Staphylococcus epidermidis SrrAB regulates bacterial growth and biofilm formation differently under oxic and microaerobic conditions

Journal of Bacteriology

Volumn 197, Issue 3, 2015, Pages 459-476

  Wu, Youcong ^a,b   Wu, Yang ^a   Zhu, Tao ^a,c   Han, Haiyan ^a   Liu, Huayong ^a   Xu, Tao ^a   Francois, Patrice ^d   Fischer, Adrien ^d   Bai, Li ^b   Götz, Friedrich ^e   Qu, Di ^a  

^a FUDAN UNIVERSITY   (China)

^b DALI UNIVERSITY   (China)

^c WANNAN MEDICAL COLLEGE   (China)

^d GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^e UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; CYTOCHROME; OXIDOREDUCTASE; BACTERIAL DNA; OXYGEN; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ANAEROBIC METABOLISM; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM MUTANT; BIOFILM; CELL ADHESION; CONTROLLED STUDY; DOWN REGULATION; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; ICAA GENE; ICAR GENE; IN VITRO STUDY; IN VIVO STUDY; MICROARRAY ANALYSIS; NONHUMAN; PFLBA GENE; PRIORITY JOURNAL; PROMOTER REGION; QOXB GENE; RESPIRATORY CHAIN; SRRAB GENE; STAPHYLOCOCCUS EPIDERMIDIS; TRANSCRIPTION REGULATION; UPREGULATION; AEROBIC METABOLISM; ANAEROBIC GROWTH; DRUG EFFECTS; ELECTRON TRANSPORT; GENE DELETION; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS EPIDERMIDIS;

AEROBIOSIS; ANAEROBIOSIS; BACTERIAL ADHESION; BIOFILMS; DNA, BACTERIAL; ELECTRON TRANSPORT; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE DELETION; GENE EXPRESSION PROFILING; MICROARRAY ANALYSIS; OXYGEN; POLYSACCHARIDES, BACTERIAL; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REAL-TIME POLYMERASE CHAIN REACTION; STAPHYLOCOCCUS EPIDERMIDIS; TRANSCRIPTION FACTORS;

EID: 84920767629     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02231-14     Document Type: Article

References (46)

