Characterization of Streptococcus thermophilus two-component systems: In silico analysis, functional analysis and expression of response regulator genes in pure or mixed culture with its yogurt partner, Lactobacillus delbrueckii subsp. bulgaricus

International Journal of Food Microbiology

Volumn 151, Issue 2, 2011, Pages 171-181

  Thevenard, Benoît ^a   Rasoava, Niriaina ^a   Fourcassié, Pascal ^b   Monnet, Véronique ^a   Boyaval, Patrick ^b   Rul, Françoise ^a  

^a UMR1319 MICALIS   (France)

^b Danisco France SAS   (France)

Author keywords

Mixed culture; Streptococcus thermophilus; Two component systems; Yogurt

Indexed keywords

ERYTHROMYCIN; KANAMYCIN; YOGHURT;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIAL STRAIN; COMPARTMENT MODEL; COMPUTER MODEL; GENE EXPRESSION; GENE FUNCTION; LACTOBACILLUS DELBRUECKII; LACTOBACILLUS DELBRUECKII BULGARUS; NONHUMAN; REGULATOR GENE; RR02 GENE; RR09 GENE; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS THERMOPHILUS;

AMINO ACID SEQUENCE; ANIMALS; COCULTURE TECHNIQUES; DNA, BACTERIAL; GENES, BACTERIAL; GENES, REGULATOR; HYDROGEN PEROXIDE; LACTOBACILLUS DELBRUECKII; MILK; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; STREPTOCOCCUS THERMOPHILUS; TRANSCRIPTOME;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); LACTOBACILLUS DELBRUECKII SUBSP. BULGARICUS; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS THERMOPHILUS;

EID: 80054082798     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2011.08.019     Document Type: Article

References (64)

