Anaerobic bacteria grow within candida albicans biofilms and induce biofilm formation in suspension cultures

Current Biology

Volumn 24, Issue 20, 2014, Pages 2411-2416

  Fox, Emily P ^a   Cowley, Elise S ^b,c   Nobile, Clarissa J ^a,d   Hartooni, Nairi ^a   Newman, Dianne K ^b,c   Johnson, Alexander D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b California Institute of Technology   (United States)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAEROBIC BACTERIUM; ANAEROBIC GROWTH; BIOFILM; CANDIDA ALBICANS; CLASSIFICATION; COCULTURE; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGICAL EXAMINATION; PHYSIOLOGY;

ANAEROBIOSIS; BACTERIA, ANAEROBIC; BIOFILMS; CANDIDA ALBICANS; COCULTURE TECHNIQUES; MICROBIOLOGICAL TECHNIQUES;

EID: 84908318110     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2014.08.057     Document Type: Article

References (45)

1. D.C. Savage Microbial ecology of the gastrointestinal tract Annu. Rev. Microbiol. 31 1977 107 133
2. P.B. Eckburg, E.M. Bik, C.N. Bernstein, E. Purdom, L. Dethlefsen, M. Sargent, S.R. Gill, K.E. Nelson, and D.A. Relman Diversity of the human intestinal microbial flora Science 308 2005 1635 1638
3. D. López, H. Vlamakis, and R. Kolter Biofilms Cold Spring Harb. Perspect. Biol. 2 2010 a000398
4. R. Kolter, and E.P. Greenberg Microbial sciences: the superficial life of microbes Nature 441 2006 300 302
5. R.M. Donlan, and J.W. Costerton Biofilms: survival mechanisms of clinically relevant microorganisms Clin. Microbiol. Rev. 15 2002 167 193
6. R. Wolcott, J.W. Costerton, D. Raoult, and S.J. Cutler The polymicrobial nature of biofilm infection Clin. Microbiol. Infect. 19 2013 107 112
7. I.D. Iliev, V.A. Funari, K.D. Taylor, Q. Nguyen, C.N. Reyes, S.P. Strom, J. Brown, C.A. Becker, P.R. Fleshner, and M. Dubinsky Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis Science 336 2012 1314 1317
8. D.L. Moyes, and J.R. Naglik The mycobiome: influencing IBD severity Cell Host Microbe 11 2012 551 552
9. M.A. Ghannoum, R.J. Jurevic, P.K. Mukherjee, F. Cui, M. Sikaroodi, A. Naqvi, and P.M. Gillevet Characterization of the oral fungal microbiome (mycobiome) in healthy individuals PLoS Pathog. 6 2010 e1000713
10. R. Khatib, K.M. Riederer, J. Ramanathan, and J. Baran Jr. Faecal fungal flora in healthy volunteers and inpatients Mycoses 44 2001 151 156
11. C.J. Nobile, and A.P. Mitchell Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p Curr. Biol. 15 2005 1150 1155
12. C.J. Nobile, E.P. Fox, J.E. Nett, T.R. Sorrells, Q.M. Mitrovich, A.D. Hernday, B.B. Tuch, D.R. Andes, and A.D. Johnson A recently evolved transcriptional network controls biofilm development in Candida albicans Cell 148 2012 126 138
13. N.P. Revsbech, L.H. Larsen, J. Gundersen, T. Dalsgaard, O. Ulloa, and B. Thamdrup Determination of ultra-low oxygen concentrations in oxygen minimum zones by the STOX sensor Limnol. Oceanogr. Methods 7 2009 371 381
14. A.D. Hernday, M.B. Lohse, P.M. Fordyce, C.J. Nobile, J.L. DeRisi, and A.D. Johnson Structure of the transcriptional network controlling white-opaque switching in Candida albicans Mol. Microbiol. 90 2013 22 35
15. B. Slutsky, M. Staebell, J. Anderson, L. Risen, M. Pfaller, and D.R. Soll "White-opaque transition": a second high-frequency switching system in Candida albicans J. Bacteriol. 169 1987 189 197
16. T. Srikantha, A.R. Borneman, K.J. Daniels, C. Pujol, W. Wu, M.R. Seringhaus, M. Gerstein, S. Yi, M. Snyder, and D.R. Soll TOS9 regulates white-opaque switching in Candida albicans Eukaryot. Cell 5 2006 1674 1687
17. R.E. Zordan, D.J. Galgoczy, and A.D. Johnson Epigenetic properties of white-opaque switching in Candida albicans are based on a self-sustaining transcriptional feedback loop Proc. Natl. Acad. Sci. USA 103 2006 12807 12812
18. E.H. Rikkerink, B.B. Magee, and P.T. Magee Opaque-white phenotype transition: a programmed morphological transition in Candida albicans J. Bacteriol. 170 1988 895 899
19. M.B. Lohse, and A.D. Johnson Temporal anatomy of an epigenetic switch in cell programming: the white-opaque transition of C. albicans Mol. Microbiol. 78 2010 331 343
20. B.B. Tuch, Q.M. Mitrovich, O.R. Homann, A.D. Hernday, C.K. Monighetti, F.M. De La Vega, and A.D. Johnson The transcriptomes of two heritable cell types illuminate the circuit governing their differentiation PLoS Genet. 6 2010 e1001070
