Microbiota Succession Influences Nematode Physiology in a Beetle Microcosm Ecosystem

Abstract

Research during the last decade has generated a substantial understanding of the role of microbiota in animal development, metabolism and immunity, including humans. However, many organismal interactions involve microbial successions, such as in animal decay but also human health and disease. The complexity of most microbiota makes it difficult to obtain insight into such microbial successions, resulting in a limited understanding of microbiota for ecosystem functioning. One potential, relatively simple, model system for the analysis of microbial successions is insect decay in soil ecosystems, a highly abundant process that has however, not been investigated in detail. For example, microbiota and nematodes are the two most abundant groups of organisms in soil systems, but their interplay and successions during the decomposition of insects are currently unknown. Here, we use a semi-artificial decaying rose chafer grub microcosm to study the reciprocal interactions between microbiota and nematodes through metagenomics and transcriptomic studies. We show that the controlled addition of nematodes to beetle grub carcasses will strongly influence the microbial succession and result in a massive increase in microbial diversity. Nematodes select microbes of high nutritional value for consumption, thereby influencing the composition of microbiota on the decaying insect. Reciprocally, the activity of nematode metabolic pathways strongly responds to their microbial diet and affects fat metabolism and the formation of dauer larvae, the nematode dispersal stage. These results indicate the importance of microbial successions and their reciprocal interactions with nematodes for insect decay in soil ecosystems.