1. Bernard R., Joseph P., Guiseppi A., Chippaux M., Denizot F. YtsCD and YwoA, two independent systems that confer bacitracin resistance to Bacillus subtilis. FEMS Microbiology Letters 2003, 228:93-97.
2. Bisicchia P., Noone D., Lioliou E., Howell A., Quigley S., Jensen T., Jarmer H., Devine K.M. The essential YycFG two-component system controls cell wall metabolism in Bacillus subtilis. Molecular Microbiology 2007, 65:180-200.
3. Biswas S., Biswas I. Regulation of the glucosyltransferase (gtfBC) operon by CovR in Streptococcus mutans. Journal of Bacteriology 2006, 188:988-998.
4. Biswas I., Gruss A., Ehrlich S.D., Maguin E. High-efficiency gene inactivation and replacement system for Gram-positive bacteria. Journal of Bacteriology 1993, 175:3628-3635.
5. Biswas I., Drake L., Biswas S. Regulation of gbpC expression in Streptococcus mutans. Journal of Bacteriology 2007, 189:6521-6531.
6. Biswas I., Drake L., Erkina D., Biswas S. Involvement of sensor kinases in the stress tolerance response of Streptococcus mutans. Journal of Bacteriology 2008, 190:68-77.
7. Bolotin A., Quinquis B., Renault P., Sorokin A., Ehrlich S.D., Kulakauskas S., Lapidus A., Goltsman E., Mazur M., Pusch G.D., Fonstein M., Overbeek R., Kyprides N., Purnelle B., Prozzi D., Ngui K., Masuy D., Hancy F., Burteau S., Boutry M., Delcour J., Goffeau A., Hols P. Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nature Biotechnology 2004, 22:1554-1558.
8. Chong P., Drake L., Biswas I. Modulation of covR expression in Streptococcus mutans UA159. Journal of Bacteriology 2008, 190:4478-4488.
9. Dalton T.L., Scott J.R. CovS inactivates CovR and is required for growth under conditions of general stress in Streptococcus pyogenes. Journal of Bacteriology 2004, 186:3928-3937.
10. Deng D.M., Liu M.J., ten Cate J.M., Crielaard W. The VicRK system of Streptococcus mutans responds to oxidative stress. Journal of Dental Research 2007, 86:606-610.
11. Derzelle S., Bolotin A., Mistou M.-Y., Rul F. Proteome analysis of Streptococcus thermophilus grown in milk reveals pyruvate formate-lyase as the major upregulated protein. Applied and Environmental Microbiology 2005, 71:8597-8605.
12. Dintner S., Staron A., Berchtold E., Petri T., Mascher T., Gebhard S. Co-evolution of ABC-transporters and two-component regulatory systems as resistance modules against antimicrobial peptides in Firmicutes Bacteria. Journal of Bacteriology 2011, 10.1128/JB.05175-11.
13. Dubrac S., Boneca I.G., Poupel O., Msadek T. New insights into the WalK/WalR (YycG/YycF) essential signal transduction pathway reveal a major role in controlling cell wall metabolism and biofilm formation in Staphylococcus aureus. Journal of Bacteriology 2007, 189:8257-8269.
14. Dubrac S., Bisicchia P., Devine K.M., Msadek T. A matter of life and death: cell wall homeostasis and the WalKR (YycGF) essential signal transduction pathway. Molecular Microbiology 2008, 70:1307-1322.
15. Ducros V.M.A., Lewis R.J., Verma C.S., Dodson E.J., Leonard G., Turkenburg J.P., Murshudov G.N., Wilkinson A.J., Brannigan J.A. Crystal structure of GerE, the ultimate transcriptional regulator of spore formation in Bacillus subtilis. Journal of Molecular Biology 2001, 306:759-771.
16. Dyer C.M., Dahlquist F.W. Switched or not?: The structure of unphosphorylated CheY bound to the N terminus of FliM. Journal of Bacteriology 2006, 188:7354-7363.
17. Fontaine L., Hols P. The inhibitory spectrum of thermophilin 9 from Streptococcus thermophilus LMD-9 depends on the production of multiple peptides and the activity of BlpG(St), a thiol-disulfide oxidase. Applied and Environmental Microbiology 2008, 74:1102-1110.
18. Fontaine L., Boutry C., Guedon E., Guillot A., Ibrahim M., Grossiord B., Hols P. Quorum-sensing regulation of the production of Blp bacteriocins in Streptococcusthermophilus. Journal of Bacteriology 2007, 189:7195-7205.
19. Froehlich B.J., Bates C., Scott J.R. Streptococcus pyogenes CovR/S mediates growth in iron starvation and in the presence of the human cationic antimicrobial peptide LL-37. Journal of Bacteriology 2008, 191:673-677.
20. Fujita M., Gonzalez-Pastor J.E., Losick R. High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. Journal of Bacteriology 2005, 187:1357-1368.
21. Fukushima T., Szurmant H., Kim E.J., Perego M., Hoch J.A. A sensor histidine kinase co-ordinates cell wall architecture with cell division in Bacillus subtilis. Molecular Microbiology 2008, 69:621-632.
22. Galperin M.Y. A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiology 2005, 5.
23. Galperin M.Y. structural classification of bacterial response regulators: diversity of output domains and domain combinations. Journal of Bacteriology 2006, 188:4169-4182.
