Host immunogenetic variation and gut microbiome functionality in a wild vertebrate population.

Abstract

BACKGROUND: The gut microbiome (GM) -important for host health and survival- is partially shaped by host immunogenetics. However, to date, no study has investigated the influence of host Major Histocompatibility Complex (MHC) genes on gut microbiome functionality in a wild population. Here we use a natural population of the Seychelles warbler (Acrocephalus sechellensis) to assess the effects of MHC genes on GM taxonomy and functionality using shotgun metagenomics. RESULTS: Our results show that taxonomic GM composition was associated with MHC-II diversity and the presence of one specific MHC-I allele (Ase-ua 7). Specifically, MHC-II diversity was associated with decreased Lactococcus lactis and increased Staphylococcus lloydii abundance, while Ase-ua 7 was linked to reduced Enterococcus casselifavus and Gordonia sp OPL2 but increased Escherichia coli and Vulcaniibacterium thermophilum. These taxonomic changes may reflect differences in MHC-mediated microbial recognition. In contrast, functional GM composition was significantly associated with increasing individual MHC-I diversity but not MHC-II diversity. In particular, increasing MHC-I diversity was associated with an increased prevalence of microbial defence genes but a reduced prevalence of microbial metabolism genes. Analysis also revealed that functional GM networks were more fragmented in high compared to low MHC-I diversity hosts. CONCLUSION: These results suggest that MHC variation (particularly at MHC-I) plays an important role in shaping both the taxonomy and function of the GM in wild vertebrates. In the Seychelles warbler, this results in trade-offs whereby there is an increase in microbial defence and a reduction in GM metabolic potential in individuals with higher MHC-I diversity. Thus, this work sheds light on the possible costs and benefits of maintaining a healthy microbiome, which is essential for understanding how the GM and immune system co-evolve. Video Abstract.