Unveiling Candida albicans intestinal carriage in healthy volunteers: the role of micro- and mycobiota, diet, host genetics and immune response

Margot  Delavy; Natacha Sertour; Etienne Patin; Emmanuelle Le Chatelier; Nathaniel Cole; Florian  Dubois; Zixuan  Xie; Violaine  Saint-André; Chaysavanh Manichanh; Alan Walker; Lluis  Quintana-Murci; Darragh  Duffy; Christophe d'Enfert; Marie Elisabeth  Bougnoux; Milieu Intérieur consortium

doi:10.1080/19490976.2023.2287618

Unveiling Candida albicans intestinal carriage in healthy volunteers: the role of micro- and mycobiota, diet, host genetics and immune response

Margot Delavy, Natacha Sertour, Etienne Patin, Emmanuelle Le Chatelier, Nathaniel Cole, Florian Dubois, Zixuan Xie, Violaine Saint-André, Chaysavanh Manichanh, Alan Walker, Lluis Quintana-Murci, Darragh Duffy, Christophe d'Enfert, Marie Elisabeth Bougnoux^* (Corresponding Author), Milieu Intérieur consortium

^*Corresponding author for this work

The Rowett Institute of Nutrition and Health

Research output: Contribution to journal › Article › peer-review

1 Citation (Scopus)

Abstract

Candida albicans is a commensal yeast present in the gut of most healthy individuals but with highly variable concentrations. However, little is known about the host factors that influence colonization densities. We investigated how microbiota, host lifestyle factors, and genetics could shape C. albicans intestinal carriage in 695 healthy individuals from the Milieu Intérieur cohort. C. albicans intestinal carriage was detected in 82.9% of the subjects using quantitative PCR. Using linear mixed models and multiway-ANOVA, we explored C. albicansintestinal levels with regard to gut microbiota composition and lifestyle
factors including diet. By analyzing shotgun metagenomics data and C. albicans
qPCR data, we showed that Intestinimonas butyriciproducens was the only gut
microbiota species whose relative abundance was negatively correlated with C.
albicans concentration. Diet is also linked to C. albicans growth, with eating
between meals and a low-sodium diet being associated with higher C. albicans
levels. Furthermore, by Genome-Wide Association Study, we identified 26 single
nucleotide polymorphisms suggestively associated with C. albicans colonization.
n addition, we found that the intestinal levels of C. albicans might influence the
20 host immune response, specifically in response to fungal challenge. We analyzed the transcriptional levels of 546 immune genes and the concentration of cytokines after whole blood stimulation with C. albicans cells and showed positive associations between the extent of C. albicans intestinal levels and NLRP3 expression, as well as secreted IL-2 and CXCL5 concentrations.
Taken together, these findings open the way for potential new interventional strategies to curb C. albicans intestinal overgrowth.

Original language	English
Article number	2287618
Number of pages	25
Journal	Gut Microbes
Volume	15
Issue number	2
Early online date	28 Nov 2023
DOIs	https://doi.org/10.1080/19490976.2023.2287618
Publication status	Published - 28 Nov 2023

Bibliographical note

Acknowledgements
This work was supported by a grant from Agence Nationale de la Recherche
(FunComPath ANR-14-IFEC-0004), the French Government’s Investissement d’Avenir program (Laboratoire d’Excellence Integrative Biology of Emerging Infectious Diseases [ANR10-LABX-62-IBEID], and [ANR-10-LABX-69-01]), the European Union's Horizon 2020 research and innovation program under the Marie Sklodowska-Curie action, Innovative Training Network (FunHoMic; Grant No. 812969 ), and the European Union's Horizon 2020 Research and Innovation Program (HDM-FUN, Grant No. 847507). AWW and the Rowett Institute (University of Aberdeen) received core funding support from the Scottish Government’s Rural and Environmental Sciences and Analytical Services (RESAS).

Keywords

Candida albicans
colonization resistance
microbiota
mycobiota
GWAS
lifestyle factors
metagenomics
host factors

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Delavy_etal_GM_Unveiling_Candida_Albicans_VoR
© 2023 The Author(s). Published with license by Taylor & Francis Group, LLC. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The terms on which this article has been published allow the posting of the Accepted Manuscript in a repository by the author(s) or with their consent.
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Cite this

Delavy, M., Sertour, N., Patin, E., Le Chatelier, E., Cole, N., Dubois, F., Xie, Z., Saint-André, V., Manichanh, C., Walker, A., Quintana-Murci, L., Duffy, D., d'Enfert, C., Bougnoux, M. E., & Milieu Intérieur consortium (2023). Unveiling Candida albicans intestinal carriage in healthy volunteers: the role of micro- and mycobiota, diet, host genetics and immune response. Gut Microbes, 15(2), Article 2287618. https://doi.org/10.1080/19490976.2023.2287618

