): 917–926.CrossRefGoogle Scholar
  40. Fuangthong, M., and J.D. Helmann. 2002. The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative. Proceedings of the National Academy of Sciences of the United States of America 99 (10): 6690–6695.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Fukuda, D., M. Watanabe, S. Sonezaki, S. Sugimoto, K. Sonomoto, and A. Ishizaki. 2002. Molecular characterization and regulatory analysis of dnaK operon of halophilic lactic acid bacterium Tetragenococcus halophila. Journal of Bioscience and Bioengineering 94 (4): 388–394.CrossRefGoogle Scholar
  42. Gao, Rong, and Ann M. Stock. 2009. Biological insights from structures of two-component proteins. Annual Review of Microbiology 63 (1): 133.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Goldenberg, D., I. Azar, and A.B. Oppenheim. 1996. Differential mRNA stability of the cspA gene in the cold-shock response of Escherichia coli. Molecular Microbiology 19 (2): 241.PubMedCrossRefPubMedCentralGoogle Scholar
  44. Gomez, Zavaglia A., E.A. Disalvo, and G.L. De Antoni. 2000. Fatty acid composition and freeze-thaw resistance in lactobacilli. Journal of Dairy Research 67 (2): 241.CrossRefGoogle Scholar
  45. Graumann, P., and M.A. Marahiel. 1997. Effects of heterologous expression of CspB, the major cold shock protein of Bacillus subtilis, on protein synthesis in Escherichia coli. Molecular and General Genetics 253 (6): 745–752.PubMedCrossRefPubMedCentralGoogle Scholar
  46. Gualerzi, C.O., A.M. Giuliodori, and C.L. Pon. 2003. Transcriptional and post-transcriptional control of cold-shock genes. Journal of Molecular Biology 331 (3): 527–539.PubMedCrossRefPubMedCentralGoogle Scholar
  47. Guillot, A., D. Obis, and M.Y. Mistou. 2000. Fatty acid membrane composition and activation of glycine-betaine transport in Lactococcus lactis subjected to osmotic stress. International Journal of Food Microbiology 55 (1–3): 47–51.PubMedCrossRefPubMedCentralGoogle Scholar
  48. Hamon, E., P. Horvatovich, E. Izquierdo, F. Bringel, E. Marchioni, D. Aoudéwerner, and S. Ennahar. 2011. Comparative proteomic analysis of Lactobacillus plantarum for the identification of key proteins in bile tolerance. BMC Microbiology 11 (1): 63.PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hoefnagel, M.H., M.J. Starrenburg, D.E. Martens, J. Hugenholtz, M. Kleerebezem, I.I. Van Swam, R. Bongers, H.V. Westerhoff, and J.L. Snoep. 2002. Metabolic engineering of lactic acid bacteria, the combined approach: Kinetic modelling, metabolic control and experimental analysis. Microbiology 148 (4): 1003–1013.PubMedCrossRefPubMedCentralGoogle Scholar
  50. Hu, B., F. Tian, G. Wang, Q. Zhang, J. Zhao, H. Zhang, and W. Chen. 2015. Enhancement of bile resistance in Lactobacillus plantarum strains by soy lecithin. Letters in Applied Microbiology 61 (1): 13.PubMedCrossRefPubMedCentralGoogle Scholar
  51. Jarocki, P., M. Podleśny, P. Glibowski, and Z. Targoński. 2014. A new insight into the physiological role of bile salt hydrolase among intestinal bacteria from the genus Bifidobacterium. Plos One 9 (12): e114379.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Jensen, Niels Bang Siemsen, Claus Rix Melchiorsen, Kirsten Væver Jokumsen, and John Villadsen. 2001. Metabolic behavior of Lactococcus lactis MG1363 in microaerobic continuous cultivation at a low dilution rate. Applied & Environmental Microbiology 67 (6): 2677.CrossRefGoogle Scholar
