Stress-related gene transcription in fish exposed to parasitic larvae of two freshwater mussels with divergent infection strategies.

Abstract

Freshwater unionoid mussels have a unique life cycle involving a temporary parasitic phase. Their larvae (glochidia) attach to the gills or fins of fish hosts where they remain encysted until metamorphosis into free-living juveniles. The physiological response of fish during the critical period of glochidial attachment is not well understood, but recent work suggests that glochidia retention and survival is enhanced in stressed and cortisol-injected hosts. In this study, the early changes induced by glochidiosis were investigated for the first time at the transcriptional level. In 2 separate experiments, juvenile yellow perch Perca flavescens were inoculated with glochidia of Elliptio complanata (a host generalist) and Lampsilis radiata (a host specialist) following a standardized procedure. The transcriptional levels of 5 genes involved in the fish response to stress were assessed in the host liver and gills 24 h post-infection using quantitative real-time PCR. The number of encysted glochidia did not significantly differ between fish inoculated with E. complanata and L. radiata. Both species induced a 3-fold increase of 70 kDa heat-shock protein gene (hsp70) transcription in host liver. However, only E. complanata influenced the transcription of cortisol-regulated genes, notably glucocorticoid receptor DNA-binding factor 1 (grlf1). This gene, known to modulate tissue responsiveness to cortisol, was downregulated in infected fish compared to controls. Our findings suggest that different glochidia species interact with their fish host in distinct ways. Additional studies are required to address this hypothesis and further investigate the significance of the observed host transcriptional responses.