Delavy, M, Sertour, N, Patin, E, Le Chatelier, E, Cole, N, Dubois, F, Xie, Z, Saint-André, V, Manichanh, C, Walker, A, Quintana-Murci, L, Duffy, D, d'Enfert, C, Bougnoux, ME & Milieu Intérieur consortium 2023, 'Unveiling Candida albicans intestinal carriage in healthy volunteers: the role of micro- and mycobiota, diet, host genetics and immune response', Gut Microbes, vol. 15, no. 2, 2287618. https://doi.org/10.1080/19490976.2023.2287618

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abstract = "Candida albicans is a commensal yeast present in the gut of most healthy individuals but with highly variable concentrations. However, little is known about the host factors that influence colonization densities. We investigated how microbiota, host lifestyle factors, and genetics could shape C. albicans intestinal carriage in 695 healthy individuals from the Milieu Int{\'e}rieur cohort. C. albicans intestinal carriage was detected in 82.9% of the subjects using quantitative PCR. Using linear mixed models and multiway-ANOVA, we explored C. albicansintestinal levels with regard to gut microbiota composition and lifestylefactors including diet. By analyzing shotgun metagenomics data and C. albicansqPCR data, we showed that Intestinimonas butyriciproducens was the only gutmicrobiota species whose relative abundance was negatively correlated with C.albicans concentration. Diet is also linked to C. albicans growth, with eatingbetween meals and a low-sodium diet being associated with higher C. albicanslevels. Furthermore, by Genome-Wide Association Study, we identified 26 singlenucleotide polymorphisms suggestively associated with C. albicans colonization.n addition, we found that the intestinal levels of C. albicans might influence the20 host immune response, specifically in response to fungal challenge. We analyzed the transcriptional levels of 546 immune genes and the concentration of cytokines after whole blood stimulation with C. albicans cells and showed positive associations between the extent of C. albicans intestinal levels and NLRP3 expression, as well as secreted IL-2 and CXCL5 concentrations.Taken together, these findings open the way for potential new interventional strategies to curb C. albicans intestinal overgrowth.",

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author = "Margot Delavy and Natacha Sertour and Etienne Patin and {Le Chatelier}, Emmanuelle and Nathaniel Cole and Florian Dubois and Zixuan Xie and Violaine Saint-Andr{\'e} and Chaysavanh Manichanh and Alan Walker and Lluis Quintana-Murci and Darragh Duffy and Christophe d'Enfert and Bougnoux, {Marie Elisabeth} and {Milieu Int{\'e}rieur consortium}",

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AU - Le Chatelier, Emmanuelle

AU - Cole, Nathaniel

AU - Dubois, Florian

AU - Xie, Zixuan

AU - Saint-André, Violaine

AU - Manichanh, Chaysavanh

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N2 - Candida albicans is a commensal yeast present in the gut of most healthy individuals but with highly variable concentrations. However, little is known about the host factors that influence colonization densities. We investigated how microbiota, host lifestyle factors, and genetics could shape C. albicans intestinal carriage in 695 healthy individuals from the Milieu Intérieur cohort. C. albicans intestinal carriage was detected in 82.9% of the subjects using quantitative PCR. Using linear mixed models and multiway-ANOVA, we explored C. albicansintestinal levels with regard to gut microbiota composition and lifestylefactors including diet. By analyzing shotgun metagenomics data and C. albicansqPCR data, we showed that Intestinimonas butyriciproducens was the only gutmicrobiota species whose relative abundance was negatively correlated with C.albicans concentration. Diet is also linked to C. albicans growth, with eatingbetween meals and a low-sodium diet being associated with higher C. albicanslevels. Furthermore, by Genome-Wide Association Study, we identified 26 singlenucleotide polymorphisms suggestively associated with C. albicans colonization.n addition, we found that the intestinal levels of C. albicans might influence the20 host immune response, specifically in response to fungal challenge. We analyzed the transcriptional levels of 546 immune genes and the concentration of cytokines after whole blood stimulation with C. albicans cells and showed positive associations between the extent of C. albicans intestinal levels and NLRP3 expression, as well as secreted IL-2 and CXCL5 concentrations.Taken together, these findings open the way for potential new interventional strategies to curb C. albicans intestinal overgrowth.

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KW - microbiota

KW - mycobiota

KW - GWAS

KW - lifestyle factors

KW - metagenomics

KW - host factors

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DO - 10.1080/19490976.2023.2287618

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Unveiling Candida albicans intestinal carriage in healthy volunteers: the role of micro- and mycobiota, diet, host genetics and immune response

Abstract

Bibliographical note

Keywords

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