Transient colonizing microbes promote gut dysbiosis and functional impairment.


Journal

NPJ biofilms and microbiomes
ISSN: 2055-5008
Titre abrégé: NPJ Biofilms Microbiomes
Pays: United States
ID NLM: 101666944

Informations de publication

Date de publication:
08 Sep 2024
Historique:
received: 20 11 2023
accepted: 27 08 2024
medline: 9 9 2024
pubmed: 9 9 2024
entrez: 8 9 2024
Statut: epublish

Résumé

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.

Identifiants

pubmed: 39245657
doi: 10.1038/s41522-024-00561-1
pii: 10.1038/s41522-024-00561-1
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

80

Subventions

Organisme : RCUK | Engineering and Physical Sciences Research Council (EPSRC)
ID : EP/S001301/1
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/S016899/1
Organisme : Science for Life Laboratory (SciLifeLab)
ID : N/A

Informations de copyright

© 2024. The Author(s).

Références

Faith, J. J. et al. The long-term stability of the human gut microbiota. Science 341, 1237439 (2013).
pubmed: 23828941 pmcid: 3791589 doi: 10.1126/science.1237439
Fassarella, M. et al. Gut microbiome stability and resilience: elucidating the response to perturbations in order to modulate gut health. Gut 70, 595 (2021).
pubmed: 33051190 doi: 10.1136/gutjnl-2020-321747
Palleja, A. et al. Recovery of gut microbiota of healthy adults following antibiotic exposure. Nat. Microbiol. 3, 1255–1265 (2018).
pubmed: 30349083 doi: 10.1038/s41564-018-0257-9
Kostic, A. D. et al. The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes. Cell Host Microbe 17, 260–273 (2015).
pubmed: 25662751 pmcid: 4689191 doi: 10.1016/j.chom.2015.01.001
Schirmer, M. et al. Compositional and Temporal Changes in the Gut Microbiome of Pediatric Ulcerative Colitis Patients Are Linked to Disease Course. Cell Host Microbe 24, 600–610.e604 (2018).
pubmed: 30308161 pmcid: 6277984 doi: 10.1016/j.chom.2018.09.009
Smith, M. I. et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 339, 548–554 (2013).
pubmed: 23363771 pmcid: 3667500 doi: 10.1126/science.1229000
Stewart, C. J. et al. Temporal development of the gut microbiome in early childhood from the TEDDY study. Nature 562, 583–588 (2018).
pubmed: 30356187 pmcid: 6415775 doi: 10.1038/s41586-018-0617-x
Vatanen, T. et al. Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life. Nat. Microbiol. 4, 470–479 (2019).
pubmed: 30559407 doi: 10.1038/s41564-018-0321-5
Levy, R. et al. Longitudinal analysis reveals transition barriers between dominant ecological states in the gut microbiome. Proc. Natl Acad. Sci. USA 117, 13839–13845 (2020).
pubmed: 32471946 pmcid: 7306764 doi: 10.1073/pnas.1922498117
Roodgar, M. et al. Longitudinal linked-read sequencing reveals ecological and evolutionary responses of a human gut microbiome during antibiotic treatment. Genome Res. 31, 1433–1446 (2021).
pubmed: 34301627 pmcid: 8327913 doi: 10.1101/gr.265058.120
Wen, C. et al. Quantitative metagenomics reveals unique gut microbiome biomarkers in ankylosing spondylitis. Genome Biol. 18, 142 (2017).
pubmed: 28750650 pmcid: 5530561 doi: 10.1186/s13059-017-1271-6
van Dijk, L. R. et al. StrainGE: a toolkit to track and characterize low-abundance strains in complex microbial communities. Genome Biol. 23, 74 (2022).
pubmed: 35255937 pmcid: 8900328 doi: 10.1186/s13059-022-02630-0
Xie, H. et al. Shotgun Metagenomics of 250 Adult Twins Reveals Genetic and Environmental Impacts on the Gut Microbiome. Cell Syst. 3, 572–584.e573 (2016).