24. Garault P., Letort C., Juillard V., Monnet V. Branched-chain amino acid biosynthesis is essential for optimal growth of Streptococcus thermophilus in milk. Applied and Environmental Microbiology 2000, 66:5128-5133.
25. Gardan R., Besset C., Guillot A., Gitton C., Monnet V. The oligopeptide transport system is essential for the development of natural competence in Streptococcus thermophilus strain LMD-9. Journal of Bacteriology 2009, 191:4647-4655.
26. Graham M.R., Smoot L.M., Migliaccio C.A.L., Virtaneva K., Sturdevant D.E., Porcella S.F., Federle M.J., Adams G.J., Scott J.R., Musser J.M. Virulence control in group A Streptococcus by a two-component gene regulatory system: global expression profiling and in vivo infection modeling. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:13855-13860.
27. Gryllos I., Lewin J.C., Wessels M.R. The CsrR/CsrS two-component system of group A Streptococcus responds to environmental Mg2+. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:4227-4232.
28. Gryllos I., Grifantini R., Colaprico A., Jiang S., Deforce E., Hakansson A., Telford J.L., Grandi G., Wessels M.R. Mg(2+) signalling defines the group A streptococcalCsrRS (CovRS) regulon. Molecular Microbiology 2007, 65:671-683.
29. Gusa A.A., Froehlich B.J., Desai D., Stringer V., Scott J.R. CovR activation of the dipeptide permease promoter (PdppA) in Group A Streptococcus. Journal of Bacteriology 2007, 189:1407-1416.
30. Herve-Jimenez L., Guillouard I., Guedon E., Gautier C., Boudebbouze S., Hols P., Monnet V., Rul F., Maguin E. Physiology of Streptococcus thermophilus during the late stage of milk fermentation with special regard to sulfur amino-acid metabolism. Proteomics 2008, 8:4273-4286.
31. Herve-Jimenez L., Guillouard I., Guedon E., Boudebbouze S., Hols P., Monnet V., Maguin E., Rul F. Postgenomic analysis of Streptococcus thermophilus cocultivated in milk with Lactobacillus delbrueckii subsp bulgaricus: involvement of nitrogen, purine, and iron metabolism. Applied and Environmental Microbiology 2009, 75:2062-2073.
32. Hoch J.A. Two-component and phosphorelay signal transduction. Current Opinion in Microbiology 2000, 3:165-170.
33. Hols P., Hancy F., Fontaine L., Grossiord B., Prozzi D., Leblond-Bourget N., Decaris B., Bolotin A., Delorme C., Ehrlich S.D., Guédon E., Monnet V., Renault P., Kleerebezem M. New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiology Reviews 2005, 29:435-463.
34. Ibrahim M., Nicolas P., Bessieres P., Bolotin A., Monnet V., Gardan R. A genome-wide survey of short coding sequences in streptococci. Microbiology 2007, 153:3631-3644.
35. Kirby J.R. Chemotaxis-like regulatory systems: unique roles in diverse bacteria. Annual Review of Microbiology 2009, 63:45-59.
36. Lamy M.C., Zouine M., Fert J., Vergassola M., Couve E., Pellegrini E., Glaser P., Kunst F., Msadek T., Trieu-Cuot P., Poyart C. CovS/CovR of group B Streptococcus: a two-component global regulatory system involved in virulence. Molecular Microbiology 2004, 54:1250-1268.
37. Lee S.F., Delaney G.D., Elkhateeb M. A two-component covRS regulatory system regulates expression of fructosyltransferase and a novel extracellular carbohydrate in Streptococcus mutans. Infection and Immunity 2004, 72:3968-3973.
38. Letort C., Juillard V. Development of a minimal chemically-defined medium for the exponential growth of Streptococcus thermophilus. Journal of Applied Microbiology 2001, 91:1023-1029.
39. Li Y.H., Lau P.C., Tang N., Svensater G., Ellen R.P., Cvitkovitch D.G. Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans. Journal of Bacteriology 2002, 184:6333-6342.
40. Lin W.J., Walthers D., Connelly J.E., Burnside K., Jewell K.A., Kenney L.J., Rajagopal L. Threonine phosphorylation prevents promoter DNA binding of the Group B Streptococcus response regulator CovR. Molecular Microbiology 2009, 71:1477-1495.
41. Liu Y.L., Burne R.A. Multiple two-component systems modulate alkali generation in Streptococcus gordonii in response to environmental stresses. Journal of Bacteriology 2009, 191:7353-7362.
42. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta CT) Method. Methods in Enzymology 2001, 25:402-408.
43. Maguin E., Prevost H., Ehrlich D., Gruss A. Efficient insertional mutagenesis in lactococci and other Gram-positive bacteria. Journal of Bacteriology 1996, 178:931-935.
44. Makarova K., Slesarev A., Wolf Y., Sorokin A., Mirkin B., Koonin E., Pavlov A., Pavlova N., Karamychev V., Polouchine N., Shakhova V., Grigoriev I., Lou Y., Rohksar D., Lucas S., Huang K., Goodstein D.M., Hawkins T., Plengvidhya V., Welker D., Hughes J., Goh Y., Benson A., Baldwin K., Lee J.H., Diaz-Muniz I., Dosti B., Smeianov V., Wechter W., Barabote R., Lorca G., Altermann E., Barrangou R., Ganesan B., Xie Y., Rawsthorne H., Tamir D., Parker C., Breidt F., Broadbent J., Hutkins R., O'Sullivan D., Steele J., Unlu G., Saier M., Klaenhammer T., Richardson P., Kozyavkin S., Weimer B., Mills D. Comparative genomics of the lactic acid bacteria. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:15611-15616.
