Transient colonizing microbes promote gut dysbiosis and functional impairment

Sunjae Lee; Victoria Meslier; Gholamreza Bidkhori; Fernando Garcia-Guevara; Lucie Etienne-Mesmin; Frederick Clasen; Junseok Park; Florian Plaza Oñate; Haizhuang Cai; Emmanuelle Le Chatelier; Nicolas Pons; Marcela Pereira; Maike Seifert; Fredrik Boulund; Lars Engstrand; Doheon Lee; Gordon Proctor; Adil Mardinoglu; Stéphanie Blanquet-Diot; David Moyes; Mathieu Almeida; S Dusko Ehrlich; Mathias Uhlen; Saeed Shoaie

doi:10.1038/s41522-024-00561-1

Transient colonizing microbes promote gut dysbiosis and functional impairment

Sunjae Lee, Victoria Meslier, Gholamreza Bidkhori, Fernando Garcia-Guevara, Lucie Etienne-Mesmin, Frederick Clasen, Junseok Park, Florian Plaza Oñate, Haizhuang Cai, Emmanuelle Le Chatelier, Nicolas Pons, Marcela Pereira, Maike Seifert, Fredrik Boulund, Lars Engstrand, Doheon Lee, Gordon Proctor, Adil Mardinoglu, Stéphanie Blanquet-Diot, David MoyesMathieu Almeida, S Dusko Ehrlich, Mathias Uhlen, Saeed Shoaie^*

^*Corresponding author for this work

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

Abstract

Species composition of the healthy adult gut microbiota tends to be stable over time. Destabilization of the gut microbiome under the influence of different factors is the main driver of the microbial dysbiosis and subsequent impacts on host physiology. Here, we used metagenomics data from a Swedish longitudinal cohort, to determine the stability of the gut microbiome and uncovered two distinct microbial species groups; persistent colonizing species (PCS) and transient colonizing species (TCS). We validated the continuation of this grouping, generating gut metagenomics data for additional time points from the same Swedish cohort. We evaluated the existence of PCS/TCS across different geographical regions and observed they are globally conserved features. To characterize PCS/TCS phenotypes, we performed bioreactor fermentation with faecal samples and metabolic modeling. Finally, using chronic disease gut metagenome and other multi-omics data, we identified roles of TCS in microbial dysbiosis and link with abnormal changes to host physiology.

Original language	English
Article number	80
Pages (from-to)	80
Journal	npj Biofilms and Microbiomes
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41522-024-00561-1
Publication status	Published - 8 Sept 2024

Keywords

Dysbiosis/microbiology
Gastrointestinal Microbiome
Humans
Metagenomics/methods
Sweden
Bacteria/classification
Feces/microbiology
Longitudinal Studies
Metagenome
Adult
Bioreactors/microbiology
Fermentation

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Lee, S., Meslier, V., Bidkhori, G., Garcia-Guevara, F., Etienne-Mesmin, L., Clasen, F., Park, J., Plaza Oñate, F., Cai, H., Le Chatelier, E., Pons, N., Pereira, M., Seifert, M., Boulund, F., Engstrand, L., Lee, D., Proctor, G., Mardinoglu, A., Blanquet-Diot, S., ... Shoaie, S. (2024). Transient colonizing microbes promote gut dysbiosis and functional impairment. npj Biofilms and Microbiomes, 10(1), 80. Article 80. https://doi.org/10.1038/s41522-024-00561-1

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abstract = "Species composition of the healthy adult gut microbiota tends to be stable over time. Destabilization of the gut microbiome under the influence of different factors is the main driver of the microbial dysbiosis and subsequent impacts on host physiology. Here, we used metagenomics data from a Swedish longitudinal cohort, to determine the stability of the gut microbiome and uncovered two distinct microbial species groups; persistent colonizing species (PCS) and transient colonizing species (TCS). We validated the continuation of this grouping, generating gut metagenomics data for additional time points from the same Swedish cohort. We evaluated the existence of PCS/TCS across different geographical regions and observed they are globally conserved features. To characterize PCS/TCS phenotypes, we performed bioreactor fermentation with faecal samples and metabolic modeling. Finally, using chronic disease gut metagenome and other multi-omics data, we identified roles of TCS in microbial dysbiosis and link with abnormal changes to host physiology.",

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Lee, S, Meslier, V, Bidkhori, G, Garcia-Guevara, F, Etienne-Mesmin, L, Clasen, F, Park, J, Plaza Oñate, F, Cai, H, Le Chatelier, E, Pons, N, Pereira, M, Seifert, M, Boulund, F, Engstrand, L, Lee, D, Proctor, G , Mardinoglu, A, Blanquet-Diot, S, Moyes, D, Almeida, M, Ehrlich, SD, Uhlen, M & Shoaie, S 2024, 'Transient colonizing microbes promote gut dysbiosis and functional impairment', npj Biofilms and Microbiomes, vol. 10, no. 1, 80, pp. 80. https://doi.org/10.1038/s41522-024-00561-1

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AU - Lee, Sunjae

AU - Meslier, Victoria

AU - Bidkhori, Gholamreza

AU - Garcia-Guevara, Fernando

AU - Etienne-Mesmin, Lucie

AU - Clasen, Frederick

AU - Park, Junseok

AU - Plaza Oñate, Florian

AU - Cai, Haizhuang

AU - Le Chatelier, Emmanuelle

AU - Pons, Nicolas

AU - Pereira, Marcela

AU - Seifert, Maike

AU - Boulund, Fredrik

AU - Engstrand, Lars

AU - Lee, Doheon

AU - Proctor, Gordon

AU - Mardinoglu, Adil

AU - Blanquet-Diot, Stéphanie

AU - Moyes, David

AU - Almeida, Mathieu

AU - Ehrlich, S Dusko

AU - Uhlen, Mathias

AU - Shoaie, Saeed

N1 - Publisher Copyright: © The Author(s) 2024.

PY - 2024/9/8

Y1 - 2024/9/8

N2 - Species composition of the healthy adult gut microbiota tends to be stable over time. Destabilization of the gut microbiome under the influence of different factors is the main driver of the microbial dysbiosis and subsequent impacts on host physiology. Here, we used metagenomics data from a Swedish longitudinal cohort, to determine the stability of the gut microbiome and uncovered two distinct microbial species groups; persistent colonizing species (PCS) and transient colonizing species (TCS). We validated the continuation of this grouping, generating gut metagenomics data for additional time points from the same Swedish cohort. We evaluated the existence of PCS/TCS across different geographical regions and observed they are globally conserved features. To characterize PCS/TCS phenotypes, we performed bioreactor fermentation with faecal samples and metabolic modeling. Finally, using chronic disease gut metagenome and other multi-omics data, we identified roles of TCS in microbial dysbiosis and link with abnormal changes to host physiology.

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KW - Gastrointestinal Microbiome

KW - Humans

KW - Metagenomics/methods

KW - Sweden

KW - Bacteria/classification

KW - Feces/microbiology

KW - Longitudinal Studies

KW - Metagenome

KW - Adult

KW - Bioreactors/microbiology

KW - Fermentation

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U2 - 10.1038/s41522-024-00561-1

DO - 10.1038/s41522-024-00561-1

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SN - 2055-5008

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JO - npj Biofilms and Microbiomes

JF - npj Biofilms and Microbiomes

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ER -

Transient colonizing microbes promote gut dysbiosis and functional impairment

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