Immunogenetic variation shapes the gut microbiome in a natural vertebrate population

Davies, Charli S., Worsley, Sarah, Maher, Kathryn, Komdeur, Jan, Burke, Terry, Dugdale, Hannah and Richardson, David S. (2022) Immunogenetic variation shapes the gut microbiome in a natural vertebrate population. Microbiome, 10. ISSN 2049-2618

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Abstract

Background: The gut microbiome (GM) can influence many biological processes in the host, impacting its health and survival, but the GM can also be influenced by the host’s traits. In vertebrates, Major Histocompatibility Complex (MHC) genes play a pivotal role in combatting pathogens and are thought to shape the host’s GM. Despite this—and the documented importance of both GM and MHC variation to individual fitness—few studies have investigated the association between the GM and MHC in the wild. Results: We characterised MHC class I (MHC-I), MHC class II (MHC-II) and GM variation in individuals within a natural population of the Seychelles warbler (Acrocephalus sechellensis). We determined how the diversity and composition of the GM varied with MHC characteristics, in addition to environmental factors and other host traits. Our results show that the presence of specific MHC alleles, but not MHC diversity, influences both the diversity and composition of the GM in this population. MHC-I alleles, rather than MHC-II alleles, had the greatest impact on the GM. GM diversity was negatively associated with the presence of three MHC-I alleles (Ase-ua3, Ase-ua4, Ase-ua5), and one MHC-II allele (Ase-dab4), while changes in GM composition were associated with the presence of four different MHC-I alleles (Ase-ua1, Ase-ua7, Ase-ua10, Ase-ua11). There were no associations between GM diversity and TLR3 genotype, but GM diversity was positively correlated with genome-wide heterozygosity and varied with host age and field period. Conclusions: These results suggest that components of the host’s immune system play a role in shaping the GM of wild animals. Host genotype—specifically MHC-I and to a lesser degree MHC-II variation—can modulate the GM, although whether this occurs directly, or indirectly through effects on host health, is unclear. Importantly, if immune genes can regulate host health through modulation of the microbiome, then it is plausible that the microbiome could also influence selection on immune genes. As such, host–microbiome coevolution may play a role in maintaining functional immunogenetic variation within natural vertebrate populations.

Item Type: Article
Additional Information: Funding Information: CSD was funded by the Natural Environment Research Council and EnvEast DTP (NE/L002582/1). The MHC laboratory work was supported by the UK Natural Environment Research Council (NERC) Biomolecular Analysis Facility at the University of Sheffield (NBAF1150). The microbiome sequencing was funded by a NERC NBAF Pilot Scheme Grant (NBAF1092) and by a NERC grant (NE/S010939/1) to DSR. Acknowledgements: We thank the Seychelles Bureau of Standards and the Department of Environment for permission to conduct fieldwork overall and Nature Seychelles for facilitating fieldwork on Cousin Island. This study would not have been possible without the contribution of exceptional fieldworkers and technicians. We particularly thank Gavin Horsburgh for assistance in MHC sequencing, Maria-Elena Mannarelli for assistance extracting the faecal samples, and Marco van der Velde for microsatellite genotyping. Bacterial data generation and analysis were carried out by the Centre for Genomic Research, University of Liverpool. The research presented in this paper was carried out on the High-Performance Computing Clusters supported respectively by the Research and Specialist Computing Support service at the University of East Anglia and IT Services at the University of Sheffield.
Uncontrolled Keywords: acrocephalus sechellensis,genetic variation,gut microbiome,life history,major histocompatibility complex,microbial diversity,microbiology,microbiology (medical) ,/dk/atira/pure/subjectarea/asjc/2400/2404
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 15 Mar 2022 16:30
Last Modified: 10 May 2022 00:40
URI: https://ueaeprints.uea.ac.uk/id/eprint/84058
DOI: 10.1186/s40168-022-01233-y

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