SOS response activation and competence development are antagonistic mechanisms in Streptococcus thermophilus

Journal of Bacteriology

Volumn 195, Issue 4, 2013, Pages 696-707

  Boutry, Céline ^a   Delplace, Brigitte ^a   Clippe, André ^a   Fontaine, Laetitia ^a   Hols, Pascal ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

MITOMYCIN; NORFLOXACIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIUM COMPETENCE; CONTROLLED STUDY; DNA INTEGRATION; DNA RECOMBINATION; DNA REPAIR; DOWN REGULATION; GENE EXPRESSION; GENETIC TRANSFORMATION; NEGATIVE FEEDBACK; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; STREPTOCOCCUS THERMOPHILUS; STRESS;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DNA DAMAGE; DNA TRANSFORMATION COMPETENCE; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; MITOMYCIN; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, BACTERIAL; SIGNAL TRANSDUCTION; SOS RESPONSE (GENETICS); SPECIES SPECIFICITY; STREPTOCOCCUS THERMOPHILUS; TRANSCRIPTOME;

EID: 84873528806     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01605-12     Document Type: Article

References (44)

1. Hols P, Hancy F, Fontaine L, Grossiord B, Prozzi D, Leblond-Bourget N, Decaris B, Bolotin A, Delorme C, Dusko Erlich S, Guedon E, Monnet V, Renault P, Kleerebezem M. 2005. New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol. Rev. 29:435-463.
2. Bolotin A, Quinquis B, Renault P, Sorokin A, Ehrlich SD, Kulakauskas S, Lapidus A, Goltsman E, Mazur M, Pusch GD, 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. 2004. Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat. Biotechnol. 22:1554-1558.
3. Fontaine L, Boutry C, de Frahan MH, Delplace B, Fremaux C, Horvath P, Boyaval P, Hols P. 2010. A novel pheromone quorum-sensing system controls the development of natural competence in Streptococcus thermophilus and Streptococcus salivarius. J. Bacteriol. 192:1444-1454.
4. Gardan R, Besset C, Guillot A, Gitton C, Monnet V. 2009. The oligopeptide transport system is essential for the development of natural competence in Streptococcus thermophilus strain LMD-9. J. Bacteriol. 191: 4647-4655.
5. Boutry C, Wahl A, Delplace B, Clippe A, Fontaine L, Hols P. 2012. Adaptor protein MecA is a negative regulator of the expression of late competence genes in Streptococcus thermophilus. J. Bacteriol. 194:1777-1788.
6. Peterson SN, Sung CK, Cline R, Desai BV, Snesrud EC, Luo P, Walling J, Li H, Mintz M, Tsegaye G, Burr PC, Do Y, Ahn S, Gilbert J, Fleischmann RD, Morrison DA. 2004. Identification of competence pheromone responsive genes in Streptococcus pneumoniae by use of DNA microarrays. Mol. Microbiol. 51:1051-1070.
7. Johnsborg O, Havarstein LS. 2009. Regulation of natural genetic transformation and acquisition of transforming DNA in Streptococcus pneumoniae. FEMS Microbiol. Rev. 33:627-642.
8. Claverys JP, Prudhomme M, Martin B. 2006. Induction of competence regulons as a general response to stress in gram-positive bacteria. Annu. Rev. Microbiol. 60:451-475.
9. Prudhomme M, Attaiech L, Sanchez G, Martin B, Claverys JP. 2006. Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae. Science 313:89-92.
10. Charpentier X, Kay E, Schneider D, Shuman HA. 2011. Antibiotics and UV radiation induce competence for natural transformation in Legionella pneumophila. J. Bacteriol. 193:1114-1121.
11. Dorer MS, Fero J, Salama NR. 2010. DNA damage triggers genetic exchange in Helicobacter pylori. PLoS Pathog. 6:e1001026.
12. Erill I, Campoy S, Barbe J. 2007. Aeons of distress: an evolutionary perspective on the bacterial SOS response. FEMS Microbiol. Rev. 31:637-656.
13. Brent R, Ptashne M. 1981. Mechanism of action of the lexA gene product. Proc. Natl. Acad. Sci. U. S. A. 78:4204-4208.
14. Little JW, Mount DW, Yanisch-Perron CR. 1981. Purified lexA protein is a repressor of the recA and lexA genes. Proc. Natl. Acad. Sci. U. S. A. 78:4199-4203.
15. Little JW. 1984. Autodigestion of lexA and phage lambda repressors. Proc. Natl. Acad. Sci. U. S. A. 81:1375-1379.
16. Fernandez De Henestrosa AR, Ogi T, Aoyagi S, Chafin D, Hayes JJ, Ohmori H, Woodgate R. 2000. Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol. Microbiol. 35:1560-1572.
17. Lesca C, Petit C, Defais M. 1991. UV induction of LexA independent proteins which could be involved in SOS repair. Biochimie 73:407-409.
18. Jiang Q, Karata K, Woodgate R, Cox MM, Goodman MF. 2009. The active form ofDNApolymerase V isUmuD=(2)C-RecA-ATP. Nature 460: 359-363.
19. Reuven NB, Arad G, Maor-Shoshani A, Livneh Z. 1999. The mutagenesis protein UmuC is a DNA polymerase activated by UmuD=, RecA, and SSB and is specialized for translesion replication. J. Biol. Chem. 274: 31763-31766.