1. Maduka-Ezeh AN, Greenwood-Quaintance KE, Karau MJ, Berbari EF, Osmon DR, Hanssen AD, Steckelberg JM, Patel R. 2012. Antimicrobial susceptibility and biofilm formation of Staphylococcus epidermidis small colony variants associated with prosthetic joint infection. Diagn Microbiol Infect Dis 74:224-229. http://dx.doi.org/10.1016/j.diagmicrobio.2012.06.029.
2. Götz F, Peters G. 2000. Colonization of medical devices by coagulasenegative staphylococci, p 55-88. In Waldvogel FA, Bisno AL (ed), Infections associated with indwelling medical devices, 3rd ed. American Society for Microbiology, Washington, DC.
3. Otto M. 2008. Staphylococcal biofilms. Curr Top Microbiol Immunol 322:207-228. http://dx.doi.org/10.1007/978-3-540-75418-3_10.
4. Götz F. 2002. Staphylococcus and biofilms. Mol Microbiol 43:1367-1378. http://dx.doi.org/10.1046/j.1365-2958.2002.02827.x.
5. Dunne WM, Jr. 2002. Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15:155-166. http://dx.doi.org/10.1128/CMR.15.2.155-166.2002.
6. Rupp ME, Fey PD, Heilmann C, Götz F. 2001. Characterization of the importance of Staphylococcus epidermidis autolysin and polysaccharide intercellular adhesin in the pathogenesis of intravascular catheterassociated infection in a rat model. J Infect Dis 183:1038-1042. http://dx.doi.org/10.1086/319279.
7. Qin Z, Ou Y, Yang L, Zhu Y, Tolker-Nielsen T, Molin S, Qu D. 2007. Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153:2083-2092. http://dx.doi.org/10.1099/mic.0.2007/006031-0.
8. Otto M. 2012. Staphylococcal infections: mechanisms of biofilm maturation and detachment as critical determinants of pathogenicity. Annu Rev Med 64:175-188. http://dx.doi.org/10.1146/annurev-med-042711-140023.
9. Periasamy S, Joo HS, Duong AC, Bach TH, Tan VY, Chatterjee SS, Cheung GY, Otto M. 2012. How Staphylococcus aureus biofilms develop their characteristic structure. Proc Natl Acad Sci USA 109:1281-1286. http://dx.doi.org/10.1073/pnas.1115006109.
10. Knobloch JK, Bartscht K, Sabottke A, Rohde H, Feucht HH, Mack D. 2001. Biofilm formation by Staphylococcus epidermidis depends on functional RsbU, an activator of the sigB operon: differential activation mechanisms due to ethanol and salt stress. J Bacteriol 183:2624-2633. http://dx.doi.org/10.1128/JB.183.8.2624-2633.2001.
11. Heilmann C, Hussain M, Peters G, Götz F. 1997. Evidence for autolysinmediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 24:1013-1024. http://dx.doi.org/10.1046/j.1365-2958.1997.4101774.x.
12. Olson ME, Garvin KL, Fey PD, Rupp ME. 2006. Adherence of Staphylococcus epidermidis to biomaterials is augmented by PIA. Clin Orthop Relat Res 451:21-24. http://dx.doi.org/10.1097/01.blo.0000229320.45416.0c.
13. Tormo MA, Marti M, Valle J, Manna AC, Cheung AL, Lasa I, Penades JR. 2005. SarA is an essential positive regulator of Staphylococcus epidermidis biofilm development. J Bacteriol 187:2348-2356. http://dx.doi.org/10.1128/JB.187.7.2348-2356.2005.
14. Zhu T, Lou Q, Wu Y, Hu J, Yu F, Qu D. 2010. Impact of the Staphylococcus epidermidis LytSR two-component regulatory system on murein hydrolase activity, pyruvate utilization and global transcriptional profile. BMC Microbiol 10:287. http://dx.doi.org/10.1186/1471-2180-10-287.
15. Lou Q, Zhu T, Hu J, Ben H, Yang J, Yu F, Liu J, Wu Y, Fischer A, Francois P, Schrenzel J, Qu D. 2011. Role of the SaeRS twocomponent regulatory system in Staphylococcus epidermidis autolysis and biofilm formation. BMC Microbiol 11:146. http://dx.doi.org/10.1186/1471-2180-11-146.
16. Wu Y, Wang J, Xu T, Liu J, Yu W, Lou Q, Zhu T, He N, Ben H, Hu J, Götz F, Qu D. 2012. The two-component signal transduction system ArlRS regulates Staphylococcus epidermidis biofilm formation in an ica-dependent manner. PLoS One 7:e40041. http://dx.doi.org/10.1371/journal.pone.0040041.
17. Sun G, Sharkova E, Chesnut R, Birkey S, Duggan MF, Sorokin A, Pujic P, Ehrlich SD, Hulett FM. 1996. Regulators of aerobic and anaerobic respiration in Bacillus subtilis. J Bacteriol 178:1374-1385.
