Decoding host responses: How a freshwater invertebrate defends against a parasitic bacterium

Abstract

Host-parasite interactions drive coevolutionary dynamics, often leading to reciprocal adaptations between hosts and parasites, a process known as the Red Queen arms race. While the molecular mechanisms underlying vertebrate and insect immune responses have been studied extensively, those of aquatic invertebrates remain unexplored, despite their critical role in ecosystem stability and aquaculture. Here, we use the Daphnia magna-Pasteuria ramosa system to investigate the hosts immune response and the molecular mechanisms underlying host-parasite interactions. We inoculated 800 D. magna hosts with 20,000 mature spores of P. ramosa and tracked the progression of infection by measuring the proportion of infected individuals and the developmental stages of the parasite at multiple time points post-inoculation (hereafter p.i.). RNA sequencing was performed at key infection phases, early (Cauliflower stage), mid (Cauliflower and Grape stages), and terminal (Cauliflower, Grape, and Mature spore stages), to capture gene expression changes linked to infection dynamics. Our transcriptomic analyses revealed key immune genes involved in host defense, including genes involved in Toll signaling pathways, thereby revealing significant changes in pathways related to immune function, host metabolism, and resource allocation. Our findings suggest that iron sequestration may serve as a host defense strategy to restrict parasite growth, representing a form of nutritional immunity. Furthermore, pathways associated with infection-induced phenotypic traits, such as somatic growth, red coloration, and castration, were significantly upregulated, underscoring the impact of the infection on host physiology. Taken together, these findings provide new insights into the interplay between hosts and parasites at a molecular level in an ecologically relevant system, advancing our understanding of infection strategies in aquatic invertebrates.