  53. Jie, Bi, Liu Song, Du Guocheng, and Chen Jian. 2016. Bile salt tolerance of Lactococcus lactis is enhanced by expression of bile salt hydrolase thereby producing less bile acid in the cells. Biotechnology Letters 38 (4): 659–665.CrossRefGoogle Scholar
  54. Jones, P.G., R.A. Vanbogelen, and F.C. Neidhardt. 1987. Induction of proteins in response to low temperature in Escherichia coli. Journal of Bacteriology 169 (5): 2092.PubMedPubMedCentralCrossRefGoogle Scholar
  55. Jones, Brian V., Máire Begley, Colin Hill, Cormac G.M. Gahan, and Julian R. Marchesi. 2008. Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proceedings of the National Academy of Sciences of the United States of America 105 (36): 13580.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Kawadamatsuo, M., Y. Shibata, and Y. Yamashita. 2009. Role of two component signaling response regulators in acid tolerance of Streptococcus mutans. Oral Microbiology & Immunology 24 (2): 173.CrossRefGoogle Scholar
  57. Keijser, B.J.F., E. Zaura, S.M. Huse, J.M.B.M. van der Vossen, F.H.J. Schuren, R.C. Montijn, J.M. Ten Cate, and W. Crielaard. 2008. Pyrosequencing analysis of the oral microflora of healthy adults. Journal of Dental Research 87 (11): 1016–1020.PubMedCrossRefGoogle Scholar
  58. Kets, Edwin P.W., and Jan A.M. De Bont. 1995. Protective effect of betaine on survival of Lactobacillus plantarum subjected to drying. Fems Microbiology Letters 116 (3): 251–255.CrossRefGoogle Scholar
  59. Kets, E., P. Teunissen, and J. De Bont. 1996. Effect of compatible solutes on survival of lactic acid bacteria subjected to drying. Applied & Environmental Microbiology 62 (1): 259–261.Google Scholar
  60. Kilstrup, M., S. Jacobsen, K. Hammer, and F.K. Vogensen. 1997. Induction of heat shock proteins DnaK, GroEL, and GroES by salt stress in Lactococcus lactis. Applied & Environmental Microbiology 63 (5): 1826–1837.Google Scholar
  61. Kim, N.R., D.W. Jeong, D.S. Ko, and J.H. Shim. 2017. Characterization of novel thermophilic alpha-glucosidase from Bifidobacterium longum. International Journal of Biological Macromolecules 99: 594–599. Scholar
  62. Koch, S., G. Oberson, E. Eugster-Meier, L. Meile, and C. Lacroix. 2007. Osmotic stress induced by salt increases cell yield, autolytic activity, and survival of lyophilization of Lactobacillus delbrueckii subsp. lactis. International Journal of Food Microbiology 117 (1): 36–42.PubMedCrossRefGoogle Scholar
  63. Konings, W.N., J.S. Lolkema, H. Bolhuis, H.W. van Veen, B. Poolman, and A.J.M. Driessen. 1997. The role of transport processes in survival of lactic acid bacteria. Energy transduction and multidrug resistance. Antonie Van Leeuwenhoek 71 (1–2): 117–128.PubMedCrossRefGoogle Scholar
  64. Krell, T., J. Lacal, A. Busch, H. Silvajiménez, M.E. Guazzaroni, and J.L. Ramos. 2010. Bacterial sensor kinases: Diversity in the recognition of environmental signals. Annual Review of Microbiology 64 (1): 539–559.PubMedCrossRefGoogle Scholar
  65. Küllenberg, Daniela, Lenka A. Taylor, Michael Schneider, and Ulrich Massing. 2012. Health effects of dietary phospholipids. Lipids in Health & Disease 11 (1): 3.CrossRefGoogle Scholar
  66. Kurdi, Peter, Koji Kawanishi, Kanako Mizutani, and Atsushi Yokota. 2006. Mechanism of growth inhibition by free bile acids in lactobacilli and Bifidobacteria. Journal of Bacteriology 188 (5): 1979.PubMedPubMedCentralCrossRefGoogle Scholar
