Variation in global transcriptomatic response to Perkinsus marinus infection among Eastern oyster families highlights potential mechanisms of disease resistance

Authors: Proestou, Dina; SULLIVAN, MARY - University Of Rhode Island

Submitted to: Fish and Shellfish Immunology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/1/2019
Publication Date: 12/3/2019
Citation: Proestou, D.A., Sullivan, M. 2019. Variation in global transcriptomatic response to Perkinsus marinus infection among Eastern oyster families highlights potential mechanisms of disease resistance. Fish and Shellfish Immunology. 96:141-151.

Interpretive Summary: Dermo disease, caused by the protozoan parasite Perkinsus marinus, is a persistent problem constraining the Eastern oyster aquaculture industry, yet the mechanistic bases for parasite pathogenicity and the host’s response are poorly understood. In order to gain insight to this consequential host-pathogen interaction, we leveraged two recent developments: 1) the quantification of genetic variation for Dermo-resistance traits in an Eastern oyster breeding population and 2) the release of a high-quality, annotated eastern oyster reference genome. In this manuscript, we describe the results of a laboratory disease challenge and subsequent global gene expression profiling of a Dermo-resistant and susceptible family in response to P. marinus injection. The two families exhibited strikingly different transcriptomic responses to the parasite. Whereas the resistant family mounted a strong, focused, early response to challenge, the susceptible family’s response was weak and ineffective. Our results will advance our understanding of the mechanisms underlying Dermo resistance in the Eastern oyster and contribute to more effective disease management strategies, including selective breeding for Dermo resistance.

Technical Abstract: Dermo disease, caused by the protozoan parasite Perkinsus marinus, negatively impacts wild and cultured Eastern oyster populations, yet our knowledge of the mechanistic bases for parasite pathogenicity and the Eastern oyster’s response to it is limited. To better understand host responses to the parasite and identify molecular mechanisms underlying disease-resistance phenotypes, we experimentally challenged two families exhibiting divergent Dermo-resistance phenotypes with the parasite, generated global expression profiles using RNAseq and identified differentially expressed transcripts between control and challenged oysters from each family at multiple time points post-parasite injection. The susceptible and resistant families exhibited strikingly different transcriptomic responses to the parasite over a 28-day time period. The resistant family exhibited a strong, focused, early response to P. marinus infection, where many significantly upregulated transcripts were associated with the biological processes “regulation of proteolysis” and “oxidation-reduction process.” P. marinus virulence factors are mainly comprised of proteases that facilitate parasite invasion and weaken host humoral defenses, thus host upregulation of transcripts associated with negative regulation of proteolysis is consistent with a Dermo-resistant phenotype. In contrast, the susceptible family mounted a very weak, disorganized, initial response to the parasite. Few transcripts were differentially expressed between control and injected oysters, and no functional enrichment was detected among them. At the final 28 d time point 2450 differentially expressed transcripts were identified and were associated with either “G-protein coupled receptor activity” (upregulated) or “microtubule-based process” (downregulated). A handful of protease inhibitors were differentially expressed between control and injected susceptible oysters, but this function was not enriched in the susceptible data set. The differential expression patterns observed in this study provide valuable insight into the functional basis of Dermo resistance and suggest that the timing of expression is just as important as the transcripts being expressed.