Effect of environmental factors and an emerging parasitic disease on gut microbiome of wild salmonid fish

Abstract

<p>The gastrointestinal tract (GIT) of fish supports a dynamic microbial ecosystem<br />that is intimately linked to host nutrient acquisition, epithelial development,<br />immune system priming, and disease prevention, and we are far from understanding<br />the complex interactions among parasites, symbiotic gut bacteria, and host fitness.<br />Here, we analyzed the effects of environmental factors and parasitic burdens on the<br />microbial composition and diversity within the GIT of the brown trout (Salmo trutta).<br />We focused on the emerging dangerous salmonid myxozoan parasite Tetracapsuloides<br />bryosalmonae, which causes proliferative kidney disease in salmonid fish, to<br />demonstrate the potential role of GIT micobiomes in the modulation of host-parasite<br />relationships. The microbial diversity in the GIT displayed clear clustering according<br />to the river of origin, while considerable variation was also found among fish from<br />the same river. Environmental variables such as oxygen concentration, water temperature,<br />and river morphometry strongly associated with both the river microbial<br />community and the GIT microbiome, supporting the role of the environment in microbial<br />assemblage and the relative insignificance of the host genotype and gender.<br />Contrary to expectations, the parasite load exhibited a significant positive relationship<br />with the richness of the GIT microbiome. Many operational taxonomic units<br />(OTUs; n 202) are more abundant in T. bryosalmonae-infected fish, suggesting that<br />brown trout with large parasite burdens are prone to lose their GIT microbiome homeostasis.<br />The OTUs with the strongest increase in infected trout are mostly nonpathogenic<br />aquatic, anaerobic sediment/sludge, or ruminant bacteria. Our results underscore<br />the significance of the interactions among parasitic disease, abiotic factors,<br />and the GIT microbiome in disease etiology.<br />IMPORTANCE Cohabiting microorganisms play diverse and important roles in the<br />biology of multicellular hosts, but their diversity and interactions with abiotic and biotic<br />factors remain largely unsurveyed. Nevertheless, it is becoming increasingly<br />clear that many properties of host phenotypes reflect contributions from the associated<br />microbiome. We focus on a question of how parasites, the host genetic background,<br />and abiotic factors influence the microbiome in salmonid hosts by using a<br />host-parasite model consisting of wild brown trout (Salmo trutta) and the myxozoan<br />Tetracapsuloides bryosalmonae, which causes widely distributed proliferative kidney<br />disease. We show that parasite infection increases the frequency of bacteria from<br />the surrounding river water community, reflecting impaired homeostasis in the fish<br />gut. Our results also demonstrate the importance of abiotic environmental factors<br />and host size in the assemblage of the gut microbiome of fish and the relative insignificance<br />of the host genotype and gender.<br /></p>