  67. Kurz, M. 2008. Compatible solute influence on nucleic acids: Many questions but few answers. Saline Systems 4: 6. Scholar
  68. Lee, Ki Beom. 2004. Cold shock response in Lactococcus lactis ssp. diacetylactis: A comparison of the protection generated by brief pre-treatment at less severe temperatures. Process Biochemistry 39 (12): 2233–2239.CrossRefGoogle Scholar
  69. Lee, J.W., and J.D. Helmann. 2006. The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation. Nature 440 (7082): 363–367.PubMedCrossRefGoogle Scholar
  70. Lee, K., H.G. Lee, and Y.J. Choi. 2008. Proteomic analysis of the effect of bile salts on the intestinal and probiotic bacterium lactobacillus reuteri. Journal of Biotechnology 137 (1–4): 14–19.PubMedCrossRefGoogle Scholar
  71. Lemos, J.A., T.A. Brown Jr., and R.A. Burne. 2004. Effects of RelA on key virulence properties of planktonic and biofilm populations of Streptococcus mutans. Infection & Immunity 72 (3): 1431–1440.CrossRefGoogle Scholar
  72. Levesque, Cm, Rwperry Mair, Pcy Lau Ja, Yh. Li, and Dg Cvitkovitch. 2007. Systemic inactivation and phenotypic characterization of two-component systems in expression of Streptococcus mutans virulence properties. Letters in Applied Microbiology 45 (4): 398.PubMedPubMedCentralCrossRefGoogle Scholar
  73. Li Y H, Lau P C Y, Tang N, et al. Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans[J]. Journal of bacteriology, 2002, 184(22): 6333–6342.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Li, C., J.L. Zhao, Y.T. Wang, X. Han, and N. Liu. 2009. Synthesis of cyclopropane fatty acid and its effect on freeze-drying survival of Lactobacillus bulgaricus L2 at different growth conditions. World Journal of Microbiology & Biotechnology 25 (9): 1659–1665.CrossRefGoogle Scholar
  75. Li, B., F. Tian, X. Liu, J. Zhao, H. Zhang, and W. Chen. 2011. Effects of cryoprotectants on viability of Lactobacillus reuteri CICC6226. Applied Microbiology Biotechnology 92: 609–616.PubMedCrossRefGoogle Scholar
  76. Machado, M. Cecilia, Claudia S. López, Horacio Heras, and Emilio A. Rivas. 2004. Osmotic response in Lactobacillus casei ATCC 393: Biochemical and biophysical characteristics of membrane. Archives of Biochemistry & Biophysics 422 (1): 61.CrossRefGoogle Scholar
  77. Macpherson, A.J., M. Heikenwalder, and S.C. Ganal-Vonarburg. 2016. The liver at the nexus of host-microbial interactions. Cell Host and Microbe 20 (5): 561–571. Scholar
  78. Magnusson, Lisa U., Anne Farewell, and Thomas Nyström. 2005. ppGpp: a global regulator in Escherichia coli. Trends in Microbiology 13 (5): 236–242.PubMedCrossRefGoogle Scholar
  79. Marchesi, J.R., D.H. Adams, F. Fava, G.D. Hermes, G.M. Hirschfield, G. Hold, M.N. Quraishi, J. Kinross, H. Smidt, K.M. Tuohy, L.V. Thomas, E.G. Zoetendal, and A. Hart. 2016. The gut microbiota and host health: A new clinical frontier. Gut 65 (2): 330–339. Scholar
  80. Martoni, Christopher, Jasmine Bhathena, Aleksandra Malgorzata Urbanska, and Satya Prakash. 2008. Microencapsulated bile salt hydrolase producing Lactobacillus reuteri for oral targeted delivery in the gastrointestinal tract. Applied Microbiology and Biotechnology 81 (2): 225–233.PubMedCrossRefGoogle Scholar
  81. Melchiorsen, C.R., K.V. Jokumsen, J. Villadsen, M.G. Johnsen, H. Israelsen, and J. Arnau. 2000. Synthesis and posttranslational regulation of pyruvate formate-lyase in Lactococcus lactis. Journal of Bacteriology 182 (17): 4783.PubMedPubMedCentralCrossRefGoogle Scholar
