Literature DB >> 28973938

Interhost dispersal alters microbiome assembly and can overwhelm host innate immunity in an experimental zebrafish model.

Adam R Burns1, Elizabeth Miller2, Meghna Agarwal3, Annah S Rolig3, Kathryn Milligan-Myhre4, Steve Seredick5, Karen Guillemin3,6, Brendan J M Bohannan2.   

Abstract

The diverse collections of microorganisms associated with humans and other animals, collectively referred to as their "microbiome," are critical for host health, but the mechanisms that govern their assembly are poorly understood. This has made it difficult to identify consistent host factors that explain variation in microbiomes across hosts, despite large-scale sampling efforts. While ecological theory predicts that the movement, or dispersal, of individuals can have profound and predictable consequences on community assembly, its role in the assembly of animal-associated microbiomes remains underexplored. Here, we show that dispersal of microorganisms among hosts can contribute substantially to microbiome variation, and is able to overwhelm the effects of individual host factors, in an experimental test of ecological theory. We manipulated dispersal among wild-type and immune-deficient myd88 knockout zebrafish and observed that interhost dispersal had a large effect on the diversity and composition of intestinal microbiomes. Interhost dispersal was strong enough to overwhelm the effects of host factors, largely eliminating differences between wild-type and immune-deficient hosts, regardless of whether dispersal occurred within or between genotypes, suggesting dispersal can independently alter the ecology of microbiomes. Our observations are consistent with a predictive model that assumes metacommunity dynamics and are likely mediated by dispersal-related microbial traits. These results illustrate the importance of microbial dispersal to animal microbiomes and motivate its integration into the study of host-microbe systems.

Entities:  

Keywords:  dispersal; innate immunity; metacommunity; microbiome; zebrafish

Mesh:

Substances:

Year:  2017        PMID: 28973938      PMCID: PMC5651736          DOI: 10.1073/pnas.1702511114

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  39 in total

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2.  Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB.

Authors:  T Z DeSantis; P Hugenholtz; N Larsen; M Rojas; E L Brodie; K Keller; T Huber; D Dalevi; P Hu; G L Andersen
Journal:  Appl Environ Microbiol       Date:  2006-07       Impact factor: 4.792

3.  Microbiota signalling through MyD88 is necessary for a systemic neutrophilic inflammatory response.

Authors:  Dipti Karmarkar; Kenneth L Rock
Journal:  Immunology       Date:  2013-12       Impact factor: 7.397

4.  Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system.

Authors:  Wendy S Garrett; Graham M Lord; Shivesh Punit; Geanncarlo Lugo-Villarino; Sarkis K Mazmanian; Susumu Ito; Jonathan N Glickman; Laurie H Glimcher
Journal:  Cell       Date:  2007-10-05       Impact factor: 41.582

5.  Effects of patch connectivity and heterogeneity on metacommunity structure of planktonic bacteria and viruses.

Authors:  Steven A J Declerck; Christian Winter; Jonathan B Shurin; Curtis A Suttle; Blake Matthews
Journal:  ISME J       Date:  2012-11-22       Impact factor: 10.302

6.  Fast gapped-read alignment with Bowtie 2.

Authors:  Ben Langmead; Steven L Salzberg
Journal:  Nat Methods       Date:  2012-03-04       Impact factor: 28.547

7.  Intestinal inflammation targets cancer-inducing activity of the microbiota.

Authors:  Janelle C Arthur; Ernesto Perez-Chanona; Marcus Mühlbauer; Sarah Tomkovich; Joshua M Uronis; Ting-Jia Fan; Barry J Campbell; Turki Abujamel; Belgin Dogan; Arlin B Rogers; Jonathan M Rhodes; Alain Stintzi; Kenneth W Simpson; Jonathan J Hansen; Temitope O Keku; Anthony A Fodor; Christian Jobin
Journal:  Science       Date:  2012-08-16       Impact factor: 47.728

8.  Innate immunity and intestinal microbiota in the development of Type 1 diabetes.

Authors:  Li Wen; Ruth E Ley; Pavel Yu Volchkov; Peter B Stranges; Lia Avanesyan; Austin C Stonebraker; Changyun Hu; F Susan Wong; Gregory L Szot; Jeffrey A Bluestone; Jeffrey I Gordon; Alexander V Chervonsky
Journal:  Nature       Date:  2008-09-21       Impact factor: 49.962