pubmed: 27818083 pmcid: 6309625 doi: 10.1016/j.cels.2016.10.004
Wirbel, J. et al. Meta-analysis of fecal metagenomes reveals global microbial signatures that are specific for colorectal cancer. Nat. Med. 25, 679–689 (2019).
pubmed: 30936547 pmcid: 7984229 doi: 10.1038/s41591-019-0406-6
Low, H. H. et al. Structure of a type IV secretion system. Nature 508, 550–553 (2014).
pubmed: 24670658 pmcid: 3998870 doi: 10.1038/nature13081
Emiola, A. & Oh, J. High throughput in situ metagenomic measurement of bacterial replication at ultra-low sequencing coverage. Nat. Commun. 9, 4956 (2018).
pubmed: 30470746 pmcid: 6251912 doi: 10.1038/s41467-018-07240-8
Bidkhori, G. & Shoaie, S. MIGRENE: The Toolbox for Microbial and Individualized GEMs,Reactobiome and Community Network Modelling. Metab. 14, 132 (2024).
Magnúsdóttir, S. et al. Generation of genome-scale metabolic reconstructions for 773 members of the human gut microbiota. Nat. Biotechnol. 35, 81–89 (2017).
pubmed: 27893703 doi: 10.1038/nbt.3703
Shoaie, S. et al. Quantifying Diet-Induced Metabolic Changes of the Human Gut Microbiome. Cell Metab. 22, 320–331 (2015).
pubmed: 26244934 doi: 10.1016/j.cmet.2015.07.001
Tramontano, M. et al. Nutritional preferences of human gut bacteria reveal their metabolic idiosyncrasies. Nat. Microbiol. 3, 514–522 (2018).
pubmed: 29556107 doi: 10.1038/s41564-018-0123-9
Meslier, V. et al. Mediterranean diet intervention in overweight and obese subjects lowers plasma cholesterol and causes changes in the gut microbiome and metabolome independently of energy intake. Gut 69, 1258 (2020).
pubmed: 32075887 doi: 10.1136/gutjnl-2019-320438
Mehta, R. S. et al. Stability of the human faecal microbiome in a cohort of adult men. Nat. Microbiol. 3, 347–355 (2018).
pubmed: 29335554 pmcid: 6016839 doi: 10.1038/s41564-017-0096-0
Qin, J. et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490, 55–60 (2012).
pubmed: 23023125 doi: 10.1038/nature11450
Qin, N. et al. Alterations of the human gut microbiome in liver cirrhosis. Nature 513, 59–64 (2014).
pubmed: 25079328 doi: 10.1038/nature13568
Jie, Z. et al. The gut microbiome in atherosclerotic cardiovascular disease. Nat. Commun. 8, 845 (2017).
pubmed: 29018189 pmcid: 5635030 doi: 10.1038/s41467-017-00900-1
Olsson, L. M. et al. Dynamics of the normal gut microbiota : A longitudinal one-year population study in Sweden. Cell Host Microbe 30, 726–739.e723 (2022).
pubmed: 35349787 doi: 10.1016/j.chom.2022.03.002
Deleersnijder, W. et al. Isolation of markers for chondro-osteogenic differentiation using cDNA library subtraction. Molecular cloning and characterization of a gene belonging to a novel multigene family of integral membrane proteins. J. Biol. Chem. 271, 19475–19482 (1996).
pubmed: 8702637 doi: 10.1074/jbc.271.32.19475
Tuckermann, J. P., Pittois, K., Partridge, N. C., Merregaert, J. & Angel, P. Collagenase-3 (MMP-13) and integral membrane protein 2a (Itm2a) are marker genes of chondrogenic/osteoblastic cells in bone formation: sequential temporal, and spatial expression of Itm2a, alkaline phosphatase, MMP-13, and osteocalcin in the mouse. J. Bone Min. Res. 15, 1257–1265 (2000).
doi: 10.1359/jbmr.2000.15.7.1257
Kirchner, J. & Bevan, M. J. ITM2A is induced during thymocyte selection and T cell activation and causes downregulation of CD8 when overexpressed in CD4(+)CD8(+) double positive thymocytes. J. Exp. Med. 190, 217–228 (1999).
