Dataset Information

Responses of an oyster host (Crassostrea virginica) and its protozoan parasite (Perkinsus marinus) to increasing air temperature.

ABSTRACT: Background:Changes in climate are predicted to influence parasite and pathogen infection patterns in terrestrial and marine environments. Increases in temperature in particular may greatly alter biological processes, such as host-parasite interactions. For example, parasites could differentially benefit from increased reproduction and transmission or hosts could benefit from elevated immune responses that may mediate or even eliminate infections. In the southeastern United States, the Eastern oyster, Crassostrea virginica, is infected by the lethal protozoan parasite, Perkinsus marinus. Under field conditions, intertidal (air-exposed) oysters have been found to have significantly higher P. marinus infection intensity and marginally higher infection prevalence than subtidal (submerged) oysters. During summer, air temperatures are much warmer than water and this exposure of intertidal oysters to higher temperatures is a suggested mechanism for increased infection intensity. Methods:We simulated intertidal exposure using controlled laboratory experiments to determine how host traits (survival and immune response) and parasite infection intensity will respond to elevated air temperature ranging from 27 °C to 53 °C during emersion at low tide. In Georgia, where our work was conducted, the average summer water temperature is 29 °C and the average maximum high air temperature in July is 33 °C (though oysters have been shown to survive at much higher air temperatures). Results:Host survival declined as temperature increased, with a definitive drop-off between 39-43 °C. Negative effects of air temperature on host immune response (phagocytic activity) were detectable only at extremely high temperatures (47-50 °C) when hosts were suffering acute mortality. Parasite infection intensity peaked at 35 °C. Discussion:Our results suggest that an increase in average summer air temperature to 35 °C or higher could affect oyster survival directly through temperature-related impacts in the short-term and indirectly through increased P. marinus infection intensity over the long-term.

SUBMITTER: Malek JC

PROVIDER: S-EPMC6033078 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Responses of an oyster host (<i>Crassostrea virginica</i>) and its protozoan parasite (<i>Perkinsus marinus</i>) to increasing air temperature.

Malek Jennafer C JC Byers James E JE

PeerJ 20180702

<h4>Background</h4>Changes in climate are predicted to influence parasite and pathogen infection patterns in terrestrial and marine environments. Increases in temperature in particular may greatly alter biological processes, such as host-parasite interactions. For example, parasites could differentially benefit from increased reproduction and transmission or hosts could benefit from elevated immune responses that may mediate or even eliminate infections. In the southeastern United States, the Ea ...[more]

PMID: 30002955

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Project description:Perkinsus marinus is a protozoan parasite of molluscs that can be propagated in vitro in a defined culture medium, in the absence of host cells. We previously reported that P. marinus trophozoites can be transfected with high efficiency by electroporation using a plasmid based on MOE, a highly expressed gene, and proposed its potential use as a "pseudoparasite." This is a novel gene expression platform for parasites of medical relevance for which the choice of the surrogate organism is based on phylogenetic affinity to the parasite of interest, while taking advantage of the whole engineered surrogate organism as a vaccination adjuvant. Here we improved the original transfection plasmid by incorporating a multicloning site, an enterokinase recognition sequence upstream of GFP, and a His-tag and demonstrate its potential suitability for the heterologous expression of Plasmodium sp. genes relevant to the development of anti-malarial vaccines. Plasmodium berghei HAP2 and MSP8, currently considered candidate genes for a malaria vaccine, were cloned into p[MOE]:GFP, and the constructs were used to transfect P. marinus trophozoites. Within 48 hr of transfection we observed fluorescent cells indicating that the P. berghei genes fused to GFP were expressed. The expression appeared to be transient for both P. berghei genes, as florescence of the transfectants diminished gradually over time. Although this heterologous expression system will require optimization for integration and constitutive expression of Plasmodium genes, our results represent attainment of proof for the "pseudoparasite" concept we previously proposed, as we show that the engineered P. marinus system has the potential to become a surrogate system suitable for expression of Plasmodium spp. genes of interest, which could eventually be used as a malaria vaccine delivery platform. The aim of the present study was to test the ability of marine protozoan parasite P. marinus to express genes of P. berghei .

