Abstract
Lactic acid bacteria (LAB) continue as an important group of gram-positive bacteria that have been extensively exploited in food industries and various biotechnological applications. Some LAB species are, however, opportunistic pathogens and were reported to be associated with overwhelming number of human infections. During the use of LAB in industry or over the course of human infection, these bacteria are exposed to environmental stress. While LAB display adaptive mechanisms to cope with adverse conditions, the regulation of these mechanisms remains to be elucidated. Recent completion of genome sequencing of various LAB strains combined with the development of advanced molecular techniques have enabled the identification of a number of putative two-component signal transduction systems, also known as two-component regulatory systems (2CRS), in LAB. Examining the effect of deleting genes specifying putative 2CRS proteins in these organisms has revealed the involvement of 2CRS in the responses of LAB to different stresses. There are lines of evidence indicating that certain 2CRS may mediate a general stress response in Enterococcus faecalis and Streptococcus pyogenes. This review highlights the influence of 2CRS on the physiology of LAB during optimal growth and survival/growth on exposure to environmental stress.
Keywords: lactic acid bacteria, stress responses, two-component signal transduction systems
Full Text
The Full Text of this article is available as a PDF (2.4 MB).
References
- 1.Axelsson L. (1998) Lactic acid bacteria: classification and physiology. In: Salminen S., and Von Wright A. (eds.) Lactic Acid Bacteria: Microbiology and Functional Aspects, pp. 1–72. 2nd edn. Marcel Dekker, Inc, New York. [Google Scholar]
- 2.Fox P. F. (1993) Cheese: An overview. In: Fox P. F. (ed.) Cheese: Chemistry, Physics and Microbiology, Vol. 1, pp. 1–36, 2nd edn. Chapman and Hall, London. [Google Scholar]
- 3.International Dairy Federation (IDF) (1999) The world dairy situation 1999. International Dairy Federation, Brussels. [Google Scholar]
- 4.Klaenhammer T., Altermann E. et al. (2002) Discovering lactic acid bacteria by genomics. Antonie van Leeuwenhoek, 82, 29–58. [DOI] [PubMed] [Google Scholar]
- 5.Adams M. R. (1999). Safety of industrial lactic acid bacteria. J. Biotechnol., 68, 171–178. [DOI] [PubMed] [Google Scholar]
- 6.Dalton T. L., and Scott J. R. (2004) CovS inactivates CovR and is required for growth under conditions of general stress in Streptococcus pyogenes. J. Bacterial., 186, 3928–3937. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Girgis H. S., Smith J., Luchansky J. B., and Klaenhammer T. R. (2002) Stress adaptations of lactic acid bacteria. In: Yousef A. E., and Juneja V. K. (eds.) Microbial stress adaptation and food safety, pp. 159–211. CRC Press, Boca Raton, Florida. [Google Scholar]
- 8.De Guchte M. V., Serror P., Chervaux C., Smokvina T., Ehrlich S. D., and Maguin E. (2002) Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek, 82, 187–216. [PubMed] [Google Scholar]
- 9.Hengge-Aronis R. (2002) Signal transduction and regulatory mechanisms involved in control of the σS (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev., 66, 373–395. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Botolin A., Wincker P., Mauger S., Jaillon O., Malarme K., Weissenbach J., Ehrlich S. D., and Sorokin A. (2001) The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp lactis IL1403. Genome Res., 11, 731–753. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Kleerebezem M., Boekhorst J. et al. (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. PNAS, 100, 1990–1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Benachour A., Muller C., Dabrowski-Coton M., Le Breton Y., Giard J. C., Rince A., Auffray Y., and Hartke A. (2005) The Enterococcus faecalis SigV protein is an extracytoplasmic function sigma factor contributing to survival following heat, acid, and ethanol treatments. J. Bacteriol., 187, 1022–1035. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Helmann J. D. (2003) The extracytoplasmic function (ECF) sigma factors. Adv. Microbiol. Physiol., 46, 47–110. [DOI] [PubMed] [Google Scholar]
- 14.Hoch J. A., and Silhavy T. J. (1995) Two component signal transduction. ASM Press, Washington, D.C. [Google Scholar]
