Biofilm extracellular DNA enhances mixed species biofilms of Staphylococcus epidermidis and Candida albicans

BMC Microbiology

Volumn 13, Issue 1, 2013, Pages

  Pammi, Mohan ^a   Liang, Rong ^a   Hicks, John ^a   Mistretta, Toni Ann ^a   Versalovic, James ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Autolysis; Biofilms; Candida; Extracellular DNA; Microarray; Mixed species; Polymicrobial; Staphylococcus

Indexed keywords

DEOXYRIBONUCLEASE; DNA;

ARTICLE; AUTOLYSIS; BIOFILM; BLOODSTREAM INFECTION; CANDIDA ALBICANS; CATHETER INFECTION; DOWN REGULATION; GENE EXPRESSION; IN VITRO STUDY; MIXED INFECTION; MORBIDITY; MORTALITY; NONHUMAN; STAPHYLOCOCCUS EPIDERMIDIS; UPREGULATION;

BACTERIA (MICROORGANISMS); CANDIDA; CANDIDA ALBICANS; MUS; STAPHYLOCOCCUS; STAPHYLOCOCCUS EPIDERMIDIS;

ADULT; ANIMALS; BIOFILMS; CANDIDA ALBICANS; CATHETER-RELATED INFECTIONS; CHILD; COINFECTION; DISEASE MODELS, ANIMAL; DNA; GENE EXPRESSION PROFILING; GENES, BACTERIAL; HUMANS; MICE; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 84887367408     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-13-257     Document Type: Article

References (50)

