Insights into early stages of the establishment of host:algal endosymbioses: Genetic responses to live versus heat-killed algae and bacterial prey in a sponge host

Abstract

The freshwater sponge Ephydatia muelleri and its Chlorella-like green algal partner is an emerging model for studying animal:algal endosymbiosis. The sponge host is a highly tractable laboratory organism, and the symbiotic algae are easily cultured. We took advantage of these traits to experimentally interrogate fundamental questions about cellular mechanisms that govern the establishment of durable intracellular partnerships between hosts and symbionts in facultative symbioses. We modified a classical experimental approach to discern the phagocytotic mechanisms that might be co-opted to permit persistent infections, and identified genes differentially expressed in E. muelleri sponges early in the establishment of endosymbiosis. We exposed algal-free E. muelleri to live native algal symbionts, native heat-killed algae, and bacteria, and then performed RNASeq so we could compare patterns of gene expression in each treatment. We contrasted differential gene expression patterns between potential food items (bacteria and heat-killed algae) and the live native Chlorella-like symbiont. We found a relatively small but interesting suite of genes that are uniquely and differentially expressed in the host exposed to live algal symbionts, and a larger number of genes uniquely triggered by host exposure to heat-killed algae. One of the host genes, an ABC transporter that is downregulated in response to live algal symbionts, was further evaluated for its possible role in establishment of the algal symbiosis. We discuss the gene expression profiles associated with host responses to living algal cells in the context of conditions necessary for long-term residency within host cells by phototrophic symbionts as well as the genetic responses to sponge phagocytosis and immune driven pathways.