45. Martinez-Hackert E., Stock A.M. Structural relationships in the OmpR family of winged-helix transcription factors. Journal of Molecular Biology 1997, 269:301-312.
46. Mitrophanov A.Y., Churchward G., Borodovsky M. Control of streptococcus pyogenes virulence: modeling of the CovR/S signal transduction system. Journal of Theorical Biology 2007, 246:113-128.
47. Nikolskaya A.N., Galperin M.Y. A novel type of conserved DNA-binding domain in the transcriptional regulators of the AlgR/AgrA/LytR family. Nucleic Acids Research 2002, 30:2453-2459.
48. Ohki R., Giyanto K., Tateno W., Masuyama S., Moriya K., Kobayashi, Ogasawara N. The BceRS two-component regulatory system induces expression of the bacitracin transporter, BceAB, in Bacillus subtilis. Molecular Microbiology 2003, 49:1135-1144.
49. Paterson G.K., Blue C.E., Mitchell T.J. Role of two-component systems in the virulence of Streptococcus pneumoniae. Journal of Medical Microbiology 2006, 55:355-363.
50. Perry J.A., Levesque C.M., Suntharaligam P., Mair R.W., Bu M., Cline R.T., Peterson S.N., Cvitkovitch D.G. Involvement of Streptococcus mutans regulator RR11 in oxidative stress response during biofilm growth and in the development of genetic competence. Letters in Applied Microbiology 2008, 47(4):39-44.
51. Pospiech A., Neumann B. A versatile quick-prep of genomic DNA from Gram-positive bacteria. Trends in Genetics 1995, 11:217-218.
52. Rul F., Ben-Yahia L., Chegdani F., Wrzosek L., Thomas S., Noordine M.-L., Gitton C., Cherbuy C., Langella P., Thomas M. Impact of the metabolic activity of Streptococcus thermophilus of the colon epithelium of gnotobiotic rats. Journal of Biological Chemistry 2011, 286:10288-10296.
53. Senadheera D., Krastel K., Mair R., Persadmehr A., Abranches J., Burne R.A., Cvitkovitch D.G. Inactivation of VicK affects acid production and acid survival of Streptococcus mutans. Journal of Bacteriology 2009, 191:6415-6424.
54. Sidote D.J., Barbieri C.M., Wu T., Stock A.M. Structure of the Staphylococcus aureus AgrA LytTR domain bound to DNA reveals a beta fold with an unusual mode of binding. Structure 2008, 16:727-735.
55. Sieuwerts S., Molenaar D., van Hijum S.A.F.T., Beerthuyzen M., Stevens M.J.A., Janssen P.W.M., Ingham C.J., de Bok F.A.M., de Vos W.M., van Hylckama Vlieg J.E.T. Mixed culture transcriptome analysis reveals molecular basis of mixed culture growth in Streptococcus thermophilus and Lactobacillus bulgaricus. Applied and Environmental Microbiology 2010, 76:7775-7784.
56. Staron A., Finkeisen D.E., Mascher T. Peptide antibiotic sensing and detoxification modules of Bacillus subtilis. Antimicrobial Agents and Chemotherapy 2011, 55:515-525.
57. Stock A.M., Robeinson V.L., Goudreau P.N. Two-component signal transduction. Annual Review of Biochemistry 2000, 69:183-215.
58. Suntharalingam P., Senadheera M.D., Mair R.W., Levesque C.M., Cvitkovitch D.G. The LiaFSR system regulates the cell envelope stress response in Streptococcusmutans. Journal of Bacteriology 2009, 191:2973-2984.
59. Tabasco R., García-Cayuela T., Peláez C., Requena T. Lactobacillus acidophilus La-5 increases lactacin B production when it senses live target bacteria. International Journal of Food Microbiology 2009, 132:109-116.
60. Trieu-Cuot P., Courvalin P. Nucleotide-sequence of the Streptococcus-faecalis plasmid gene encoding the 3-5-aminoglycoside phosphotransferase type-Iii. Gene 1983, 23:331-341.
61. Van de Guchte M., Penaud S., Grimaldi C., Barbe V., Bryson K., Nicolas P., Robert C., Oztas S., Mangenot S., Couloux A., Loux V., Dervyn R., Bossy R., Bolotin A., Batto J.M., Walunas T., Gibrat J.F., Bessieres P., Weissenbach J., Ehrlich S.D., Maguin E. The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:9274-9279.
62. Whitworth D.E., Cock P.J.A. Two-component systems of the myxobacteria: structure, diversity and evolutionary relationships. Microbiology 2008, 154:360-372.
63. Winkler M.E., Hoch J.A. Essentiality, bypass, and targeting of the YycFG (VicRK) two-component regulatory system in gram-positive bacteria. Journal of Bacteriology 2008, 190:2645-2648.
64. Zotta T., Asterinou K., Rossano R., Ricciardi A., Varcamonti M., Parente E. Effect of inactivation of stress response regulators on the growth and survival of Streptococcus thermophilus Sfi39. International Journal of Food Microbiology 2009, 129:211-220.