1. Central venous catheter removal versus in situ treatment in neonates with coagulase-negative staphylococcal bacteremia. Karlowicz MG, Furigay PJ, Croitoru DP, Buescher ES, Pediatr Infect Dis J 2002 21 1 22 27 10.1097/00006454-200201000-00005 11791093 (Pubitemid 34073953)
2. Polymicrobial bloodstream infection in pediatric patients: risk factors, microbiology, and antimicrobial management. Sutter D, Stagliano D, Braun L, Williams F, Arnold J, Ottolini M, Epstein J, Pediatr Infect Dis J 2008 27 5 400 405 10.1097/INF.0b013e31816591be 18398386
3. Intravascular catheter-related infections: new horizons and recent advances. Raad II, Hanna HA, Arch Intern Med 2002 162 8 871 878 10.1001/archinte.162.8.871 11966337 (Pubitemid 34299118)
4. Does candidemia predict threshold retinopathy of prematurity in extremely low birth weight (
5. Neonatal Candida glabrata sepsis: clinical and laboratory features compared with other Candida species. Fairchild KD, Tomkoria S, Sharp EC, Mena FV, Pediatr Infect Dis J 2002 21 1 39 43 10.1097/00006454-200201000-00009 11791097 (Pubitemid 34073957)
6. Polymicrobial bloodstream infections involving Candida species: analysis of patients and review of the literature. Klotz SA, Chasin BS, Powell B, Gaur NK, Lipke PN, Diagn Microbiol Infect Dis 2007 59 4 401 406 10.1016/j. diagmicrobio.2007.07.001 17888612 (Pubitemid 350184233)
7. Human polymicrobial infections. Brogden KA, Guthmiller JM, Taylor CE, Lancet 2005 365 9455 253 255 15652608 (Pubitemid 40138019)
8. Polymicrobial bloodstream infections among children and adolescents with central venous catheters evaluated in ambulatory care. Downes KJ, Metlay JP, Bell LM, McGowan KL, Elliott MR, Shah SS, Clin Infect Dis 2008 46 3 387 394 10.1086/525265 18181737 (Pubitemid 351263522)
9. Polymicrobial sepsis among intensive care nursery infants. Faix RG, Kovarik SM, J Perinatol 1989 9 2 131 136 2738721
10. Clinical importance of polymicrobial bacteremia. Weinstein MP, Reller LB, Murphy JR, Diagn Microbiol Infect Dis 1986 5 3 185 196 10.1016/0732-8893(86) 90001-5 3757473 (Pubitemid 16011871)
11. Case mortality in polymicrobial bloodstream infections. McKenzie FE, J Clin Epidemiol 2006 59 7 760 761 10.1016/j.jclinepi.2005.12.009 16765282 (Pubitemid 43825725)
12. Protection by Candida albicans of Staphylococcus aureus in the establishment of dual infection in mice. Carlson E, Johnson G, Infect Immun 1985 50 3 655 659 3905609 (Pubitemid 16216854)
13. Effect of strain of Staphylococcus aureus on synergism with Candida albicans resulting in mouse mortality and morbidity. Carlson E, Infect Immun 1983 42 1 285 292 6352497 (Pubitemid 13009841)
14. Synergistic effect of Candida albicans and Staphylococcus aureus on mouse mortality. Carlson E, Infect Immun 1982 38 3 921 924 7152678 (Pubitemid 13206234)
15. Neonatal coinfection model of coagulase-negative Staphylococcus (Staphylococcus epidermidis) and Candida albicans: fluconazole prophylaxis enhances survival and growth. Venkatesh MP, Pham D, Fein M, Kong L, Weisman LE, Antimicrob Agents Chemother 2007 51 4 1240 1245 10.1128/AAC.01298-06 17261622 (Pubitemid 46586800)
16. Mixed species biofilms of Candida albicans and Staphylococcus epidermidis. Adam B, Baillie GS, Douglas LJ, J Med Microbiol 2002 51 4 344 349 11926741 (Pubitemid 34252657)
17. Interactions of Candida albicans with other Candida spp. and bacteria in the biofilms. El-Azizi MA, Starks SE, Khardori N, J Appl Microbiol 2004 96 1067 1073 10.1111/j.1365-2672.2004.02213.x 15078523 (Pubitemid 38582153)
18. The biofilm matrix. Flemming HC, Wingender J, Nat Rev Microbiol 2010 8 9 623 633 20676145
19. Extracellular DNA required for bacterial biofilm formation. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS, Science 2002 295 5559 1487 10.1126/science.295.5559.1487 11859186 (Pubitemid 34173996)
20. Extracellular DNA in single- and multiple-species unsaturated biofilms. Steinberger RE, Holden PA, Appl Environ Microbiol 2005 71 9 5404 5410 10.1128/AEM.71.9.5404-5410.2005 16151131 (Pubitemid 41338275)
21. Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Izano EA, Amarante MA, Kher WB, Kaplan JB, Appl Environ Microbiol 2008 74 2 470 476 10.1128/AEM.02073-07 18039822
22. Pseudomonas-Candida interactions: an ecological role for virulence factors. Hogan DA, Kolter R, Science 2002 296 5576 2229 2232 10.1126/science.1070784 12077418 (Pubitemid 34680309)
23. Microbial interactions and differential protein expression in Staphylococcus aureus -Candida albicans dual-species biofilms. Peters BM, Jabra-Rizk MA, Scheper MA, Leid JG, Costerton JW, Shirtliff ME, FEMS Immunol Med Microbiol 2010 59 3 493 503 20608978
24. Farnesol decreases biofilms of Staphylococcus epidermidis and exhibits synergy with nafcillin and vancomycin. Pammi M, Liang R, Hicks JM, Barrish J, Versalovic J, Pediatr Res 2011 70 6 578 583 10.1203/PDR.0b013e318232a984 21857375
25. The Staphylococcus aureus lrgAB operon modulates murein hydrolase activity and penicillin tolerance. Groicher KH, Firek BA, Fujimoto DF, Bayles KW, J Bacteriol 2000 182 7 1794 1801 10.1128/JB.182.7.1794-1801.2000 10714982 (Pubitemid 30165364)
26. Characterization of the Staphylococcus aureus CidR regulon: elucidation of a novel role for acetoin metabolism in cell death and lysis. Yang SJ, Dunman PM, Projan SJ, Bayles KW, Mol Microbiol 2006 60 2 458 468 10.1111/j.1365-2958. 2006.05105.x 16573694
27. The biological role of death and lysis in biofilm development. Bayles KW, Nat Rev Microbiol 2007 5 9 721 726 10.1038/nrmicro1743 17694072 (Pubitemid 47278865)