  82. Monnet, C., C. Béal, and G. Corrieu. 2003. Improvement of the resistance of Lactobacillus delbrueckii ssp. bulgaricus to freezing by natural selection. Journal of Dairy Science 86 (10): 3048–3053.PubMedCrossRefGoogle Scholar
  83. Moser, S.A., and D.C. Savage. 2001. Bile salt hydrolase activity and resistance to toxicity of conjugated bile salts are unrelated properties in lactobacilli. Applied & Environmental Microbiology 67 (8): 3476–3480.CrossRefGoogle Scholar
  84. Nascimento, M.M., V.V. Gordan, C.W. Garvan, C.M. Browngardt, and R.A. Burne. 2009. Correlations of oral bacterial arginine and urea catabolism with caries experience. Oral Microbiology & Immunology 24 (2): 89.CrossRefGoogle Scholar
  85. O’Connell-Motherway, M., P. Morel, and Sinderen D. Van. 2000. Six putative two-component regulatory systems isolated from Lactococcus lactis subsp. cremoris MG1363. Microbiology 146 (4): 935–947.PubMedCrossRefGoogle Scholar
  86. Palmfeldt, J., and B. Hahn-Hägerdal. 2000. Influence of culture pH on survival of Lactobacillus reuteri subjected to freeze-drying. International Journal of Food Microbiology 55 (1–3): 235.PubMedCrossRefGoogle Scholar
  87. Panoff, Jean Michel, Bouachanh Thammavongs, Jean Marie Laplace, Axel Hartke, Philippe Boutibonnes, and Yanick Auffray. 1995. Cryotolerance and cold adaptation in Lactococcus lactis subsp. lactis IL1403. Cryobiology 32 (6): 516–520.CrossRefGoogle Scholar
  88. Panoff, J.M., B. Thammavongs, M. Guéguen, and P. Boutibonnes. 1998. Cold stress responses in mesophilic bacteria. Cryobiology 36 (2): 75–83.PubMedCrossRefGoogle Scholar
  89. Panoff, J.M., B. Thammavongs, and M. Guéguen. 2000. Cryoprotectants lead to phenotypic adaptation to freeze-thaw stress in Lactobacillus delbrueckii ssp. bulgaricus CIP 101027T. Cryobiology 40 (3): 264–269.PubMedCrossRefGoogle Scholar
  90. Patel, Anil K., Reeta R. Singhania, Ashok Pandey, and Sudhir B. Chincholkar. 2010. Probiotic bile salt hydrolase: Current developments and perspectives. Applied Biochemistry and Biotechnology 162 (1): 166–180.PubMedCrossRefGoogle Scholar
  91. Peschel, Andreas. 2002. How do bacteria resist human antimicrobial peptides? Trends in Microbiology 10 (4): 179–186.PubMedCrossRefGoogle Scholar
  92. Phadtare, S. 2004. Recent developments in bacterial cold-shock response. Current Issues in Molecular Biology 6 (2): 125.PubMedGoogle Scholar
  93. Piuri, M., C. Sanchez-Rivas, and S.M. Ruzal. 2005. Cell wall modifications during osmotic stress in Lactobacillus casei. Journal of Applied Microbiology 98 (1): 84–95.PubMedCrossRefGoogle Scholar
  94. Prasad, Jaya, Paul Mcjarrow, and Pramod Gopal. 2003. Heat and osmotic stress responses of probiotic Lactobacillus rhamnosus HN001 (DR20) in relation to viability after drying. Applied & Environmental Microbiology 69 (2): 917–925.CrossRefGoogle Scholar
  95. Rallu, F., A. Gruss, and E. Maguin. 1996. Lactococcus lactis and stress. Antonie Van Leeuwenhoek 70 (2–4): 243–251.PubMedCrossRefGoogle Scholar
  96. Rallu, F., A. Gruss, S.D. Ehrlich, and E. Maguin. 2000. Acid- and multistress-resistant mutants of Lactococcus lactis: Identification of intracellular stress signals. Molecular Microbiology 35 (3): 517.PubMedCrossRefGoogle Scholar
  97. Rault, A., C. Béal, S. Ghorbal, et al. 2007. Multiparametric flow cytometry allows rapid assessment and comparison of lactic acid bacteria viability after freezing and during frozen storage.[J]. Cryobiology 55 (1): 35–43.PubMedCrossRefPubMedCentralGoogle Scholar
