The gut microbiota response to helminth infection depends on host sex and genotype

Abstract

Vertebrates’ gut microbial communities can be altered by the hosts’ parasites. Helminths inhabiting the gut lumen can interact directly with their host’s microbiota via physical contact, chemical products, or competition for nutrients. Indirect interactions can also occur, for instance when helminths induce or suppress host immunity in ways that have collateral effects on the microbiota. If there is genetic variation in host immune responses to parasites, we would expect such indirect effects to be conditional on host genotype. To test for such genotype by infection interactions, we experimentally exposed Gasterosteus aculeatus to their naturally co-evolved parasite, Schistocephalus solidus. The host microbiota differed in response to parasite exposure, and between infected and uninfected fish. The magnitude and direction of microbial responses to infection differed between host sexes, and also differed between variants at autosomal quantitative trait loci. These results indicate that host genotype and sex regulate the effect of helminth infection on a vertebrate gut microbiota. If this result holds in other taxa, especially humans, then helminth-based therapeutics for dysbiosis might need to be tailored to host genotype and sex.

The host phenotype and microbiome varies with infection status, parasite origin and parasite microbiome composition

“…Our results indicate that the microbiome composition of fish exposed to S. solidus strongly depends on host genotype. In control individuals, we observed host genotype-specific constitutive differences in microbiome composition that confirm that host-based selective processes shape the organism microbiota [86][87][88], probably due to constitutive differences in immune gene expression pathways between populations [33,73,89,90]. In agreement, we found host-genotype dependent differences in the relationship between key immune genes and abundance of bacterial families, indicating that fish of different origins have developed different sensitivity to different bacterial families.…”

“…Regardless of host or parasite genotype, and regardless of the lab environment, exposure and infection by S. solidus were associated with consistent changes in the microbiome. Indeed, herein, and within Ling et al [36], a significant increase in Rhodobacteriales was found associated with exposure and infection by S. solidus. In addition, both our field study and experimental infections revealed a previously unreported increase in alpha diversity metrics and bacterial load in infected individuals.…”

“…We also observed variations among studies that may be due to differences in environmental conditions, of using sticklebacks with different genetic background, and from using different strains of parasites. Indeed, while Ling et al [36] showed an increase in Lactobacilliales in infected individuals, we observed an increase in Vibrionales and Desulfovibrionales following experimental infection and field sampling, respectively. The colonization of the gut of infected fish by these bacteria may be dependent on their initial presence in the environment of the fish.…”

“…Conversely, geographic variation in host immune response imposes selection pressures on parasites that locally adapt to their hosts and display different virulence mechanisms [34,35]. However, it remains to be determined whether this fine-tuned crosstalk between host immune response and parasite virulence impacts host microbiota [36]. The finding that a single parasite species can differentially impact the immune system and microbiota of different host species [37], and conversely, that a single host species host different bacterial communities depending on the parasite species it is infected with [38], support this hypothesis.…”

Immune Gene Expression Covaries with Gut Microbiome Composition in Stickleback

“…Here, we report evidence for covariation between hosts' gene expression and their gut microbiota, from a large sample of laboratory-bred three-spined stickleback (Gasterosteus aculeatus), a small fish native to northern temperate coastal marine and freshwater habitats. Like many vertebrates, individual stickleback harbor hundreds of microbial taxa (operational taxonomic units [OTUs]) in their intestines (46)(47)(48)(49). The composition of this microbiota differs dramatically between cooccurring individuals within a given natural population and between populations (between neighboring lakes, adjacent lakes and streams, or marine versus freshwater [ (46)(47)(48)(50)(51)(52)).…”