28. The Staphylococcus aureus LytSR two-component regulatory system affects biofilm formation. Sharma-Kuinkel BK, Mann EE, Ahn JS, Kuechenmeister LJ, Dunman PM, Bayles KW, J Bacteriol 2009 191 15 4767 4775 10.1128/JB.00348-09 19502411
29. Analysis of genetic elements controlling Staphylococcus aureus lrgAB expression: potential role of DNA topology in SarA regulation. Fujimoto DF, Brunskill EW, Bayles KW, J Bacteriol 2000 182 17 4822 4828 10.1128/JB.182.17. 4822-4828.2000 10940023 (Pubitemid 30641804)
30. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Rice KC, Mann EE, Endres JL, Weiss EC, Cassat JE, Smeltzer MS, Bayles KW, Proc Natl Acad Sci USA 2007 104 19 8113 8118 10.1073/pnas.0610226104 17452642 (Pubitemid 47185884)
31. Staphylococcus aureus requires cardiolipin for survival under conditions of high salinity. Tsai M, Ohniwa RL, Kato Y, Takeshita SL, Ohta T, Saito S, Hayashi H, Morikawa K, BMC Microbiol 2011 11 13 10.1186/1471-2180-11-13 21241511
32. Characterization of Staphylococcus aureus cardiolipin synthases 1 and 2 and their contribution to accumulation of cardiolipin in stationary phase and within phagocytes. Koprivnjak T, Zhang D, Ernst CM, Peschel A, Nauseef WM, Weiss JP, J Bacteriol 2011 193 16 4134 4142 10.1128/JB.00288-11 21665977
33. The physiology and collective recalcitrance of microbial biofilm communities. Gilbert P, Maira-Litran T, McBain AJ, Rickard AH, Whyte FW, Adv Microb Physiol 2002 46 202 256 12073654
34. Maximal transcription of aur (aureolysin) and sspA (serine protease) in Staphylococcus aureus requires staphylococcal accessory regulator R (sarR) activity. Gustafsson E, Oscarsson J, FEMS Microbiol Lett 2008 284 2 158 164 10.1111/j.1574-6968.2008.01198.x 18576947 (Pubitemid 351813419)
35. Crystal structure of the SarR protein from Staphylococcus aureus. Liu Y, Manna A, Li R, Martin WE, Murphy RC, Cheung AL, Zhang G, Proc Natl Acad Sci USA 2001 98 12 6877 6882 10.1073/pnas.121013398 11381122 (Pubitemid 32538310)
36. Characterization of sarR, a modulator of sar expression in Staphylococcus aureus. Manna A, Cheung AL, Infect Immun 2001 69 2 885 896 10.1128/IAI.69.2. 885-896.2001 11159982 (Pubitemid 32109553)
37. Staphylococci express a receptor for human transferrin: identification of a 42-kilodalton cell wall transferrin-binding protein. Modun B, Kendall D, Williams P, Infect Immun 1994 62 9 3850 3858 8063401 (Pubitemid 24264329)
38. The Staphylococcus aureus and Staphylococcus epidermidis transferrin-binding proteins are expressed in vivo during infection. Modun BJ, Cockayne A, Finch R, Williams P, Microbiology 1998 144 Pt 4 1005 1012 9579074 (Pubitemid 28187926)
39. Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. Mann EE, Rice KC, Boles BR, Endres JL, Ranjit D, Chandramohan L, Tsang LH, Smeltzer MS, Horswill AR, Bayles KW, PLoS One 2009 4 6 5822 10.1371/journal.pone.0005822 19513119
40. Extracellular DNA in biofilms. Montanaro L, Poggi A, Visai L, Ravaioli S, Campoccia D, Speziale P, Arciola CR, Int J Artif Organs 2011 34 9 824 831 10.5301/ijao.5000051 22094562
41. Extracellular DNA-dependent biofilm formation by Staphylococcus epidermidis RP62A in response to subminimal inhibitory concentrations of antibiotics. Kaplan JB, Jabbouri S, Sadovskaya I, Res Microbiol 2011 162 5 535 541 10.1016/j.resmic.2011.03.008 21402153
42. Identification and molecular characterization of a putative regulatory locus that affects autolysis in Staphylococcus aureus. Brunskill EW, Bayles KW, J Bacteriol 1996 178 3 611 618 8550490 (Pubitemid 26036630)
43. A LysR-type regulator, CidR, is required for induction of the Staphylococcus aureus cidABC operon. Yang SJ, Rice KC, Brown RJ, Patton TG, Liou LE, Park YH, Bayles KW, J Bacteriol 2005 187 17 5893 5900 10.1128/JB.187.17. 5893-5900.2005 16109930 (Pubitemid 41262786)
44. Impact of the Staphylococcus epidermidis LytSR two-component regulatory system on murein hydrolase activity, pyruvate utilization and global transcriptional profile. Zhu T, Lou Q, Wu Y, Hu J, Yu F, Qu D, BMC Microbiol 2010 10 287 10.1186/1471-2180-10-287 21073699
45. Role of the SaeRS two-component regulatory system in Staphylococcus epidermidis autolysis and biofilm formation. Lou Q, Zhu T, Hu J, Ben H, Yang J, Yu F, Liu J, Wu Y, Fischer A, Francois P, et al. BMC Microbiol 2011 11 146 10.1186/1471-2180-11-146 21702925
46. Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Qin Z, Ou Y, Yang L, Zhu Y, Tolker-Nielsen T, Molin S, Qu D, Microbiology 2007 153 Pt 7 2083 2092 17600053 (Pubitemid 47074063)
47. Analysis of a marine phototrophic biofilm by confocal laser scanning microscopy using the new image quantification software PHLIP. Mueller LN, de Brouwer JF, Almeida JS, Stal LJ, Xavier JB, BMC Ecol 2006 6 1 10.1186/1472-6785-6-1 16412253
48. OligoArray 2.0: design of oligonucleotide probes for DNA microarrays using a thermodynamic approach. Rouillard JM, Zuker M, Gulari E, Nucleic Acids Res 2003 31 12 3057 3062 10.1093/nar/gkg426 12799432 (Pubitemid 37441764)
49. Development and evaluation of different normalization strategies for gene expression studies in Candida albicans biofilms by real-time PCR. Nailis H, Coenye T, Van Nieuwerburgh F, Deforce D, Nelis HJ, BMC Mol Biol 2006 7 25 10.1186/1471-2199-7-25 16889665 (Pubitemid 44309027)
50. Characteristics of biofilm formation by Candida albicans. Ramage G, Vandewalle K, Wickes BL, Lopez-Ribot JL, Rev Iberoam Micol 2001 18 4 163 170 15496122 (Pubitemid 34116636)