  98. Rezaïki, Lahcen, Bénédicte Cesselin, Yuji Yamamoto, Karin Vido, Evelien Van West, Philippe Gaudu, and Alexandra Gruss. 2004. Respiration metabolism reduces oxidative and acid stress to improve long-term survival of Lactococcus lactis. Molecular Microbiology 53 (5): 1331–1342.PubMedCrossRefGoogle Scholar
  99. Romantsov, T., Z. Guan, and J.M. Wood. 2009. Cardiolipin and the osmotic stress responses of bacteria. Biochimica et Biophysica Acta 1788 (10): 2092–2100.PubMedPubMedCentralCrossRefGoogle Scholar
  100. Santi, I., R. Grifantini, S.M. Jiang, C. Brettoni, G. Grandi, M.R. Wessels, and M. Soriani. 2009. CsrRS regulates group B Streptococcus virulence gene expression in response to environmental pH: A new perspective on vaccine development. Journal of Bacteriology 191 (17): 5387–5397.PubMedPubMedCentralCrossRefGoogle Scholar
  101. Santivarangkna, C., B. Higl, and P. Foerst. 2008. Protection mechanisms of sugars during different stages of preparation process of dried lactic acid starter cultures. Food Microbiology 25 (3): 429–441.PubMedCrossRefGoogle Scholar
  102. Senadheera, M. Dilani, Bernard Guggenheim, Grace A. Spatafora, Yi Chen Cathy Huang, Jison Choi, David C.I. Hung, Jennifer S. Treglown, Steven D. Goodman, Richard P. Ellen, and Dennis G. Cvitkovitch. 2005. A VicRK signal transduction system in Streptococcus mutans affects gtfBCD, gbpB, and ftf expression, biofilm formation, and genetic competence development. Journal of Bacteriology 187 (12): 4064.PubMedPubMedCentralCrossRefGoogle Scholar
  103. Senadheera, D., K. Krastel, R. Mair, A. Persadmehr, J. Abranches, R.A. Burne, and D.G. Cvitkovitch. 2009. Inactivation of VicK affects acid production and acid survival of Streptococcus mutans. Journal of Bacteriology 191 (20): 6415–6424.PubMedPubMedCentralCrossRefGoogle Scholar
  104. Sheehan, Vivien M., Roy D. Sleator, Gerald F. Fitzgerald, and Colin Hill. 2006. Heterologous expression of BetL, a betaine uptake system, enhances the stress tolerance of Lactobacillus salivarius UCC118. Applied & Environmental Microbiology 72 (3): 2170–2177.CrossRefGoogle Scholar
  105. Sheehan, Vivien M., Roy D. Sleator, Colin Hill, and Gerald F. Fitzgerald. 2007. Improving gastric transit, gastrointestinal persistence and therapeutic efficacy of the probiotic strain Bifidobacterium breve UCC2003. Microbiology 153 (10): 3563–3571.PubMedCrossRefGoogle Scholar
  106. Shimrat, M. 2005. Influence of fermentation time, cryoprotectant and neutralization of cell concentrate on freeze-drying survival, storage stability, and acid and bile exposure of Bifidobacterium animalis ssp. lactis cells produced without milk-based ingredients. Journal of Applied Microbiology 99 (6): 1330.CrossRefGoogle Scholar
  107. Siaterlis, A., G. Deepika, and D. Charalampopoulos. 2009. Effect of culture medium and cryoprotectants on the growth and survival of probiotic lactobacilli during freeze drying. Letters in Applied Microbiology 48 (3): 295.PubMedCrossRefGoogle Scholar
  108. Stead, D., and S.F. Park. 2000. Roles of Fe superoxide dismutase and catalase in resistance of Campylobacter coli to freeze-thaw stress. Applied & Environmental Microbiology 66 (7): 3110–3112.CrossRefGoogle Scholar
  109. Streit, F., G. Corrieu, and C. Béal. 2007. Acidification improves cryotolerance of Lactobacillus delbrueckii subsp. bulgaricus CFL1. Journal of Biotechnology 128 (3): 659–667.PubMedCrossRefGoogle Scholar