pubmed: 10432285 pmcid: 2195576 doi: 10.1084/jem.190.2.217
Van den Plas, D. & Merregaert, J. Constitutive overexpression of the integral membrane protein Itm2A enhances myogenic differentiation of C2C12 cells. Cell Biol. Int. 28, 199–207 (2004).
pubmed: 14984746 doi: 10.1016/j.cellbi.2003.11.019
Lin, Y. T. et al. Indole-3 acetic acid increased risk of impaired cognitive function in patients receiving hemodialysis. Neurotoxicology 73, 85–91 (2019).
pubmed: 30826344 doi: 10.1016/j.neuro.2019.02.019
Rosario, D. et al. Systematic analysis of gut microbiome reveals the role of bacterial folate and homocysteine metabolism in Parkinson’s disease. Cell Rep. 34, 108807 (2021).
pubmed: 33657381 doi: 10.1016/j.celrep.2021.108807
Ravi, A. et al. Loss of microbial diversity and pathogen domination of the gut microbiota in critically ill patients. Micro. Genom. 5, e000293 (2019).
David, L. A. et al. Host lifestyle affects human microbiota on daily timescales. Genome Biol. 15, R89 (2014).
pubmed: 25146375 pmcid: 4405912 doi: 10.1186/gb-2014-15-7-r89
Jalanka-Tuovinen, J. et al. Intestinal Microbiota in Healthy Adults: Temporal Analysis Reveals Individual and Common Core and Relation to Intestinal Symptoms. PLOS ONE 6, e23035 (2011).
pubmed: 21829582 pmcid: 3145776 doi: 10.1371/journal.pone.0023035
Schmidt, T. S. et al. Extensive transmission of microbes along the gastrointestinal tract. Elife 8, e42693 (2019).
pubmed: 30747106 pmcid: 6424576 doi: 10.7554/eLife.42693
Alazawi, W. et al. Periodontitis is associated with significant hepatic fibrosis in patients with non-alcoholic fatty liver disease. PLoS One 12, e0185902 (2017).
pubmed: 29220367 pmcid: 5722374 doi: 10.1371/journal.pone.0185902
Qin, N. et al. Opposing effects of HIF1α and HIF2α on chromaffin cell phenotypic features and tumor cell proliferation: Insights from MYC-associated factor X. Int. J. Cancer 135, 2054–2064 (2014).
pubmed: 24676840 doi: 10.1002/ijc.28868
Hu, S. et al. Ectopic gut colonization: a metagenomic study of the oral and gut microbiome in Crohn’s disease. Gut Pathog. 13, 13 (2021).
pubmed: 33632307 pmcid: 7905567 doi: 10.1186/s13099-021-00409-5
Fischetti, V. A. et al. Gram-positive pathogens (John Wiley & Sons, 2019).
Makki, K., Deehan, E. C., Walter, J. & Bäckhed, F. The Impact of Dietary Fiber on Gut Microbiota in Host Health and Disease. Cell Host Microbe 23, 705–715 (2018).
pubmed: 29902436 doi: 10.1016/j.chom.2018.05.012
Yang, W. & Cong, Y. Gut microbiota-derived metabolites in the regulation of host immune responses and immune-related inflammatory diseases. Cell Mol. Immunol. 18, 866–877 (2021).
pubmed: 33707689 pmcid: 8115644 doi: 10.1038/s41423-021-00661-4
Sampson, T. R. et al. Gut Microbiota Regulate Motor Deficits and Neuroinflammation in a Model of Parkinson’s Disease. Cell 167, 1469–1480.e1412 (2016).
pubmed: 27912057 pmcid: 5718049 doi: 10.1016/j.cell.2016.11.018
Remund, B., Yilmaz, B. & Sokollik, C. D-Lactate: Implications for Gastrointestinal Diseases. Child 10, 945 (2023).
doi: 10.3390/children10060945
Ghoshal, U. C. et al. Asian-Pacific consensus on small intestinal bacterial overgrowth in gastrointestinal disorders: An initiative of the Indian Neurogastroenterology and Motility Association. Indian J. Gastroenterol. 41, 483–507 (2022).
pubmed: 36214973 pmcid: 9549446 doi: 10.1007/s12664-022-01292-x
Bergström, G. et al. The Swedish CArdioPulmonary BioImage Study: objectives and design. J. Intern. Med. 278, 645–659 (2015).
