Anaerobic Bacteria Grow within Candida albicans Biofilms and Induce Biofilm Formation in Suspension Cultures

Fox, Emily P.; Cowley, Elise S.; Nobile, Clarissa J.; Hartooni, Nairi; Newman, Dianne K.; Johnson, Alexander D.

doi:10.1016/j.cub.2014.08.057

Cited by 207Antifungal resistance and susceptibilityBacterial biofilms and quorum sensingFungal and yeast genetics research

Anaerobic Bacteria Grow within Candida albicans Biofilms and Induce Biofilm Formation in Suspension Cultures

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Fox, Emily P., Cowley, Elise S., Nobile, Clarissa J., Hartooni, Nairi, Newman, Dianne K., Johnson, Alexander D.·2014·Current Biology

DOI 10.1016/j.cub.2014.08.057PMC PMC4252622

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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.

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When cultured together with Candida albicans in ambient oxygen, Bacteroides fragilis and Clostridium perfringens could induce Candida albicans to form mini-biofilms, which could protect the bacteria and allow them to proliferate under otherwise toxic conditions.
“Moreover, when cultured together with C. albicans in ambient oxygen, these anaerobes could induce the latter to form mini-biofilms, which, in turn, could protect the bacteria and allow them to proliferate under otherwise toxic conditions.”
From Candida albicans Biofilms and Human Disease (2015) · cites this paper as [60]
In a study of dual-species biofilms Candida albicans forms with gut microbiota members, biofilms formed by Candida albicans provided a hypoxic microenvironment that could support the growth of Bacteroides fragilis and Clostridium perfringens even though the biofilms were grown under oxygen-rich conditions.
“In this study, biofilms formed by C. albicans provided a hypoxic microenvironment that could support the growth of the two strictly anaerobic bacteria, B. fragilis and C. perfringens—even though the biofilms were grown under oxygen-rich conditions.”
From Candida albicans Biofilms and Human Disease (2015) · cites this paper as [60]

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Authors: Fox, E. P., Cowley, E. S., Nobile, C. J., Hartooni, N., Newman, D. K., & Johnson, A. D.
Affiliations: University of California, San Francisco (US)
California Institute of Technology (US)
University of California, Merced (US)
Corresponding author: Johnson, Alexander D.
ORCID: Fox, Emily P.
Cowley, Elise S.
Nobile, Clarissa J.
Hartooni, Nairi
Newman, Dianne K.
Johnson, Alexander D.
Venue: Current Biology
Publisher: Elsevier BV
Published: 2014-10
Volume: 24
Issue: 20
Pages: 2411-2416
ISSN: 0960-9822 (ISSN-L)
DOI: 10.1016/j.cub.2014.08.057
PMC: PMC4252622
OpenAlex: W1993028695
Cited by: 207
References: 54
Citations by year: 2026: 14 · 2025: 22 · 2024: 8 · 2023: 17 · 2022: 24 · 2021: 26 · 2020: 21 · 2019: 19 · 2018: 11 · 2017: 15 · 2016: 15 · 2015: 14 · 2014: 1
FWCI: 10.51
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 384 d)
Locations: Current Biology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
CaltechAUTHORS (California Institute of Technology) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: Howard Hughes Medical Institute
Sandler Foundation
National Institutes of Health
University of California, San Francisco
National Heart, Lung, and Blood Institute (R01HL117328)
National Institute of General Medical Sciences (T32GM007810)
National Institute of Allergy and Infectious Diseases (K99AI100896, R01AI083311, T32AI060537)
Topics: Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Keywords: Candida albicans, anaerobic bacteria, polymicrobial biofilms, Clostridium perfringens, Bacteroides fragilis, Escherichia coli, Klebsiella pneumoniae, Enterococcus faecalis, hypoxic microenvironment, fungal-bacterial interactions, gut microbiota
MeSH terms: Anaerobiosis, Bacteria, Anaerobic, Candida albicans, Microbiological Techniques, Biofilms, Coculture Techniques

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Anaerobic Bacteria Grow within Candida albicans Biofilms and Induce Biofilm Formation in Suspension Cultures

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