  110. Suutari, M., and S. Laakso. 1992. Changes in fatty acid branching and unsaturation of Streptomyces griseus and Brevibacterium fermentans as a response to growth temperature. Applied & Environmental Microbiology 58 (7): 2338.Google Scholar
  111. Taranto, M.P., F. Sesma, A. Pesce De Ruiz Holgado, and G.F. De Valdez. 1997. Bile salts hydrolase plays a key role on cholesterol removal by Lactobacillus reuteri. Biotechnology Letters 19 (9): 845–847.CrossRefGoogle Scholar
  112. Tsou, Chih-Chiang, Dmitry Avtonomov, Brett Larsen, Monika Tucholska, Hyungwon Choi, Anne-Claude Gingras, and Alexey I. Nesvizhskii. 2015. DIA-Umpire: Comprehensive computational framework for data-independent acquisition proteomics. Nature Methods 12 (3): 258–264. Scholar
  113. Tymczyszyn, E.E. 2005. Influence of the growth at high osmolality on the lipid composition, water permeability and osmotic response of Lactobacillus bulgaricus. Archives of Biochemistry & Biophysics 443 (1): 66–73.CrossRefGoogle Scholar
  114. Uchihashi, T., R. Iino, T. Ando, and H. Noji. 2011. High-speed atomic force microscopy reveals rotary catalysis of rotorless F1-ATPase. Science 333 (6043): 755.PubMedCrossRefGoogle Scholar
  115. Van De Guchte, Maarten, Pascale Serror, Christian Chervaux, Tamara Smokvina, Stanislav D. Ehrlich, and Emmanuelle Maguin. 2002. Stress responses in lactic acid bacteria. Antonie Van Leeuwenhoek 82 (1–4): 187.PubMedCrossRefGoogle Scholar
  116. Velly, H., M. Bouix, S. Passot, C. Penicaud, H. Beinsteiner, S. Ghorbal, P. Lieben, and F. Fonseca. 2015. Cyclopropanation of unsaturated fatty acids and membrane rigidification improve the freeze-drying resistance of Lactococcus lactis subsp. lactis TOMSC161. Applied Microbiology & Biotechnology 99 (2): 907.CrossRefGoogle Scholar
  117. Verneuil, N., A. Rincé, M. Sanguinetti, B. Posteraro, G. Fadda, Y. Auffray, A. Hartke, and J.C. Giard. 2005. Contribution of a PerR-like regulator to the oxidative-stress response and virulence of enterococcus faecalis. Microbiology 151 (12): 3997–4004.PubMedCrossRefGoogle Scholar
  118. Vido, Karin, Dominique Le Bars, Michel Yves Mistou, Patricia Anglade, Alexandra Gruss, and Philippe Gaudu. 2004. Proteome analyses of heme-dependent respiration in Lactococcus lactis: Involvement of the proteolytic system. Journal of Bacteriology 186 (6): 1648–1657.PubMedPubMedCentralCrossRefGoogle Scholar
  119. Vido, K., H. Diemer, A. Van Dorsselaer, E. Leize, V. Juillard, A. Gruss, and P. Gaudu. 2005. Roles of thioredoxin reductase during the aerobic life of Lactococcus lactis. Journal of Bacteriology 187 (2): 601–610.PubMedPubMedCentralCrossRefGoogle Scholar
  120. Vrancken, G., T. Rimaux, S. Weckx, L. De Vuyst, and F. Leroy. 2009. Environmental pH determines citrulline and ornithine release through the arginine deiminase pathway in Lactobacillus fermentum IMDO 130101. International Journal of Food Microbiology 135 (3): 216–222.PubMedCrossRefPubMedCentralGoogle Scholar
  121. Wang, Y., G. Corrieu, and C. Béal. 2005a. Fermentation pH and temperature influence the cryotolerance of Lactobacillus acidophilus RD758. Journal of Dairy Science 88 (1): 21–29.PubMedCrossRefPubMedCentralGoogle Scholar
  122. Wang, Y., J. Delettre, A. Guillot, G. Corrieu, and C. Béal. 2005b. Influence of cooling temperature and duration on cold adaptation of Lactobacillus acidophilus RD758. Cryobiology 50 (3): 294–307.PubMedCrossRefPubMedCentralGoogle Scholar