pubmed: 26096600 pmcid: 4744991 doi: 10.1111/joim.12384
Pons, N. et al. METEOR, a platform for quantitative metagenomic profiling of complex ecosystems. In International Conference on Biology, Informatics, and Mathematics, JOBIM, Montpelier, France, 7–9 (2010).
Lee, S. et al. Global compositional and functional states of the human gut microbiome in health and disease. Genome Res. 34, 967–978 (2024).
Le Chatelier, E. et al. Richness of human gut microbiome correlates with metabolic markers. Nature 500, 541–546 (2013).
pubmed: 23985870 doi: 10.1038/nature12506
Ruppé, E. et al. Prediction of the intestinal resistome by a three-dimensional structure-based method. Nat. Microbiol. 4, 112–123 (2019).
pubmed: 30478291 doi: 10.1038/s41564-018-0292-6
Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M. & Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, D490–D495 (2014).
pubmed: 24270786 doi: 10.1093/nar/gkt1178
Svartström, O. et al. Ninety-nine de novo assembled genomes from the moose (Alces alces) rumen microbiome provide new insights into microbial plant biomass degradation. ISME J. 11, 2538–2551 (2017).
pubmed: 28731473 pmcid: 5648042 doi: 10.1038/ismej.2017.108
Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59–60 (2015).
pubmed: 25402007 doi: 10.1038/nmeth.3176
Gillespie, J. J. et al. PATRIC: the comprehensive bacterial bioinformatics resource with a focus on human pathogenic species. Infect. Immun. 79, 4286–4298 (2011).
pubmed: 21896772 pmcid: 3257917 doi: 10.1128/IAI.00207-11
Mao, C. et al. Curation, integration and visualization of bacterial virulence factors in PATRIC. Bioinformatics 31, 252–258 (2015).
pubmed: 25273106 doi: 10.1093/bioinformatics/btu631
Mukherjee, S. et al. Genomes OnLine database (GOLD) v.7: updates and new features. Nucleic Acids Res. 47, D649–d659 (2019).
pubmed: 30357420 doi: 10.1093/nar/gky977
Blin, K. et al. antiSMASH 4.0-improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res. 45, W36–W41 (2017).
pubmed: 28460038 pmcid: 5570095 doi: 10.1093/nar/gkx319
Tagliamonte, S. et al. Mediterranean diet consumption affects the endocannabinoid system in overweight and obese subjects: possible links with gut microbiome, insulin resistance and inflammation. Eur. J. Nutr. 60, 3703–3716 (2021).
pubmed: 33763720 pmcid: 8437855 doi: 10.1007/s00394-021-02538-8
Ideker, T., Ozier, O., Schwikowski, B. & Siegel, A. F. Discovering regulatory and signalling circuits in molecular interaction networks. Bioinformatics 18, S233–S240 (2002).
pubmed: 12169552 doi: 10.1093/bioinformatics/18.suppl_1.S233
Deschamps, C. et al. Comparative methods for fecal sample storage to preserve gut microbial structure and function in an in vitro model of the human colon. Appl. Microbiol. Biotechnol. 104, 10233–10247 (2020).
pubmed: 33085024 doi: 10.1007/s00253-020-10959-4
Thévenot, J. et al. Enterohemorrhagic Escherichia coli O157:H7 survival in an in vitro model of the human large intestine and interactions with probiotic yeasts and resident microbiota. Appl. Environ. Microbiol. 79, 1058–1064 (2013).
pubmed: 23204410 pmcid: 3568547 doi: 10.1128/AEM.03303-12
Mitchell, A. L. et al. MGnify: the microbiome analysis resource in 2020. Nucleic Acids Res. 48, D570–D578 (2020).
pubmed: 31696235
Arkin, A. P. et al. KBase: The United States Department of Energy Systems Biology Knowledgebase. Nat. Biotechnol. 36, 566–569 (2018).
pubmed: 29979655 pmcid: 6870991 doi: 10.1038/nbt.4163