21. R.E. Zordan, M.G. Miller, D.J. Galgoczy, B.B. Tuch, and A.D. Johnson Interlocking transcriptional feedback loops control white-opaque switching in Candida albicans PLoS Biol. 5 2007 e256
22. J.M. Synnott, A. Guida, S. Mulhern-Haughey, D.G. Higgins, and G. Butler Regulation of the hypoxic response in Candida albicans Eukaryot. Cell 9 2010 1734 1746
23. O.R. Homann, J. Dea, S.M. Noble, and A.D. Johnson A phenotypic profile of the Candida albicans regulatory network PLoS Genet. 5 2009 e1000783
24. R. Martin, G.P. Moran, I.D. Jacobsen, A. Heyken, J. Domey, D.J. Sullivan, O. Kurzai, and B. Hube The Candida albicans-specific gene EED1 encodes a key regulator of hyphal extension PLoS ONE 6 2011 e18394
25. X. Zhao, K.J. Daniels, S.H. Oh, C.B. Green, K.M. Yeater, D.R. Soll, and L.L. Hoyer Candida albicans Als3p is required for wild-type biofilm formation on silicone elastomer surfaces Microbiology 152 2006 2287 2299
26. Y. Liu, and S.G. Filler Candida albicans Als3, a multifunctional adhesin and invasin Eukaryot. Cell 10 2011 168 173
27. R.J. Silverman, A.H. Nobbs, M.M. Vickerman, M.E. Barbour, and H.F. Jenkinson Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities Infect. Immun. 78 2010 4644 4652
28. B.M. Peters, E.S. Ovchinnikova, B.P. Krom, L.M. Schlecht, H. Zhou, L.L. Hoyer, H.J. Busscher, H.C. van der Mei, M.A. Jabra-Rizk, and M.E. Shirtliff Staphylococcus aureus adherence to Candida albicans hyphae is mediated by the hyphal adhesin Als3p Microbiology 158 2012 2975 2986
29. C.J. Nobile, D.R. Andes, J.E. Nett, F.J. Smith, F. Yue, Q.-T. Phan, J.E. Edwards, S.G. Filler, and A.P. Mitchell Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo PLoS Pathog. 2 2006 e63
30. D.J. Bradshaw, P.D. Marsh, C. Allison, and K.M. Schilling Effect of oxygen, inoculum composition and flow rate on development of mixed-culture oral biofilms Microbiology 142 1996 623 629
31. D.J. Bradshaw, P.D. Marsh, G.K. Watson, and C. Allison Role of Fusobacterium nucleatum and coaggregation in anaerobe survival in planktonic and biofilm oral microbial communities during aeration Infect. Immun. 66 1998 4729 4732
32. T. Rossignol, C. Ding, A. Guida, C. d'Enfert, D.G. Higgins, and G. Butler Correlation between biofilm formation and the hypoxic response in Candida parapsilosis Eukaryot. Cell 8 2009 550 559
33. J. Bonhomme, M. Chauvel, S. Goyard, P. Roux, T. Rossignol, and C. d'Enfert Contribution of the glycolytic flux and hypoxia adaptation to efficient biofilm formation by Candida albicans Mol. Microbiol. 80 2011 995 1013
34. C. Stichternoth, and J.F. Ernst Hypoxic adaptation by Efg1 regulates biofilm formation by Candida albicans Appl. Environ. Microbiol. 75 2009 3663 3672
35. W.J. Loesche Oxygen sensitivity of various anaerobic bacteria Appl. Microbiol. 18 1969 723 727
36. F.P. Tally, P.R. Stewart, V.L. Sutter, and J.E. Rosenblatt Oxygen tolerance of fresh clinical anaerobic bacteria J. Clin. Microbiol. 1 1975 161 164
37. J. Li, V. Adams, T.L. Bannam, K. Miyamoto, J.P. Garcia, F.A. Uzal, J.I. Rood, and B.A. McClane Toxin plasmids of Clostridium perfringens Microbiol. Mol. Biol. Rev. 77 2013 208 233
38. D.L. Stevens, M.J. Aldape, and A.E. Bryant Life-threatening clostridial infections Anaerobe 18 2012 254 259
39. K. Lewis Persister cells Annu. Rev. Microbiol. 64 2010 357 372
40. K.M. Yeater, J. Chandra, G. Cheng, P.K. Mukherjee, X. Zhao, S.L. Rodriguez-Zas, K.E. Kwast, M.A. Ghannoum, and L.L. Hoyer Temporal analysis of Candida albicans gene expression during biofilm development Microbiology 153 2007 2373 2385
41. P. Uppuluri, A.K. Chaturvedi, A. Srinivasan, M. Banerjee, A.K. Ramasubramaniam, J.R. Köhler, D. Kadosh, and J.L. Lopez-Ribot Dispersion as an important step in the Candida albicans biofilm developmental cycle PLoS Pathog. 6 2010 e1000828
42. G.S. Baillie, and L.J. Douglas Role of dimorphism in the development of Candida albicans biofilms J. Med. Microbiol. 48 1999 671 679
43. J.E. Nett, A.J. Lepak, K. Marchillo, and D.R. Andes Time course global gene expression analysis of an in vivo Candida biofilm J. Infect. Dis. 200 2009 307 313
44. K. Pande, C. Chen, and S.M. Noble Passage through the mammalian gut triggers a phenotypic switch that promotes Candida albicans commensalism Nat. Genet. 45 2013 1088 1091
45. X. Peng, J. Sun, D. Iserentant, C. Michiels, and H. Verachtert Flocculation and coflocculation of bacteria by yeasts Appl. Microbiol. Biotechnol. 55 2001 777 781