Project description:Infectious disease outbreaks are causing widespread declines of marine invertebrates including corals, sea stars, shrimps, and molluscs. Dermo is a lethal infectious disease of the eastern oyster Crassostrea virginica caused by the protist Perkinsus marinus. The Pacific oyster Crassostrea gigas is resistant to Dermo due to differences in the host-parasite interaction that is not well understood. We compared transcriptomic responses to P. marinus challenge in the two oysters at early and late infection stages. Dynamic and orchestrated regulation of large sets of innate immune response genes were observed in both species with remarkably similar patterns for most orthologs, although responses in C. virginica were stronger, suggesting strong or over-reacting immune response could be a cause of host mortality. Between the two species, several key immune response gene families differed in their expansion, sequence variation and/or transcriptional response to P. marinus, reflecting evolutionary divergence in host-parasite interaction. Of note, significant upregulation of inhibitors of apoptosis (IAPs) was observed in resistant C. gigas but not in susceptible C. virginica, suggesting upregulation of IAPs is an active defense mechanism, not a passive response orchestrated by P. marinus. Compared with C. gigas, C. virginica exhibited greater expansion of toll-like receptors (TLRs) and positive selection in P. marinus responsive TLRs. The C1q domain containing proteins (C1qDCs) with the galactose-binding lectin domain that is involved in P. marinus recognition, were only present and significantly upregulated in C. virginica. These results point to previously undescribed differences in host defense genes between the two oyster species that may account for the difference in susceptibility, providing an expanded portrait of the evolutionary dynamics of host-parasite interaction in lophotrochozoans that lack adaptive immunity. Our findings suggest that C. virginica and P. marinus have a history of coevolution and the recent outbreaks may be due to increased virulence of the parasite.

Project description:BackgroundThe eastern oyster, Crassostrea virginica, is a euryhaline species that can thrive across a wide range of salinities (5-35). As with all estuarine species, individual oysters must be able to regulate their osmotic balance in response to constant temporal variation in salinity. At the population level, recurrent viability selection may be an additional mechanism shaping adaptive osmoregulatory phenotypes at the margins of oyster salinity tolerance. To identify candidate genes for osmoregulation, we sequenced, assembled, and annotated the transcriptome of wild juvenile eastern oysters from 'high' and 'low' salinity regimes. Annotations and candidates were mostly based on the Pacific oyster (Crassostrea gigas) genome sequence so osmoregulatory relevance in C. virginica was explored by testing functional enrichment of genes showing spatially discrete patterns of expression and by quantifying coding sequence divergence.ResultsThe assembly of sequence reads and permissive clustering of potentially oversplit alleles resulted in 98,729 reftigs (contigs and singletons). Of these, 50,736 were annotated with 9,307 belonging to a set of candidate osmoregulatory genes identified from the C. gigas genome. A total of 218,777 SNPs (0.0185 SNPs/bp) were identified in annotated reftigs of C. virginica. Amino acid divergence between translations of C. virginica annotated reftigs and C. gigas coding sequence averaged 23.2 % with an average dN/dS ratio of 0.074, suggesting purifying selection on protein sequences. The high and low salinity source oysters each expressed a subset of genes unique to that group, and the functions for these annotated genes were consistent with known molecular mechanisms for osmotic regulation in molluscs.ConclusionsMost of the osmoregulatory gene candidates experimentally identified in C. gigas are present in this C. virginica transcriptome. In general these congeners show coding sequence divergence too high to make the C. gigas genome a useful reference for C. virginica bioinformatics. However, strong purifying selection is characteristic of the osmoregulatory candidates so functional annotations are likely to correspond. An initial examination of C. virginica presence/absence expression patterns across the salinity gradient in a single estuary suggests that many of these candidates have expression patterns that co-vary with salinity, consistent with osmoregulatory function in C. virginica.

Dataset Information

Responses of an oyster host (Crassostrea virginica) and its protozoan parasite (Perkinsus marinus) to increasing air temperature.

Publications

Responses of an oyster host (<i>Crassostrea virginica</i>) and its protozoan parasite (<i>Perkinsus marinus</i>) to increasing air temperature.

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