Ecology of Candida albicans gut colonization: inhibition of Candida adhesion, colonization, and dissemination from the gastrointestinal tract by bacterial antagonism
Open accessAbstract
Antibiotic-treated and untreated Syrian hamsters were inoculated intragastrically with Candida albicans to determine whether C. albicans could opportunistically colonize the gastrointestinal tract and disseminate to visceral organs. Antibiotic treatment decreased the total population levels of the indigenous bacterial flora and predisposed hamsters to gastrointestinal overgrowth and subsequent systemic dissemination by C. albicans in 86% of the animals. Both control hamsters not given antibiotics and antibiotic-treated animals reconventionalized with an indigenous microflora showed significantly lower gut populations of C. albicans, and C. albicans organisms were cultured from the visceral organs of 0 and 10% of the animals, respectively. Conversely, non-antibiotic-treated hamsters inoculated repeatedly with C. albicans had high numbers of C. albicans in the gut, and viable C. albicans was recovered from the visceral organs of 53% of the animals. Examination of the mucosal surfaces from test and control animals indicated further that animals which contained a complex indigenous microflora had significantly lower numbers of C. albicans associated with their gut walls than did antibiotic-treated animals. The ability of C. albicans to associate with intestinal mucosal surfaces also was tested by an in vitro adhesion assay. The results indicate that the indigenous microflora reduced the mucosal association of C. albicans by forming a dense layer of bacteria in the mucus gel, out-competing yeast cells for adhesion sites, and producing inhibitor substances (possibly volatile fatty acids, secondary bile acids, or both) that reduced C. albicans adhesion. It is suggested, therefore, that the indigenous intestinal microflora suppresses C. albicans colonization and dissemination from the gut by inhibiting Candida-mucosal association and reducing C. albicans population levels in the gut.
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C. albicans is a member of the healthy microbiota, asymptomatically colonizing the gastrointestinal tract, reproductive tract, oral cavity, and skin of most humans.
“It is a member of the healthy microbiota, asymptomatically colonizing the gastrointestinal (GI) tract, reproductive tract, oral cavity, and skin of most humans (1, 64, 87, 97, 99).”
From <i>Candida albicans</i> Biofilms and Human Disease (2015) · cites this paper as [87]
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BackgroundAdhesion and Association Mechanisms of Candida albicans
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“[12,13] Of the risk factors, fungal colonization by Candida species is common for any IFI.”
BackgroundInfluentialProbiotics and prebiotics: microflora management for improved gut health
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“tropicalis with bacteria (22) and may not reveal possible”
BackgroundInfluentialGut flora and disease resistance
Hentges, D. J. (1992) · Springer eBooks · doi:10.1007/978-94-011-2364-8_5 · Cited by 85 · see citing works
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Invited Review: Immunologic Structure and Function of the Gastrointestinal Tract
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Mechanisms of association of Candida albicans with intestinal mucosa
Kennedy, M. J., Volz, P. A., Edwards, C. A., & Yangey, R. J. (1987) · Journal of Medical Microbiology · doi:10.1099/00222615-24-4-333 · Cited by 75 · see citing works
Self-citationKennedy, M. J., & Sandin, R. L. (1988) · Medical Mycology · doi:10.1080/02681218880000121 · Cited by 74 · see citing works
Self-citationGow, N. A. R., & Netea, M. G. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0462 · Cited by 75 · see citing works
“Candida colonization is also influenced by quantitative and qualitative aspects of the microbiome, such as Lactobacilli that inhibit fungal adhesion and growth by producing H2O2 and bacteriocin-like compounds [76].”
BackgroundThe Multibiome: The Intestinal Ecosystem's Influence on Immune Homeostasis, Health, and Disease
Filyk, H. A., & Osborne, L. C. (2016) · EBioMedicine · doi:10.1016/j.ebiom.2016.10.007 · Cited by 70 · see citing works
“In addition, bacterial-derived fatty-acid metabolites can impair Candida albicans colonization of intestinal tissue, and a complex bacterial microbiome inhibits translocation of pathogenic C. albicans across the intestinal barrier (Kennedy and Volz, 1985).”
BackgroundEkenna, O., & Sherertz, R. J. (1987) · Infection and Immunity · doi:10.1128/iai.55.7.1558-1563.1987 · Cited by 72 · see citing works
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Gastric colonization of Candida albicans differs in mice fed commercial and purified diets.