Auteurs

Sunjae Lee (S)

Centre for Host-Microbiome Interactions, Faculty of Dentistry, Oral & Craniofacial Sciences, King's College London, London, SE1 9RT, UK.
School of Life Sciences, Gwangju Institute of Science and Technology, Jouy-en-Josas, 61005, Republic of Korea.

Victoria Meslier (V)

University Paris-Saclay, INRAE, MetaGenoPolis, 78350, Jouy-en-Josas, France.

Gholamreza Bidkhori (G)

Centre for Host-Microbiome Interactions, Faculty of Dentistry, Oral & Craniofacial Sciences, King's College London, London, SE1 9RT, UK.

Fernando Garcia-Guevara (F)

Centre for Host-Microbiome Interactions, Faculty of Dentistry, Oral & Craniofacial Sciences, King's College London, London, SE1 9RT, UK.
Science for Life Laboratory, KTH - Royal Institute of Technology, Stockholm, SE-171 21, Sweden.

Lucie Etienne-Mesmin (L)

Université Clermont Auvergne, INRAE, UMR 454 MEDIS, 28 place Henri Dunant, F-63000, Clermont-Ferrand, France.

Frederick Clasen (F)

Centre for Host-Microbiome Interactions, Faculty of Dentistry, Oral & Craniofacial Sciences, King's College London, London, SE1 9RT, UK.

Junseok Park (J)

Department of Bio and Brain Engineering, KAIST, 291 Daehak-ro, Yuseong-gu, Daejeon, 305-701, Republic of Korea.

Florian Plaza Oñate (F)

University Paris-Saclay, INRAE, MetaGenoPolis, 78350, Jouy-en-Josas, France.

Haizhuang Cai (H)

Centre for Host-Microbiome Interactions, Faculty of Dentistry, Oral & Craniofacial Sciences, King's College London, London, SE1 9RT, UK.

Emmanuelle Le Chatelier (E)

University Paris-Saclay, INRAE, MetaGenoPolis, 78350, Jouy-en-Josas, France.

Nicolas Pons (N)

University Paris-Saclay, INRAE, MetaGenoPolis, 78350, Jouy-en-Josas, France.

Marcela Pereira (M)

Centre for Translational Microbiome Research, Department of Microbiology, Tumour and Cell Biology, Karolinska Institutet, Stockholm, SE-171 77, Sweden.

Maike Seifert (M)

Centre for Translational Microbiome Research, Department of Microbiology, Tumour and Cell Biology, Karolinska Institutet, Stockholm, SE-171 77, Sweden.

Fredrik Boulund (F)

Centre for Translational Microbiome Research, Department of Microbiology, Tumour and Cell Biology, Karolinska Institutet, Stockholm, SE-171 77, Sweden.

Lars Engstrand (L)

Centre for Translational Microbiome Research, Department of Microbiology, Tumour and Cell Biology, Karolinska Institutet, Stockholm, SE-171 77, Sweden.

Doheon Lee (D)

Department of Bio and Brain Engineering, KAIST, 291 Daehak-ro, Yuseong-gu, Daejeon, 305-701, Republic of Korea.

Gordon Proctor (G)

Centre for Host-Microbiome Interactions, Faculty of Dentistry, Oral & Craniofacial Sciences, King's College London, London, SE1 9RT, UK.

Adil Mardinoglu (A)

Centre for Host-Microbiome Interactions, Faculty of Dentistry, Oral & Craniofacial Sciences, King's College London, London, SE1 9RT, UK.
Science for Life Laboratory, KTH - Royal Institute of Technology, Stockholm, SE-171 21, Sweden.

Stéphanie Blanquet-Diot (S)

Université Clermont Auvergne, INRAE, UMR 454 MEDIS, 28 place Henri Dunant, F-63000, Clermont-Ferrand, France.

David Moyes (D)

Centre for Host-Microbiome Interactions, Faculty of Dentistry, Oral & Craniofacial Sciences, King's College London, London, SE1 9RT, UK.

Mathieu Almeida (M)

University Paris-Saclay, INRAE, MetaGenoPolis, 78350, Jouy-en-Josas, France.

S Dusko Ehrlich (SD)

University Paris-Saclay, INRAE, MetaGenoPolis, 78350, Jouy-en-Josas, France.

Mathias Uhlen (M)

Science for Life Laboratory, KTH - Royal Institute of Technology, Stockholm, SE-171 21, Sweden.

Saeed Shoaie (S)

Centre for Host-Microbiome Interactions, Faculty of Dentistry, Oral & Craniofacial Sciences, King's College London, London, SE1 9RT, UK. saeed.shoaie@kcl.ac.uk.
Science for Life Laboratory, KTH - Royal Institute of Technology, Stockholm, SE-171 21, Sweden. saeed.shoaie@kcl.ac.uk.

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