Anaerobic Bacteria Grow within Candida albicans Biofilms and Induce Biofilm Formation in Suspension Cultures
Abstract
The human microbiome contains diverse microorganisms, which share and compete for the same environmental niches. A major microbial growth form in the human body is the biofilm state, where tightly packed bacterial, archaeal, and fungal cells must cooperate and/or compete for resources in order to survive. We examined mixed biofilms composed of the major fungal species of the gut microbiome, Candida albicans, and each of five prevalent bacterial gastrointestinal inhabitants: Bacteroides fragilis, Clostridium perfringens, Escherichia coli, Klebsiella pneumoniae, and Enterococcus faecalis. We observed that biofilms formed by C. albicans provide a hypoxic microenvironment that supports the growth of two anaerobic bacteria, even when cultured in ambient oxic conditions that are normally toxic to the bacteria. We also found that coculture with bacteria in biofilms induces massive gene expression changes in C. albicans, including upregulation of WOR1, which encodes a transcription regulator that controls a phenotypic switch in C. albicans, from the "white" cell type to the "opaque" cell type. Finally, we observed that in suspension cultures, C. perfringens induces aggregation of C. albicans into "mini-biofilms," which allow C. perfringens cells to survive in a normally toxic environment. This work indicates that bacteria and C. albicans interactions modulate the local chemistry of their environment in multiple ways to create niches favorable to their growth and survival.
Additional Information
© 2014 Elsevier Ltd. Received 9 March 2014, Revised 31 July 2014, Accepted 22 August 2014, Available online 9 October 2014. Published: October 9, 2014. We thank Matthew Lohse, Aaron Hernday, Chiraj Dalal, Oliver Homann, and Jose Christian Perez for strains or plasmids used in this study; Sheena Singh Babak and Trevor Sorrells for comments on the manuscript; and Jorge Mendoza for technical assistance. We appreciate the use of the UCSF Nikon Imaging Center. This study was supported by NIH grant R01AI083311 (to A.D.J.) and by a UCSF Program for Breakthrough Biomedical Research award, funded partly by the Sandler Foundation. E.P.F. was supported by NIH fellowship T32AI060537, C.J.N. was supported by NIH grant K99AI100896, and D.K.N. and E.S.C. were supported by the Howard Hughes Medical Institute (HHMI) and the National Heart, Lung, and Blood Institute of the NIH (R01HL117328). D.K.N. is an HHMI Investigator.Attached Files
Accepted Version - nihms626355.pdf
Supplemental Material - mmc1.pdf
Supplemental Material - mmc2.xlsx
Supplemental Material - mmc3.xlsx
Supplemental Material - mmc4.xlsx
Supplemental Material - mmc5.xlsx
Supplemental Material - mmc6.xlsx
Supplemental Material - mmc7.xlsx
Supplemental Material - mmc8.pdf
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Additional details
- PMCID
- PMC4252622
- Eprint ID
- 50565
- Resolver ID
- CaltechAUTHORS:20141020-141511951
- NIH
- R01AI083311
- UCSF Program for Breakthrough Biomedical Research
- Sandler Foundation
- NIH
- T32AI060537
- NIH
- K99AI100896
- Howard Hughes Medical Institute (HHMI)
- NIH
- R01HL117328
- Created
-
2014-10-20Created from EPrint's datestamp field
- Updated
-
2021-11-10Created from EPrint's last_modified field
- Caltech groups
- Division of Geological and Planetary Sciences