Abstract
Until recently, the study of major histocompability complex (MHC) mediated immunity has focused on the direct link between MHC diversity and susceptibility to parasite infection. However, MHC genes can also influence host health indirectly through the sculpting of the bacterial community that in turn shape immune responses. We investigated the links between MHC class I and II gene diversity gut microbiome diversity and micro- (adenovirus, AdV) and macro- (helminth) parasite infection probabilities in a wild population of non-human primates, mouse lemurs of Madagascar. This setup encompasses a plethora of underlying interactions between parasites, microbes and adaptive immunity in natural populations. Both MHC classes explained shifts in microbiome composition and the effect was driven by a few select microbial taxa. Among them were three taxa (Odoribacter, Campylobacter and Prevotellaceae-UCG-001) which were in turn linked to AdV and helminth infection status, correlative evidence of the indirect effect of the MHC via the microbiome. Our study provides support for the coupled role of MHC diversity and microbial flora as contributing factors of parasite infection.
Highlights
Reciprocal interactions between the hosts’ immune system and the gut microbial flora are essential in defining the course of a parasitic challenge for three main reasons
Consistent with previous work on mouse lemurs [32, 36], AdV and helminth prevalence in our study population was high; 29.4% of individuals tested AdVpos (42 from the 143 individuals screened for AdV infection), 40.1% of individuals (35 from the 85 individuals screened for helminth infection) were infected with helminths, and 8.6% of individuals were co-infected with AdV and helminths (10 from the 85 individuals screened for both AdV and helminth infection)
We detected a total of 226 MHC class I region (MHCI) functional alleles in the population and based on physicochemical variables (z-values [37]) of the amino acid sites affected by positive selection (PSS) and grouped them into 17 major histocompatibility complex (MHC) supertypes (ST) (Materials and methods, S1 Fig and S1 Table)
Summary
Reciprocal interactions between the hosts’ immune system and the gut microbial flora are essential in defining the course of a parasitic challenge for three main reasons. Specific bacterial taxa can prime immune signaling that provoke the activation of an inflammatory response against parasites [1, 2]. The competitive advantage of commensal bacterial taxa over a niche can limit the growth and expansion of pathogenic bacteria [5, 6]. Evidence of these and other forms of colonization resistance underscore the relevance of immune mechanisms that encourage a balanced state between tolerance towards commensal bacteria and resistance against offending invaders [7, 8]. The involvement of the major histocompatibility complex (MHC) in antigen-specific immune response appears to contribute to microbial colonization [12,13,14], the interplay between the natural variation of the MHC and microbial communities in parasite resistance has yet to be explored
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