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“(2) Competition for resources such as nutrients or space could have prevented establishment of a new member of the skin microbiota [66,67].”
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Lohse, M. B., Gulati, M., Craik, C. S., Johnson, A. D., & Nobile, C. J. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01027 · Cited by 65 · see citing works
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Yu, L., Lee, K. K., Sheth, H. B., Lane-Bell, P., Srivastava, G., Hindsgaul, O., PARANCHYCH, W., Hodges, R. S., & Irvin, R. T. (1994) · Infection and Immunity · doi:10.1128/iai.62.7.2843-2848.1994 · Cited by 61 · see citing works
“ment (29), phenotypic state (30), growth media (48), commensal bacteria (6, 32, 46), germ tube formation (34), and tissue sites (59).”
BackgroundHost defense system interactions with Candida.
Greenfield, R. A. (1992) · PubMed · Cited by 57 · see citing works
Mellado, E., Cuenca‐Estrella, M., Regadera, J., González, M. E., Dı́az-Guerra, T. M., & Rodriguez-Tudela, J. L. (2000) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/s0732-8893(00)00165-6 · Cited by 56 · see citing works
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Wiesner, S. M., Jechorek, R. P., Garni, R. M., Bendel, C. M., & Wells, C. L. (2001) · Clinical and Diagnostic Laboratory Immunology · doi:10.1128/cdli.8.1.192-195.2001 · Cited by 54 · see citing works
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“albicans to intestinal epithelium in the noncompromised host [23].”
BackgroundSelf-citationTranscriptional Circuits Regulating Developmental Processes in Candida albicans
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“Previous studies used substantially shorter duration of feeding (<3 days) (8, 14, 28).”
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Gastrointestinal candidiasis in a murine model of severe combined immunodeficiency syndrome
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“A number of studies have more carefully evaluated changes in bacterial flora and Candida GI colonization in rodents in response to antibacterial therapy than was our purpose here, and they have demonstrated enhancement of Candida colonization by various antibacterial regimens (12, 15, 16).”
BackgroundCandida albicans translocation across the gut mucosa following burn injury
Inoue, S., Wirman, J. A., Alexander, J. W., Trocki, O., & Cardell, R. R. (1988) · Journal of Surgical Research · doi:10.1016/0022-4804(88)90152-7 · Cited by 51 · see citing works
Gizaw, A., Marami, L. M., Teshome, I., Sarba, E. J., Admasu, P., Atalel, D., Mulatu, G., Bune, W. M., Bayu, M. D., Tadesse, M., et al. (2022) · Advances in Pharmacological and Pharmaceutical Sciences · doi:10.1155/2022/3299146 · Cited by 50 · see citing works
“Administration of antibiotics and immunosuppressive drugs are some of the factors associated with Candida infection [22].”
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“For example, competition between bacteria and fungi leads to stunted Candida growth.(78) The release of various compounds can drive these interactions.”
BackgroundVargas, S. L., Patrick, C. C., Ayers, G. D., & Hughes, W. T. (1993) · Infection and Immunity · doi:10.1128/iai.61.2.619-626.1993 · Cited by 48 · see citing works
“Generally, an enlarged cecum (5 to 10% of the total body weight) indicates the presence of relatively simple intestinal microflora (12, 19).”
BackgroundInfluentialCANDIDA CARRIAGE IN THE ALIMENTARY TRACT OF LIVER TRANSPLANT CANDIDATES
Kusne, S., Tobin, D., Pasculle, A. W., Thiel, D. H. V., Ho, M., & Starzl, T. E. (1994) · Transplantation · doi:10.1097/00007890-199402150-00014 · Cited by 47 · see citing works
“There are experimental models demonstrating that animals treated with antibiotics and then “challenged” with yeast develop not only a high gastro-intestinal colonization rate, but also visceral dissemination (9).”
BackgroundCandidemia in HIV-Infected Subjects
Tumbarello, M., Tacconelli, E., Donati, K. D. G., Morace, G., Fadda, G., & Cauda, R. (1999) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s100960050327 · Cited by 47 · see citing works
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“It has been shown that most of the infections involving Candida are endogenously acquired from the gastrointestinal (GI) tract [1].”