- 15.Neidhardt F. C. (2002) Microbial reaction to environment: bacterial stress responses revisited in the genomic-proteomic era. In: Hodgson D. A., and Thomas C. M. (eds.) Signals, Switches, Regulons and Cascades: Control of Bacterial Gene Expression, pp. 1–18. Cambridge University Press, Cambridge. [Google Scholar]
- 16.El-Sharoud W. M. (2002) Locating a stress sensor. Microbiologist, 3, 34–35. [Google Scholar]
- 17.White D. (2000) The Physiology and Biochemistry of Prokaryotes. 2nd edn. Oxford University Press, New York. [Google Scholar]
- 18.Hellingwerf K. J. (2005) Bacterial observations: a rudimentary form of intelligence? Trends Microbiol., 13, 152–158. [DOI] [PubMed] [Google Scholar]
- 19.Parkinson J. S. (1995) Genetic approaches for signalling pathways and proteins. In: Hoch J. A., and Silhavy T. J. (eds.) Two-component Signal Transduction, pp. 9–23. ASM Press, Washington, D.C. [Google Scholar]
- 20.West A. H., and Stock A. M. (2001) Histidine kinases and response regulator proteins in two-component signalling systems. Trends Biochem. Sci., 26, 369–376. [DOI] [PubMed] [Google Scholar]
- 21.Ulrich L. E., Koonin E. V., and Zhulin I. B. (2005) One-component systems dominate signal transduction in prokaryotes. Trends Microbiol., 13, 52–56. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Stock A. M., Robinson V. L., and Goudreau P. N. (2000) Two-component signal transduction. Annu. Rev. Biochem., 69, 183–215. [DOI] [PubMed] [Google Scholar]
- 23.Foussard M., Cabantous S., Pedelacq J.-D., Guillet V., Tranier S., Mourey L., Brick C., and Samama J.-P. (2001) The molecular puzzle of two-component signalling cascades. Microbes Infect., 3, 417–424. [DOI] [PubMed] [Google Scholar]
- 24.Perego M., and Hoch J. A. (1996) Protein aspartate phosphatases control the output of two-component signal transduction systems. Trends Genet., 12, 97–10. [DOI] [PubMed] [Google Scholar]
- 25.Hellingwerf K. J., Crielaard W. C., De Mattos J. T., Hoff W. D., Kort R., Verhamme D. T., and Avignone-Rossa C. (1998) Current topics in signal transduction in bacteria. Antonie van Leeuwenhoek, 74, 211–227. [DOI] [PubMed] [Google Scholar]
- 26.Altermann E., Russell W. M. et al. (2004) Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. PNAS, 102, 3906–3912. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Hancock L., and Perego M. (2004) Two-component signal transduction in Enterococcus faecalis. J. Bacterial., 184, 5819–5825. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Morel-Deville F., Ehrlich S. D., and Morel P. (1997) Identification by PCR of genes encoding multiple response regulators. Microbiology, 143, 1513–1520. [DOI] [PubMed] [Google Scholar]
- 29.Morel-Deville F., Fauvel F., and Morel P. (1998) Two-component signal-tansducing systems involved in stress responses and vancomycin susceptibility in Lactobacillus sakei. Microbiology, 144, 2873–2883. [DOI] [PubMed] [Google Scholar]
- 30.O'Connell-Motherway M., Fitzgerald G. F., and van Sinderen D. (1997) Cloning and sequence analysis of putative histidine protein kinases isolated from Lactococcus lactis subsp. cremoris MG1363. Appl. Environ. Microbiol., 63, 2454–2459. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.O'Connell-Motherway M., van Sinderen D., Morel-Deville F., Fitzgerald G. F., Ehrlich S. D., and Morel P. (2000) Six putative two-component regulatory systems isolated from Lactococcus lactis subsp. cremoris MG1363. Microbiol., 46, 935–947. [DOI] [PubMed] [Google Scholar]
- 32.Ng W. L., and Winkler M. E. (2004) Singular structures and operon organisations of essential two-component systems in species of Streptococcus. Microbiology, 150, 3096–3098. [DOI] [PubMed] [Google Scholar]
- 33.Ng W. L., Robertson G. T., Kazmierczak K. M., Zhoa J., Gilmour R., and Winkler M. E. (2003) Constitutive expression of PcsB suppresses the requirement for the essential VicR (YycF) response regulator in Streptococcus pneumoniae R6. Mol. Microbiol., 50, 1647–1663. [DOI] [PubMed] [Google Scholar]
- 34.Ng W. L., Kazmierczak K. M., and Winkler M. E. (2003) Defective cells wall synthesis in Streptococcus pneumoniae R6 depleted for the essential PcsB putative murein hydrolase or the VicR (YycF) response regulator in Streptococcus pneumoniae R6. Mol. Microbiol., 53, 1161–1175. [DOI] [PubMed] [Google Scholar]
