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

Abstract

Background: A growing literature demonstrates the impact of helminths on their host gut microbiome. However, there is now a need to investigate helminth associated microbes and the complex tripartite interactions between parasite, microbes, and hosts. Methods: We investigated whether the stickleback host microbiome depends on eco-evolutionary variables by testing the impact of exposure to the parasite Schistocephalus solidus, infection success, host genotype, parasite genotype, and parasite microbiome composition. Results: We observed constitutive differences in the microbiome of stickleback of different origin that increased when sticklebacks exposed to the parasite resisted infection. In contrast, the microbiome of successfully infected sticklebacks varies with parasite genotype. More specifically, we reveal that the association between microbiome and immune gene expression increases in infected individuals, and varies with parasite genotype. In addition, we showed that S. solidus hosts a complex endo-microbiome and that the abundance and prevalence of an unknown Chloroflexi in the parasite correlate with expression of host immune genes including foxp3, tnfr1, cd97, stat6 and marco. Conclusions: Within this first comprehensive analysis of a cestode’s interaction with bacteria, we demonstrate that (i) regardless of infection success, parasites contribute to modulating the host microbiome, (ii). when infection is successful, the host microbiome varies with parasite genotype due to genotype-dependent variation in parasite immunomodulation, and (iii) the parasite-associated microbiome is distinct from its host’s and contribute to the host immune response to infection. While a growing number of studies focus on determining the genetic and environmental factors contributing to host microbiome composition, this study reveals that parasites, parasite genetic factors, and parasite microbiomes can contribute regardless of whether the infection was successful.

A framework for testing the impact of co-infections on host gut microbiomes

“…D Single infections can also lead to both stochastic and deterministic effects. Three-spined stickleback ( Gasterosteus aculeatus ), for instance, infected with the cestode Schistocephalus solidus had a more dispersed and shifted gut microbial community [ 22 ]. * = significant differences (i.e., p -value < 0.05); ns = non-significant differences (i.e., p -value > 0.05) …”

“…D Single infections can also lead to both stochastic and deterministic effects. Three-spined stickleback (Gasterosteus aculeatus), for instance, infected with the cestode Schistocephalus solidus had a more dispersed and shifted gut microbial community [22]. * = significant differences (i.e., p-value < 0.05); ns = non-significant differences (i.e., p-value > 0.05) bacterium "Candidatus Neoehrlichia mikurensis" were co-infected with the zoonotic Lyme disease agent Borrelia afyelii [31]; and 79% of field voles (Microtus agrestis) were co-infected with a protozoan, virus and/or bacteria [32]; 72% of helminth-infected marbled spinefoot rabbit fish Siganus rivulatus were also infected with at least one additional helminth species [33]; viral co-infections in virus-positive bats range from approximately 1% [34] to up to 40% [35].…”