Effects of chronic metal exposure and metamorphosis on the microbiomes of larval and adult insects and riparian spiders through the aquatic-riparian food web

Abstract

The macroinvertebrate microbiome controls various aspects of the host's physiology, from regulation of environmental contaminants to reproductive output. Aquatic insects provide critical nutritional subsidies linking aquatic and riparian food webs while simultaneously serving as a contaminant pathway for riparian insectivores in polluted ecosystems. Previous studies have characterized the transport and transfer of contaminants from aquatic to riparian ecosystems through insect metamorphosis, but both contaminant exposure and metamorphosis are energetically intensive processes that may cause host microbiomes to undergo radical transformation in structure and function, potentially affecting the host's physiology. We collected arthropods from three sites within Torch Lake, a historical copper mine in the Keweenaw Peninsula, Michigan, USA, and three sites within a nearby reference lake. Our objectives were to: 1) characterize the variation in microbiome communities and predicted metagenomic functions with legacy copper mining activity across space, among host types and family-level host taxonomy, 2) characterize how insect metamorphosis alters the microbiome community, including the degree of endosymbiotic infection, and predicted metagenomic function. We field-collected organisms, extracted their DNA, and sequenced the 16S region of the rRNA gene to characterize microbiome communities, then predicted metagenomic function. Site, lake, and host taxonomy affected the host microbiome community composition. Copper exposure increased the abundance of xenobiotic and lipid metabolism pathways in the Araneidae spider microbiome. Insect metamorphosis reduced the alpha diversity, altered the community composition, and predicted metagenomic function. We observed a bioconcentration of endosymbiotic bacteria in adult insects, especially holometabolous insects. Through metamorphosis, we observed a transition in function from xenobiotic degradation pathways to carbohydrate metabolism. Overall, contaminant exposure alters the microbiome composition in aquatic insects and riparian spiders and alters the function of the microbiome across the aquatic-riparian interface. Furthermore, metamorphosis is a critical element in shaping the aquatic insect microbiome across its life history.