Fungal β-1,3-Glucan Increases Ofloxacin Tolerance of Escherichia coli in a Polymicrobial E. coli/Candida albicans Biofilm

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 6, 2015, Pages 3052-3058

  De Brucker, Katrijn ^a   Tan, Yulong ^a   Vints, Katlijn ^a   De Cremer, Kaat ^a,b   Braem, Annabel ^a   Verstraeten, Natalie ^a   Michiels, Jan ^a   Vleugels, Jef ^a   Cammue, Bruno P A ^a,b   Thevissen, Karin ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOTERICIN B; BETA 1,3 GLUCAN; CASPOFUNGIN; KANAMYCIN; LAMINARAN; OFLOXACIN; ANTIFUNGAL AGENT; BETA GLUCAN; BETA-1,3-GLUCAN;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIUM CULTURE; BIOFILM; CANDIDA ALBICANS; COLONY FORMING UNIT; DRUG TOLERANCE; ENZYME DEGRADATION; ESCHERICHIA COLI K 12; EXTRACELLULAR MATRIX; FUNGUS CULTURE; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; ANTIFUNGAL RESISTANCE; DRUG EFFECTS; ESCHERICHIA COLI; METABOLISM; ULTRASTRUCTURE;

ANTIFUNGAL AGENTS; BETA-GLUCANS; BIOFILMS; CANDIDA ALBICANS; DRUG RESISTANCE, FUNGAL; ESCHERICHIA COLI; OFLOXACIN;

EID: 84980367675     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.04650-14     Document Type: Article

References (49)

1. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322. http://dx.doi.org/10.1126/science.284.5418.1318.
2. Douglas LJ. 2003. Candida biofilms and their role in infection. Trends Microbiol 11:30-36. http://dx.doi.org/10.1016/S0966-842X(02)00002-1.
3. Edwards SJ, Kjellerup BV. 2013. Applications of biofilms in bioremediation and biotransformation of persistent organic pollutants, pharmaceuticals/personal care products, and heavy metals. Appl Microbiol Biotechnol 97:9909-9921. http://dx.doi.org/10.1007/s00253-013-5216-z.
4. Calderon K, Gonzalez-Martinez A, Gomez-Silvan C, Osorio F, Rodelas B, Gonzalez-Lopez J. 2013. Archaeal diversity in biofilm technologies applied to treat urban and industrial wastewater: recent advances and future prospects. Int J Mol Sci 14:18572-18598. http://dx.doi.org/10.3390/ijms140918572.
5. Gutierrez-Correa M, Ludena Y, Ramage G, Villena GK. 2012. Recent advances on filamentous fungal biofilms for industrial uses. Appl Biochem Biotechnol 167:1235-1253. http://dx.doi.org/10.1007/s12010-012-9555-5.
6. Fanning S, Mitchell AP. 2012. Fungal biofilms. PLoS Pathog 8:e1002585. http://dx.doi.org/10.1371/journal.ppat.1002585.
7. Beloin C, Roux A, Ghigo JM. 2008. Escherichia coli biofilms. Curr Top Microbiol Immunol 322:249-289.
8. Wood TK. 2009. Insights on Escherichia coli biofilm formation and inhibition from whole-transcriptome profiling. Environ Microbiol 11:1-15. http://dx.doi.org/10.1111/j.1462-2920.2008.01768.x.
9. Ramage G, Vandewalle K, Lopez-Ribot JL, Wickes BL. 2002. The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans. FEMS Microbiol Lett 214:95-100. http://dx.doi.org/10.1111/j.1574-6968.2002.tb11330.x.
10. Nobile CJ, Andes DR, Nett JE, Smith FJ, Yue F, Phan QT, Edwards JE, Filler SG, Mitchell AP. 2006. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog 2:e63. http://dx.doi.org/10.1371/journal.ppat.0020063.
11. Nobile CJ, Mitchell AP. 2005. Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr Biol 15:1150-1155. http://dx.doi.org/10.1016/j.cub.2005.05.047.
12. Nobile CJ, Fox EP, Nett JE, Sorrells TR, Mitrovich QM, Hernday AD, Tuch BB, Andes DR, Johnson AD. 2012. A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148:126-138. http://dx.doi.org/10.1016/j.cell.2011.10.048.
13. Elias S, Banin E. 2012. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev 36:990-1004. http://dx.doi.org/10.1111/j.1574-6976.2012.00325.x.
14. Holmes AR, McNab R, Jenkinson HF. 1996. Candida albicans binding to the oral bacterium Streptococcus gordonii involves multiple adhesinreceptor interactions. Infect Immun 64:4680-4685.
15. Holmes AR, Gopal PK, Jenkinson HF. 1995. Adherence of Candida albicans to a cell surface polysaccharide receptor on Streptococcus gordonii. Infect Immun 63:1827-1834.
16. Hogan DA, Vik A, Kolter R. 2004. A Pseudomonas aeruginosa quorumsensing molecule influences Candida albicans morphology. Mol Microbiol 54:1212-1223. http://dx.doi.org/10.1111/j.1365-2958.2004.04349.x.
17. Brand A, Barnes JD, Mackenzie KS, Odds FC, Gow NA. 2008. Cell wall glycans and soluble factors determine the interactions between the hyphae of Candida albicans and Pseudomonas aeruginosa. FEMS Microbiol Lett 287:48-55. http://dx.doi.org/10.1111/j.1574-6968.2008.01301.x.
18. Holcombe LJ, McAlester G, Munro CA, Enjalbert B, Brown AJ, Gow NA, Ding C, Butler G, O'Gara F, Morrissey JP. 2010. Pseudomonas aeruginosa secreted factors impair biofilm development in Candida albicans. Microbiology 156:1476-1486. http://dx.doi.org/10.1099/mic.0.037549-0.
19. Morales DK, Jacobs NJ, Rajamani S, Krishnamurthy M, Cubillos-Ruiz JR, Hogan DA. 2010. Antifungal mechanisms by which a novel Pseudomonas aeruginosa phenazine toxin kills Candida albicans in biofilms. Mol Microbiol 78:1379-1392. http://dx.doi.org/10.1111/j.1365-2958.2010.07414.x.
20. Burmolle M, Webb JS, Rao D, Hansen LH, Sorensen SJ, Kjelleberg S. 2006. Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol 72:3916-3923. http://dx.doi.org/10.1128/AEM.03022-05.
21. Harriott MM, Noverr MC. 2009. Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother 53:3914-3922. http://dx.doi.org/10.1128/AAC.00657-09.
22. Adam B, Baillie GS, Douglas LJ. 2002. Mixed species biofilms of Candida albicans and Staphylococcus epidermidis. J Med Microbiol 51:344-349.
23. Ryan RP, Fouhy Y, Garcia BF, Watt SA, Niehaus K, Yang L, Tolker-Nielsen T, Dow JM. 2008. Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol Microbiol 68:75-86. http://dx.doi.org/10.1111/j.1365-2958.2008.06132.x.
24. Thein ZM, Smaranayake YH, Smaranayake LP. 2007. Dietary sugars, serum and the biocide chlorhexidine digluconate modify the population and structural dynamics of mixed Candida albicans and Escherichia coli biofilms. APMIS 115:1241-1251. http://dx.doi.org/10.1111/j.1600-0643.2007.00735.x.
25. Pastar I, Nusbaum AG, Gil J, Patel SB, Chen J, Valdes J, Stojadinovic O, Plano LR, Tomic-Canic M, Davis SC. 2013. Interactions of methicillin resistant Staphylococcus aureus USA300 and Pseudomonas aeruginosa in polymicrobial wound infection. PLoS One 8:e56846. http://dx.doi.org/10.1371/journal.pone.0056846.
26. Peters BM, Noverr MC. 2013. Candida albicans-Staphylococcus aureus polymicrobial peritonitis modulates host innate immunity. Infect Immun 81:2178-2189. http://dx.doi.org/10.1128/IAI.00265-13.
