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Understanding Crassostrea virginica tolerance of Perkinsus marinus through global gene expression analysis
Dina A Proestou1, Mary E Sullivan1, Kathryn Markey Lundgren1
1National Cold Water Marine Aquaculture Center, USDA Agricultural Research Service, Kingston, RI, United States.
Abstract:
Disease tolerance, a host's ability to limit damage from a given parasite burden, is quantified by the relationship between pathogen load and host survival or reproduction. Dermo disease, caused by the protozoan parasite P. marinus, negatively impacts survival in both wild and cultured eastern oyster (C. virginica) populations. Resistance to P. marinus has been the focus of previous studies, but tolerance also has important consequences for disease management in cultured and wild populations. In this study we measured dermo tolerance and evaluated global expression patterns of two sensitive and two tolerant eastern oyster families experimentally challenged with distinct doses of P. marinus (0, 106, 107, and 108 parasite spores per gram wet weight, n = 3-5 individuals per family per dose). Weighted Gene Correlation Network Analysis (WGCNA) identified several modules correlated with increasing parasite dose/infection intensity, as well as phenotype. Modules positively correlated with dose included transcripts and enriched GO terms related to hemocyte activation and cell cycle activity. Additionally, these modules included G-protein coupled receptor, toll-like receptor, and tumor necrosis factor pathways, which are important for immune effector molecule and apoptosis activation. Increased metabolic activity was also positively correlated with treatment. The module negatively correlated with infection intensity was enriched with GO terms associated with normal cellular activity and growth, indicating a trade-off with increased immune response. The module positively correlated with the tolerant phenotype was enriched for transcripts associated with "programmed cell death" and contained a large number of tripartite motif-containing proteins. Differential expression analysis was also performed on the 108 dosed group using the most sensitive family as the comparison reference. Results were consistent with the network analysis, but signals for "programmed cell death" and serine protease inhibitors were stronger in one tolerant family than the other, suggesting that there are multiple avenues for disease tolerance. These results provide new insight for defining dermo response traits and have important implications for applying selective breeding for disease management.
Insights
Eastern oysters (C. virginica) exhibit disease tolerance to the parasite P. marinus. Gene expression analysis reveals distinct molecular pathways, including programmed cell death, associated with dermo disease tolerance and resistance.
Area of Science:
- Aquatic immunology
- Oyster aquaculture
- Disease ecology
Background:
- Dermo disease, caused by the protozoan parasite Perkinsus marinus (P. marinus), significantly reduces survival in eastern oyster (Crassostrea virginica) populations.
- While disease resistance has been studied, disease tolerance—the host's ability to limit damage despite parasite burden—is crucial for managing oyster populations.
Purpose of the Study:
- To quantify dermo disease tolerance in eastern oysters.
- To investigate global gene expression patterns in oysters with varying tolerance levels when challenged with P. marinus.
- To identify molecular mechanisms underlying disease tolerance for selective breeding.
Main Methods:
- Experimental challenge of four eastern oyster families (two sensitive, two tolerant) with four doses of P. marinus (0, 10^6, 10^7, 10^8 spores/g).
- Weighted Gene Correlation Network Analysis (WGCNA) to identify gene modules correlated with parasite dose and disease phenotype.
- Differential gene expression analysis comparing tolerant and sensitive families.
Main Results:
- Gene modules positively correlated with P. marinus dose were enriched for immune activation (hemocytes, G-protein coupled receptors, toll-like receptors, TNF pathways) and increased metabolic activity.
- A module negatively correlated with infection intensity showed enrichment for normal cellular activity and growth, suggesting a trade-off with immune response.
- The tolerant phenotype was associated with "programmed cell death" and tripartite motif-containing proteins, with variations between tolerant families.
Conclusions:
- Disease tolerance in oysters involves complex molecular mechanisms, including programmed cell death and potentially multiple pathways.
- Understanding these tolerance mechanisms can inform selective breeding strategies to enhance disease resistance in aquaculture and wild populations.
- This study provides novel insights into oyster immune responses and disease tolerance traits.