18. Nakano MM, Zuber P, Glaser P, Danchin A, Hulett FM. 1996. Twocomponent regulatory proteins ResD-ResE are required for transcriptional activation of fnr upon oxygen limitation in Bacillus subtilis. J Bacteriol 178:3796-3802.
19. Throup JP, Zappacosta F, Lunsford RD, Annan RS, Carr SA, Lonsdale JT, Bryant AP, McDevitt D, Rosenberg M, Burnham MK. 2001. The srhSR gene pair from Staphylococcus aureus: genomic and proteomic approaches to the identification and characterization of gene function. Biochemistry 40:10392-10401. http://dx.doi.org/10.1021/bi0102959.
20. Yarwood JM, McCormick JK, Schlievert PM. 2001. Identification of a novel two-component regulatory system that acts in global regulation of virulence factors of Staphylococcus aureus. J Bacteriol 183:1113-1123. http://dx.doi.org/10.1128/JB.183.4.1113-1123.2001.
21. Pragman AA, Yarwood JM, Tripp TJ, Schlievert PM. 2004. Characterization of virulence factor regulation by SrrAB, a two-component system in Staphylococcus aureus. J Bacteriol 186:2430-2438. http://dx.doi.org/10.1128/JB.186.8.2430-2438.2004.
22. Ulrich M, Bastian M, Cramton SE, Ziegler K, Pragman AA, Bragonzi A, Memmi G, Wolz C, Schlievert PM, Cheung A, Döring G. 2007. The staphylococcal respiratory response regulator SrrAB induces ica gene transcription and polysaccharide intercellular adhesin expression, protecting Staphylococcus aureus from neutrophil killing under anaerobic growth conditions. Mol Microbiol 65:1276-1287. http://dx.doi.org/10.1111/j.1365-2958.2007.05863.x.
23. Tu Quoc PH, Genevaux P, Pajunen M, Savilahti H, Georgopoulos C, Schrenzel J, Kelley WL. 2007. Isolation and characterization of biofilm formation-defective mutants of Staphylococcus aureus. Infect Immun 75: 1079-1088. http://dx.doi.org/10.1128/IAI.01143-06.
24. Cerca N, Brooks JL, Jefferson KK. 2008. Regulation of the intercellular adhesin locus regulator (icaR) by SarA, sigmaB, and IcaR in Staphylococcus aureus. J Bacteriol 190:6530-6533. http://dx.doi.org/10.1128/JB.00482-08.
25. Rohde H, Burdelski C, Bartscht K, Hussain M, Buck F, Horstkotte MA, Knobloch JK, Heilmann C, Herrmann M, Mack D. 2005. Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol Microbiol 55:1883-1895. http://dx.doi.org/10.1111/j.1365-2958.2005.04515.x.
26. Hu J, Xu T, Zhu T, Lou Q, Wang X, Wu Y, Huang R, Liu J, Liu H, Yu F, Ding B, Huang Y, Tong W, Qu D. 2011. Monoclonal antibodies against accumulation-associated protein affect EPS biosynthesis and enhance bacterial accumulation of Staphylococcus epidermidis. PLoS One 6:e20918. http://dx.doi.org/10.1371/journal.pone.0020918.
27. Christner M, Heinze C, Busch M, Franke G, Hentschke M, Bayard Duhring S, Buttner H, Kotasinska M, Wischnewski V, Kroll G, Buck F, Molin S, Otto M, Rohde H. 2012. sarA negatively regulates Staphylococcus epidermidis biofilm formation by modulating expression of 1 MDa extracellular matrix binding protein and autolysis-dependent release of eDNA. Mol Microbiol 86:394-410. http://dx.doi.org/10.1111/j.1365-2958.2012.08203.x.
28. Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT, Ravel J, Paulsen IT, Kolonay JF, Brinkac L, Beanan M, Dodson RJ, Daugherty SC, Madupu R, Angiuoli SV, Durkin AS, Haft DH, Vamathevan J, Khouri H, Utterback T, Lee C, Dimitrov G, Jiang L, Qin H, Weidman J, Tran K, Kang K, Hance IR, Nelson KE, Fraser CM. 2005. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilmproducing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol 187:2426-2438. http://dx.doi.org/10.1128/JB.187.7.2426-2438.2005.
29. Flamm RK, Hinrichs DJ, Thomashow MF. 1984. Introduction of pAMβ1 into Listeria monocytogenes by conjugation and homology between native L. monocytogenes plasmids. Infect Immun 44:157-161.
30. Arnaud M, Chastanet A, Debarbouille M. 2004. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70:6887-6891. http://dx.doi.org/10.1128/AEM.70.11.6887-6891.2004.
31. Helle L, Kull M, Mayer S, Marincola G, Zelder ME, Goerke C, Wolz C, Bertram R. 2011. Vectors for improved Tet repressor-dependent gradual gene induction or silencing in Staphylococcus aureus. Microbiology 157: 3314-3323. http://dx.doi.org/10.1099/mic.0.052548-0.
