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The Spatial Heterogeneity of the Gut Limits Predation and Fosters Coexistence of Bacteria and Bacteriophages

Authors :
Luisa De Sordi
Thierry Pedron
Claudia Eberl
Lorenzo Chaffringeon
Quentin Lamy-Besnier
Pascal Campagne
Marion Bérard
Laurent Debarbieux
Bärbel Stecher
Marta Lourenço
Bactériophage, bactérie, hôte - Bacteriophage, bacterium, host
Institut Pasteur [Paris]
Collège doctoral [Sorbonne universités]
Sorbonne Université (SU)
Centre de Recherche Saint-Antoine (CR Saint-Antoine)
Sorbonne Université (SU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-CHU Saint-Antoine [AP-HP]
Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Sorbonne Université (SU)-Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Sorbonne Université (SU)
Université Paris Descartes - Paris 5 (UPD5)
Hub Bioinformatique et Biostatistique - Bioinformatics and Biostatistics HUB
Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS)
Max von Pettenkofer-Institut for Hygiene and Medical Microbiology
Ludwig-Maximilians-Universität München (LMU)
Animalerie centrale (Plate-forme)
German Center for Infection Research, Partnersite Munich (DZIF)
Institut Carnot Pasteur Maladie Infectieuse ANR-11-CARN-017-01
M.L. is part of the Pasteur - Paris University (PPU) International PhD Program. M.L. is funded by Institut Carnot Pasteur Maladie Infectieuse (ANR 11-CARN 017-01). L.D.S. is funded by a Roux-Cantarini fellowship from the Institut Pasteur (Paris, France). L.C. is funded by a PhD fellowships from the Ministère de l’Enseignement Supérieur et de la Recherche, France, École Doctorale n°394. Q.L.-B. is funded by École Doctorale FIRE - Program Bettencourt. B.S. is supported by the German Center of Infection Research (DZIF), the Center for Gastrointestinal Microbiome Research (CEGIMIR), the DFG, Germany, Priority Programme SPP1656 (STE 1971/4-2 and STE 1971/6-1), and the Collaborative Research Center CRC 1371.
We thank Harald Brüssow for critically reading the manuscript and Jorge Moura de Sousa for valuable discussion and opinion on early versions of the manuscript. We thank Dwayne Roach and Anne Chevallereau for valuable discussions. We thank Sean Benler for kindly sharing the comprehensive HMM database of Ig-like domains identified on Pfam database. We thank the members of the Centre for Gnotobiology Platform of the Institut Pasteur (Thierry Angélique, Eddie Maranghi, Martine Jacob, and Marisa Gabriela Lopez Dieguez) for their help with the animal work. We thank Cédric Fund for 16S libraries and sequencing from the Biomics Platform, C2RT, Institut Pasteur, Paris, France, supported by France Génomique (ANR-10-INBS-09-09) and IBISA.
Institut Pasteur [Paris] (IP)
Collège Doctoral
Centre de Recherche Saint-Antoine (CRSA)
Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)
Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)
Cova Rodrigues, Ana
Source :
Cell Host & Microbe, Cell Host & Microbe, 2020, 28 (3), pp.390-401.e5. ⟨10.1016/j.chom.2020.06.002⟩
Publication Year :
2020
Publisher :
HAL CCSD, 2020.

Abstract

International audience; The ecological dynamics underlying the coexistence between antagonistic populations of bacteria and their viruses, bacteriophages (phages), in the mammalian gut microbiota remain poorly understood. We challenged a murine synthetic bacterial community with phages to study the factors allowing phages-bacteria coexistence. Coexistence was not dependent on the development of phage-resistant clones nor on the ability of phages to extend their host range. Instead, our data suggest that phage-inaccessible sites in the mucosa serve as a spatial refuge for bacteria. From there, bacteria disseminate in the gut lumen where they are predated by luminal phages fostering the presence of intestinal phage populations. The heterogeneous biogeography of microbes contributes to the long-term coexistence of phages with phage-susceptible bacteria. This observation could explain the persistence of intestinal phages in humans as well as the low efficiency of oral phage therapy against enteric pathogens in animal models and clinical trials.

Details

Language :
English
ISSN :
19313128
Database :
OpenAIRE
Journal :
Cell Host & Microbe, Cell Host & Microbe, 2020, 28 (3), pp.390-401.e5. ⟨10.1016/j.chom.2020.06.002⟩
Accession number :
edsair.doi.dedup.....bd7b1f3a6cef5ac348495243527b8a94