- 35.Mohedano M. L., Overweg K., de la Fuente A., Reuter M., Altabe S., Mulholland F., de Mendoza D., Lopez P., and Wells J. M. (2005) Evidence that the essential response regulator YycF in Streptococcus pneumoniae modulates expression of fatty acid biosynthesis genes and alters membrane composition. J. Bacteriol., 187, 2357–2367. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Li Y.-H., Lau P. C. Y., Tang N., Svensater G., Ellen R. P., and Cvitkovitch D. G. (2002) Novel Two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans. J. Bacterial., 184, 6333–6342. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Le Breton Y., Boel G., Benachour A., Prevost H., Auffray Y., and Rince A. (2003) Molecular characterization of Enterococcus faecalis two-component signal transduction pathways related to environmental stresses. Environ. Microbiology, 5, 329–337. [DOI] [PubMed] [Google Scholar]
- 38.Le Breton Y., Maze A., Hartke A., Lemarinier S., Auffray Y., and Rince A. (2002) Isolation and characterisation of bile salts sensitive mutants of Enterococcus faecalis. Curr. Microbiol., 45, 434–439. [DOI] [PubMed] [Google Scholar]
- 39.Azcarate-Peril M. A., McAuliffe O., Altermann E., Lick S., Russel W. M., and Klaenhammer T. R. (2005) Microarray analysis of a two-component regulatory system involved in acid resistance and proteolytic acitivity in Lactobacillus acidophilus. Appl. Environ. Microbiol., 71, 5794–5804. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Cheigh C.-I., and Pyun Y.-R. (2005) Nisin biosynthesis and its properties. Biotech. Lett., 27, 1641–1648. [DOI] [PubMed] [Google Scholar]
- 41.Engelke G., Gutowski-Eckel Z., Kiesau P., Siegers K., Hammelmann M., and Entian K. D. (1994) Regulation of nisin biosynthesis and immunity in Lactococcus lactis 6F3. Appl. Environ. Microbiol., 60, 814–825. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Teng F., Wang L., Singh K. V., Murray B. E., and Weinstock G. M. (2002) Involvement of PhoP-PhoS homologs in Enterococcus faecalis virulence. Infect. Immunol., 70, 1991–1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Cotter P. D., Emerson N., Gahan C. G. M., and Hill C. (1999) Identification and disruption of lisRK, a genetic locus encoding a two-component signal transduction system involved in stress tolerance and virulence in Listeria monocytogenes. J. Bacterial., 181, 6840–6843. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Arthur M., Molinas C., and Courvalin P. (1992) The VanS-VanR two-component regulatory system controls synthesis of depsipeptide peptidoglycan precursors in Enterococcus faecium BM4147. J. Bacteriol., 174, 2582–2591. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Hoffer S. M., Westerhoff H. V., Hellingwerf K. J., Postma P. W., and Tommassen J. (2001) Autoamplification of a two-component regulatory system results in “learning” behavior. J. Bacteriol., 183, 4914–4917. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Bearson S., Dearson B., and Foster J. W. (1997) Acid stress responses in enterobacteria. FEMS Microbiol. Lett., 147, 173–180. [DOI] [PubMed] [Google Scholar]
- 47.Marty-Teysset C., de la Torre F., and Garel J. R. (2000) Increased production of hydrogen peroxide by Lactobacillus delbrueckii subsp. bulgaricus upon aeration: involvement of an NADH oxidase in oxidative stress. Appl. Environ. Microbiol., 66, 262–267. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48.Hutkins R. W., Ellefson W. L., and Kashket E. R. (1987). Betaine transport imparts osmotolerance on a strain of Lactobacillus acidophilus. Appl. Environ. Microbiol., 53, 2275–2281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.O'Callaghan J., and Condon S. (2000) Growth of Lactococcus lactis strains at low water activity: correlation with the ability to accumulate glycine betaine. Int. J. Food Microbiol., 55, 127–31. [DOI] [PubMed] [Google Scholar]
- 50.Flahaut S., Hartke A., Giard J. C., Benachour A., Boutibonnes P., and Auffray Y. (1996) Relationship between stress response toward bile salts, acid and heat treatment in Enterococcus faecalis. FEMS Microbiol. Lett., 15, 49–54. [DOI] [PubMed] [Google Scholar]
- 51.Whistler C. A., Corbell N. A., Sarniguet A., Ream W., and Loper J. E. (1998) The two-component regulators GacS and GacA influence accumulation of the stationary phase sigma factor σS and the stress response in Pseudomonas fluorescence Pf-5. J. Bacteriol., 180, 6635–6641. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Mukhopadhyay S., Audia J. P., Roy R. N., and Schellhorn H. E. (2000) Transcriptional induction of the conserved alterantive sigma factor RpoS in Escherichia coli is dependent on BarA, a probable two-component regulator. Mol. Microbiol., 37, 371–381. [DOI] [PubMed] [Google Scholar]