32. Charpentier E, Anton AI, Barry P, Alfonso B, Fang Y, Novick RP. 2004. Novel cassette-based shuttle vector system for gram-positive bacteria. Appl Environ Microbiol 70:6076-6085. http://dx.doi.org/10.1128/AEM.70.10.6076-6085.2004.
33. He N, Hu J, Liu H, Zhu T, Huang B, Wang X, Wu Y, Wang W, Qu D. 2011. Enhancement of vancomycin activity against biofilms by using ultrasound-targeted microbubble destruction. Antimicrob Agents Chemother 55:5331-5337. http://dx.doi.org/10.1128/AAC.00542-11.
34. Liu Q, Fan J, Niu C, Wang D, Wang J, Wang X, Villaruz AE, Li M, Otto M, Gao Q. 2011. The eukaryotic-type serine/threonine protein kinase Stk is required for biofilm formation and virulence in Staphylococcus epidermidis. PLoS One 6:e25380. http://dx.doi.org/10.1371/journal.pone.0025380.
35. Gerke C, Kraft A, Sussmuth R, Schweitzer O, Götz F. 1998. Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J Biol Chem 273:18586-18593. http://dx.doi.org/10.1074/jbc.273.29.18586.
36. Charbonnier Y, Gettler B, Francois P, Bento M, Renzoni A, Vaudaux P, Schlegel W, Schrenzel J. 2005. A generic approach for the design of whole-genome oligoarrays, validated for genomotyping, deletion mapping and gene expression analysis on Staphylococcus aureus. BMC Genomics 6:95. http://dx.doi.org/10.1186/1471-2164-6-95.
37. Scherl A, Francois P, Charbonnier Y, Deshusses JM, Koessler T, Huyghe A, Bento M, Stahl-Zeng J, Fischer A, Masselot A, Vaezzadeh A, Galle F, Renzoni A, Vaudaux P, Lew D, Zimmermann-Ivol CG, Binz PA, Sanchez JC, Hochstrasser DF, Schrenzel J. 2006. Exploring glycopeptide-resistance in Staphylococcus aureus: a combined proteomics and transcriptomics approach for the identification of resistancerelated markers. BMC Genomics 7:296. http://dx.doi.org/10.1186/1471-2164-7-296.
38. Pragman AA, Herron-Olson L, Case LC, Vetter SM, Henke EE, Kapur V, Schlievert PM. 2007. Sequence analysis of the Staphylococcus aureus srrAB loci reveals that truncation of srrA affects growth and virulence factor expression. J Bacteriol 189:7515-7519. http://dx.doi.org/10.1128/JB.00547-07.
39. Pragman AA, Ji YD, Schlievert PM. 2007. Repression of Staphylococcus aureus SrrAB using inducible antisense srrA alters growth and virulence factor transcript levels. Biochemistry-Us 46:314-321. http://dx.doi.org/10.1021/bi0603266.
40. Cramton SE, Ulrich M, Götz F, Doring G. 2001. Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun 69:4079-4085. http://dx.doi.org/10.1128/IAI.69.6.4079-4085.2001.
41. Hammer ND, Reniere ML, Cassat JE, Zhang Y, Hirsch AO, Indriati Hood M, Skaar EP. 2013. Two heme-dependent terminal oxidases power Staphylococcus aureus organ-specific colonization of the vertebrate host. mBio 4:e00241-13. http://dx.doi.org/10.1128/mBio.00241-13.
42. Kinkel TL, Roux CM, Dunman PM, Fang FC. 2013. The Staphylococcus aureus SrrAB two-component system promotes resistance to nitrosative stress and hypoxia. mBio 4:e00696-13. http://dx.doi.org/10.1128/mBio.00696-13.
43. Fuchs S, Pane-Farre J, Kohler C, Hecker M, Engelmann S. 2007. Anaerobic gene expression in Staphylococcus aureus. J Bacteriol 189:4275-4289. http://dx.doi.org/10.1128/JB.00081-07.
44. Masalha M, Borovok I, Schreiber R, Aharonowitz Y, Cohen G. 2001. Analysis of transcription of the Staphylococcus aureus aerobic class Ib and anaerobic class III ribonucleotide reductase genes in response to oxygen. J Bacteriol 183:7260-7272. http://dx.doi.org/10.1128/JB.183.24.7260-7272.2001.
45. Leibig M, Liebeke M, Mader D, Lalk M, Peschel A, Gotz F. 2011. Pyruvate formate lyase acts as a formate supplier for metabolic processes during anaerobiosis in Staphylococcus aureus. J Bacteriol 193:952-962. http://dx.doi.org/10.1128/JB.01161-10.
46. Roca I, Ballana E, Panosa A, Torrents E, Gibert I. 2008. Fumarate and nitrate reduction (FNR)-dependent activation of the Escherichia coli anaerobic ribonucleotide reductase nrdDG promoter. Int Microbiol 11:49-56.