27. Peters BM, Jabra-Rizk MA, Scheper MA, Leid JG, Costerton JW, Shirtliff ME. 2010. Microbial interactions and differential protein expression in Staphylococcus aureus-Candida albicans dual-species biofilms. FEMS Immunol Med Microbiol 59:493-503. http://dx.doi.org/10.1111/j.1574-695X.2010.00710.x.
28. Vandecandelaere I, Matthijs N, Nelis HJ, Depuydt P, Coenye T. 2013. The presence of antibiotic-resistant nosocomial pathogens in endotracheal tube biofilms and corresponding surveillance cultures. Pathog Dis 69:142-148. http://dx.doi.org/10.1111/2049-632X.12100.
29. Samaranayake YH, Bandara HM, Cheung BP, Yau J Y, Yeung SK, Samaranayake LP. 2014. Enteric Gram-negative bacilli suppress Candida biofilms on Foley urinary catheters. APMIS 122:47-58. http://dx.doi.org/10.1111/apm.12098.
30. Levison ME, Pitsakis PG. 1987. Susceptibility to experimental Candida albicans urinary tract infection in the rat. J Infect Dis 155:841-846. http://dx.doi.org/10.1093/infdis/155.5.841.
31. Burd RS, Raymond CS, Dunn DL. 1992. Endotoxin promotes synergistic lethality during concurrent Escherichia coli and Candida albicans infection. J Surg Res 52:537-542. http://dx.doi.org/10.1016/0022-4804 (92)90125-J.
32. Klaerner HG, Uknis ME, Acton RD, Dahlberg PS, Carlone-Jambor C, Dunn DL. 1997. Candida albicans and Escherichia coli are synergistic pathogens during experimental microbial peritonitis. J Surg Res 70:161-165. http://dx.doi.org/10.1006/jsre.1997.5110.
33. Kuhn DM, George T, Chandra J, Mukherjee PK, Ghannoum MA. 2002. Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob Agents Chemother 46:1773-1780. http://dx.doi.org/10.1128/AAC.46.6.1773-1780.2002.
34. Fonzi WA, Irwin MY. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134:717-728.
35. Nobile CJ, Nett JE, Hernday AD, Homann OR, Deneault JS, Nantel A, and Es DR, Johnson AD, Mitchell AP. 2009. Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol 7:e1000133. http://dx.doi.org/10.1371/journal.pbio.1000133.
36. Bachmann BJ. 1972. Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol Rev 36:525-557.
37. Al-Fattani MA, Douglas LJ. 2006. Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J Med Microbiol 55:999-1008. http://dx.doi.org/10.1099/jmm.0.46569-0.
38. Nett J, Lincoln L, Marchillo K, Massey R, Holoyda K, Hoff B, Van-Handel M, and Es D. 2007. Putative role of beta-1, 3 glucans in Candida albicans biofilm resistance. Antimicrob Agents Chemother 51:510-520. http://dx.doi.org/10.1128/AAC.01056-06.
39. Zarnowski R, Westler WM, Lacmbouh GA, Marita JM, Bothe JR, Bernhardt J, Lounes-Hadj SA, Fontaine J, Sanchez H, Hatfield RD, Ntambi JM, Nett JE, Mitchell AP, And es DR. 2014. Novel entries in a fungal biofilm matrix encyclopedia. mBio 5:e01333-14. http://dx.doi.org/10.1128/mBio.01333-14.
40. Lal P, Sharma D, Pruthi P, Pruthi V. 2010. Exopolysaccharide analysis of biofilm-forming Candida albicans. J Appl Microbiol 109:128-136. http://dx.doi.org/10.1111/j.1365-2672.2009.04634.x.
41. Bandara HM, Yau JY, Watt RM, Jin LJ, Samaranayake LP. 2009. Escherichia coli and its lipopolysaccharide modulate in vitro Candida biofilm formation. J Med Microbiol 58:1623-1631. http://dx.doi.org/10.1099/jmm.0.012989-0.
42. Thein ZM, Samaranayake YH, Samaranayake LP. 2006. Effect of oral bacteria on growth and survival of Candida albicans biofilms. Arch Oral Biol 51:672-680. http://dx.doi.org/10.1016/j.archoralbio.2006.02.005.
43. Kart D, Tavernier S, Van AH, Nelis HJ, Coenye T. 2014. Activity of disinfectants against multispecies biofilms formed by Staphylococcus aureus, Candida albicans and Pseudomonas aeruginosa. Biofouling 30:377-383. http://dx.doi.org/10.1080/08927014.2013.878333.
44. Sadovskaya I, Vinogradov E, Li J, Hachani A, Kowalska K, Filloux A. 2010. High-level antibiotic resistance in Pseudomonas aeruginosa biofilm: the ndvB gene is involved in the production of highly glycerolphosphorylated beta-(1-3)-glucans, which bind aminoglycosides. Glycobiology 20:895-904. http://dx.doi.org/10.1093/glycob/cwq047.
45. Mah TF, Pitts B, Pellock B, Walker GC, Stewart PS, O'Toole GA. 2003. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:306-310. http://dx.doi.org/10.1038/nature02122.
46. Vediyappan G, Rossignol T, d'Enfert C. 2010. Interaction of Candida albicans biofilms with antifungals: transcriptional response and binding of antifungals to beta-glucans. Antimicrob Agents Chemother 54:2096-2111. http://dx.doi.org/10.1128/AAC.01638-09.
47. Nett JE, Sanchez H, Cain MT, and Es DR. 2010. Genetic basis of Candida biofilm resistance due to drug-sequestering matrix glucan. J Infect Dis 202:171-175. http://dx.doi.org/10.1086/651200.
48. Taff HT, Nett JE, Zarnowski R, Ross KM, Sanchez H, Cain MT, Hamaker J, Mitchell AP, and Es DR. 2012. A Candida biofilm-induced pathway for matrix glucan delivery: implications for drug resistance. PLoS Pathog 8:e1002848. http://dx.doi.org/10.1371/journal.ppat.1002848.
49. Jefferson KK, Goldmann DA, Pier GB. 2005. Use of confocal microscopy to analyze the rate of vancomycin penetration through Staphylococcus aureus biofilms. Antimicrob Agents Chemother 49:2467-2473. http://dx.doi.org/10.1128/AAC.49.6.2467-2473.2005.