  123. Wang, E., M.C. Bauer, A. Rogstam, S. Linse, D.T. Logan, and C. von Wachenfeldt. 2008. Structure and functional properties of the Bacillus subtilis transcriptional repressor Rex. Molecular Microbiology 69 (2): 466–478.PubMedCrossRefPubMedCentralGoogle Scholar
  124. Wang, G., S. Yin, H. An, S. Chen, and Y. Hao. 2011. Coexpression of bile salt hydrolase gene and catalase gene remarkably improves oxidative stress and bile salt resistance in Lactobacillus casei. Journal of Industrial Microbiology & Biotechnology 38 (8): 985–990.CrossRefGoogle Scholar
  125. Winstedt, L., L. Frankenberg, L. Hederstedt, and C. Von Wachenfeldt. 2000. Enterococcus faecalis V583 contains a cytochrome bd-type respiratory oxidase. Journal of Bacteriology 182 (13): 3863–3866.PubMedPubMedCentralCrossRefGoogle Scholar
  126. Wouters, J.A., B. Jeynov, F.M. Rombouts, W.M. de Vos, O.P. Kuipers, and T. Abee. 1999. Analysis of the role of 7 kDa cold-shock proteins of Lactococcus lactis MG1363 in cryoprotection. Microbiology 145 (11): 3185.PubMedCrossRefPubMedCentralGoogle Scholar
  127. Wouters, Jeroen A., Frank M. Rombouts, Oscar P. Kuipers, Willem M. De Vos, and T. Abee. 2000. The role of cold-shock proteins in low-temperature adaptation offood-related bacteria. Systematic & Applied Microbiology 23 (2): 165–173.CrossRefGoogle Scholar
  128. Wouters, J.A., H. Frenkiel, W.M.D. Vos, et al. 2001. Cold shock proteins of Lactococcus lactis MG1363 are involved in Cryoprotection and in the production of cold-induced proteins[J]. Applied and Environmental Microbiology 67 (11): 5171–5178.PubMedPubMedCentralCrossRefGoogle Scholar
  129. Wu, C., J. Zhang, M. Wang, G. Du, and J. Chen. 2012. Lactobacillus casei combats acid stress by maintaining cell membrane functionality. Journal of Industrial Microbiology & Biotechnology 39 (7): 1031–1039.CrossRefGoogle Scholar
  130. Xie, Y., L.S. Cutler, A. Chou, and B. Weimer. 2004. DNA macroarray profiling of Lactococcus lactis subsp. lactis IL1403 gene expression during environmental stresses. Applied & Environmental Microbiology 70 (11): 6738–6747.CrossRefGoogle Scholar
  131. Xiong, Zhi Qiang, Qiao Hui Wang, Ling Hui Kong, Xin Song, Guang Qiang Wang, Yong Jun Xia, Hui Zhang, Yong Sun, and Lian Zhong Ai. 2017. Short communication: Improving the activity of bile salt hydrolases in Lactobacillus casei based on in silico molecular docking and heterologous expression. Journal of Dairy Science 100 (2): 975–980.PubMedCrossRefGoogle Scholar
  132. Zeeb, Markus, Klaas E.A. Max, Ulrich Weininger, Christian Löw, Heinrich Sticht, and Jochen Balbach. 2006. Recognition of T-rich single-stranded DNA by the cold shock protein Bs-CspB in solution. Nucleic Acids Research 34 (16): 4561–4571.PubMedPubMedCentralCrossRefGoogle Scholar
  133. Zhang, Juan, Du Guo Cheng, Yanping Zhang, Xian Yan Liao, Miao Wang, Yin Li, and Jian Chen. 2010. Glutathione protects Lactobacillus sanfranciscensis against freeze-thawing, freeze-drying, and cold treatment. Applied & Environmental Microbiology 76 (9): 2989–2996.CrossRefGoogle Scholar
  134. Zhao, Shanshan, Qiuxiang Zhang, Guangfei Hao, Xiaoming Liu, Jianxin Zhao, Yongquan Chen, Hao Zhang, and Wei Chen. 2014. The protective role of glycine betaine in Lactobacillus plantarum ST-III against salt stress. Food Control 44: 208–213.CrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.School of Food Science and TechnologyJiangnan UniversityWuxiChina

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