9.  Social networks predict gut microbiome composition in wild baboons.

Authors:  Jenny Tung; Luis B Barreiro; Michael B Burns; Jean-Christophe Grenier; Josh Lynch; Laura E Grieneisen; Jeanne Altmann; Susan C Alberts; Ran Blekhman; Elizabeth A Archie
Journal:  Elife       Date:  2015-03-16       Impact factor: 8.140

10.  Cohabiting family members share microbiota with one another and with their dogs.

Authors:  Se Jin Song; Christian Lauber; Elizabeth K Costello; Catherine A Lozupone; Gregory Humphrey; Donna Berg-Lyons; J Gregory Caporaso; Dan Knights; Jose C Clemente; Sara Nakielny; Jeffrey I Gordon; Noah Fierer; Rob Knight
Journal:  Elife       Date:  2013-04-16       Impact factor: 8.140

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  51 in total

1.  Analysis of the gut and gill microbiome of resistant and susceptible lines of rainbow trout (Oncorhynchus mykiss).

Authors:  Ryan M Brown; Gregory D Wiens; Irene Salinas
Journal:  Fish Shellfish Immunol       Date:  2018-12-01       Impact factor: 4.581

2.  Epithelial delamination is protective during pharmaceutical-induced enteropathy.

Authors:  Scott T Espenschied; Mark R Cronan; Molly A Matty; Olaf Mueller; Matthew R Redinbo; David M Tobin; John F Rawls
Journal:  Proc Natl Acad Sci U S A       Date:  2019-08-07       Impact factor: 11.205

Review 3.  Primate microbiomes over time: Longitudinal answers to standing questions in microbiome research.

Authors:  Johannes R Björk; Mauna Dasari; Laura Grieneisen; Elizabeth A Archie
Journal:  Am J Primatol       Date:  2019-04-02       Impact factor: 2.371

4.  Ecological Correlates of Large-Scale Turnover in the Dominant Members of Pseudacris crucifer Skin Bacterial Communities.

Authors:  Myra C Hughey; Eric R Sokol; Jenifer B Walke; Matthew H Becker; Lisa K Belden
Journal:  Microb Ecol       Date:  2019-04-04       Impact factor: 4.552

Review 5.  Ecological and evolutionary mechanisms underlying patterns of phylosymbiosis in host-associated microbial communities.

Authors:  Kevin D Kohl
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2020-03-23       Impact factor: 6.237

6.  Successive passaging of a plant-associated microbiome reveals robust habitat and host genotype-dependent selection.

Authors:  Norma M Morella; Francis Cheng-Hsuan Weng; Pierre M Joubert; C Jessica E Metcalf; Steven Lindow; Britt Koskella
Journal:  Proc Natl Acad Sci U S A       Date:  2019-12-05       Impact factor: 11.205

Review 7.  Timescales of gut microbiome dynamics.

Authors:  Brandon H Schlomann; Raghuveer Parthasarathy
Journal:  Curr Opin Microbiol       Date:  2019-11-02       Impact factor: 7.934

8.  Evolutionary and ecological consequences of gut microbial communities.

Authors:  Nancy A Moran; Howard Ochman; Tobin J Hammer
Journal:  Annu Rev Ecol Evol Syst       Date:  2019-08-29       Impact factor: 13.915

9.  Drainage of inflammatory macromolecules from the brain to periphery targets the liver for macrophage infiltration.

Authors:  Linlin Yang; Jessica A Jiménez; Alison M Earley; Victoria Hamlin; Victoria Kwon; Cameron T Dixon; Celia E Shiau
Journal:  Elife       Date:  2020-07-31       Impact factor: 8.140

10.  Swimming motility of a gut bacterial symbiont promotes resistance to intestinal expulsion and enhances inflammation.

Authors:  Travis J Wiles; Brandon H Schlomann; Elena S Wall; Reina Betancourt; Raghuveer Parthasarathy; Karen Guillemin
Journal:  PLoS Biol       Date:  2020-03-20       Impact factor: 8.029

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