20. Au N, Kuester-Schoeck E, Mandava V, Bothwell LE, Canny SP, Chachu K, Colavito SA, Fuller SN, Groban ES, Hensley LA, O'Brien TC, Shah A, Tierney JT, Tomm LL, O'Gara TM, Goranov AI, Grossman AD, Lovett CM. 2005. Genetic composition of the Bacillus subtilis SOS system. J. Bacteriol. 187:7655-7666.
21. Savijoki K, Ingmer H, Frees D, Vogensen FK, Palva A, Varmanen P. 2003. Heat and DNA damage induction of the LexA-like regulator HdiR from Lactococcus lactis is mediated by RecA and ClpP. Mol. Microbiol. 50:609-621.
22. Varhimo E, Savijoki K, Jalava J, Kuipers OP, Varmanen P. 2007. Identification of a novel streptococcal gene cassette mediating SOS mutagenesis in Streptococcus uberis. J. Bacteriol. 189:5210-5222.
23. Sambrook J, Fritsch E, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
24. Letort C, Juillard V. 2001. Development of a minimal chemically-defined medium for the exponential growth of Streptococcus thermophilus. J. Appl. Microbiol. 91:1023-1029.
25. Fontaine L, Dandoy D, Boutry C, Delplace B, de Frahan MH, Fremaux C, Horvath P, Boyaval P, Hols P. 2010. Development of a versatile procedure based on natural transformation for marker-free targeted genetic modification in Streptococcus thermophilus. Appl. Environ. Microbiol. 76:7870-7877.
26. Dower WJ, Miller JF, Ragsdale CW. 1988. High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 16:6127-6145.
27. Ferain T, Hobbs JN, Jr, Richardson J, Bernard N, Garmyn D, Hols P, Allen NE, Delcour J. 1996. Knockout of the two ldh genes has a major impact on peptidoglycan precursor synthesis in Lactobacillus plantarum. J. Bacteriol. 178:5431-5437.
28. Blomqvist T, Steinmoen H, Havarstein LS. 2006. Natural genetic transformation: a novel tool for efficient genetic engineering of the dairy bacterium Streptococcus thermophilus. Appl. Environ. Microbiol. 72:6751-6756.
29. Fontaine L, Boutry C, Guedon E, Guillot A, Ibrahim M, Grossiord B, Hols P. 2007. Quorum-sensing regulation of the production of Blp bacteriocins in Streptococcus thermophilus. J. Bacteriol. 189:7195-7205.
30. Mortier-Barriere I, de Saizieu A, Claverys JP, Martin B. 1998. Competence- specific induction of recA is required for full recombination proficiency during transformation in Streptococcus pneumoniae. Mol. Microbiol. 27:159-170.
31. Sutton MD, Smith BT, Godoy VG, Walker GC. 2000. The SOS response: recent insights into umuDC-dependent mutagenesis and DNA damage tolerance. Annu. Rev. Genet. 34:479-497.
32. Beaber JW, Hochhut B, Waldor MK. 2004. SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427:72-74.
33. Phillips I, Culebras E, Moreno F, Baquero F. 1987. Induction of the SOS response by new 4-quinolones. J. Antimicrob. Chemother. 20:631-638.
34. Drlica K, Zhao X. 1997. DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol. Mol. Biol. Rev. 61:377-392.
35. Drlica K. 1999. Mechanism of fluoroquinolone action. Curr. Opin. Microbiol. 2:504-508.
36. Kowalczykowski SC. 1991. Biochemistry of genetic recombination: energetics and mechanism of DNA strand exchange. Annu. Rev. Biophys. Biophys. Chem. 20:539-575.
37. Redfield RJ. 1993. Evolution of natural transformation: testing the DNA repair hypothesis in Bacillus subtilis and Haemophilus influenzae. Genetics 133:755-761.
38. Raymond-Denise A, Guillen N. 1991. Identification of dinR, a DNA damage-inducible regulator gene of Bacillus subtilis. J. Bacteriol. 173: 7084-7091.
39. Martin B, Garcia P, Castanie MP, Claverys JP. 1995. The recA gene of Streptococcus pneumoniae is part of a competence-induced operon and controls lysogenic induction. Mol. Microbiol. 15:367-379.
40. Turlan C, Prudhomme M, Fichant G, Martin B, Gutierrez C. 2009. SpxA1, a novel transcriptional regulator involved in X-state (competence) development in Streptococcus pneumoniae. Mol. Microbiol. 73:492-506.
41. Zhang Y, Nakano S, Choi SY, Zuber P. 2006. Mutational analysis of the Bacillus subtilis RNA polymerase alpha C-terminal domain supports the interference model of Spx-dependent repression. J. Bacteriol. 188:4300-4311.
42. Schultz D, Wolynes PG, Ben Jacob E, Onuchic JN. 2009. Deciding fate in adverse times: sporulation and competence in Bacillus subtilis. Proc. Natl. Acad. Sci. U. S. A. 106:21027-21034.
43. Law J, Buist G, Haandrikman A, Kok J, Venema G, Leenhouts K. 1995. A system to generate chromosomal mutations in Lactococcus lactis which allows fast analysis of targeted genes. J. Bacteriol. 177:7011-7018.
44. Fleuchot B, Gitton C, Guillot A, Vidic J, Nicolas P, Besset C, Fontaine L, Hols P, Leblond-Bourget N, Monnet V, Gardan R. 2011. Rgg proteins associated with internalized small hydrophobic peptides: a new quorumsensing mechanism in streptococci. Mol. Microbiol. 80:1102-1119.