BackgroundSensing of the Microbial Neighborhood by Candida albicans
Mallick, E. M., & Bennett, R. J. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003661 · Cited by 42 · see citing works
Human gut bifidobacteria inhibit the growth of the opportunistic fungal pathogen Candida albicans
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Effect of INT1 Gene on Candida albicans Murine Intestinal Colonization
Kinneberg, K. M., Bendel, C. M., Jechorek, R. P., Cebelinski, E. A., Gale, C. A., Berman, J. G., Erlandsen, S. L., Hostetter, M. K., & Wells, C. L. (1999) · Journal of Surgical Research · doi:10.1006/jsre.1999.5755 · Cited by 41 · see citing works
In VitroAntifungal Activity of Equol againstCandida albicans
Lee, J., & Chee, H. Y. (2010) · Mycobiology · doi:10.4489/myco.2010.38.4.328 · Cited by 40 · see citing works
“Approximately 30~50% of the human population is capable of producing equol from daidzein in their GITs [7].”
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Microorganisms and Diarrhea in Enterally Fed Intensive Care Unit Patients
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Host defense system interactions withCandida
Greenfield, R. A. (1992) · Medical Mycology · doi:10.1080/02681219280000141 · Cited by 62 · see citing works
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“albicans.(12,13) Although these reports suggest that commensal bacteria resist C.”
BackgroundMarquis, M., Lewandowski, D., Dugas, V., Aumont, F., Sénéchal, S., Jolicoeur, P., Hanna, Z., & de Repentigny, L. (2006) · Infection and Immunity · doi:10.1128/iai.74.4.2382-2391.2006 · Cited by 34 · see citing works
“albicans in a germfree environment (29, 30), and they were therefore devoid of a protective bacterial flora (31).”
BackgroundPharmaceutical Probiotics for the Treatment of Anaerobic and Other Infections
McFarland, L. V., & Elmer, G. W. (1997) · Anaerobe · doi:10.1006/anae.1996.0062 · Cited by 33 · see citing works
“Attachment site competition or toxin receptor site competition has also been proposed in a few studies [36,46–49].”
BackgroundBertagnolio, S., Donati, K. D. G., Tacconelli, E., Scoppettuolo, G., Posteraro, B., Fadda, G., Cauda, R., & Tumbarello, M. (2004) · Journal of Chemotherapy · doi:10.1179/joc.2004.16.2.172 · Cited by 32 · see citing works
NOSOCOMIAL INFECTION IN THE SURGICAL INTENSIVE CARE UNIT
Nathens, A. B., Chu, P. T. Y., & Marshall, J. C. (1992) · Infectious Disease Clinics of North America · doi:10.1016/s0891-5520(20)30468-2 · Cited by 32 · see citing works
Sandin, R. L., Rogers, A. L., Beneke, E. S., & Fernández, M. (1987) · Mycopathologia · doi:10.1007/bf00437297 · Cited by 32 · see citing works
“Conversely, antibiotic treatment of hamsters decreased the number of bacteria in their intestines and promoted yeast adhesion, colonization and dissemination from the gut [8].”
BackgroundCandida and antibiotic-associated diarrhoea
Krause, R., & Reisinger, E. C. (2005) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2004.00978.x · Cited by 32 · see citing works
“albicans adhesion is reduced and the growth of Candida is suppressed further by the competition for growth-limiting nutrients [8–10].”
Background
- Authors
- Kennedy, M. J., & Volz, P. A.
- Venue
- Infection and Immunity
- Publisher
- American Society for Microbiology
- Published
- 1985-09
- Volume
- 49
- Issue
- 3
- Pages
- 654-663
- ISSN
- 0019-9567 (ISSN-L)
- 1098-5522
- PMC
- PMC261235
- OpenAlex
- W1907372042
- Cited by
- 208
- References
- 65
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 2 · 2023: 4 · 2022: 8 · 2021: 6 · 2020: 12 · 2019: 5 · 2018: 3 · 2017: 7 · 2016: 4 · 2015: 6 · 2014: 6 · 2013: 9 · 2012: 2
- FWCI
- 7.45
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Infection and Immunity (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Keywords
- Candida albicans, intestinal colonization, bacterial antagonism, antibiotic-induced dysbiosis, systemic candidiasis, mucosal colonization, secondary bile acids, volatile fatty acids, Syrian hamster model, opportunistic fungal infection
- MeSH terms
- Adhesiveness, Animals, Antibiosis, Anti-Bacterial Agents, Candida albicans, Cecum, Digestive System, Ecology, Cricetinae, Intestinal Mucosa, Male, Mesocricetus, Microscopy, Electron, Scanning, Bacterial Physiological Phenomena
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