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Elevated temperature attenuates ovarian functions and induces apoptosis and oxidative stress in the American oyster, Crassostrea virginica: potential mechanisms and signaling pathways.

ABSTRACT: Global climate change is predicted to intensify thermal stress in marine and coastal organisms, affecting their development, growth, and reproductive functions. In this study, we performed histological observations on ovarian development, immunohistochemical analyses of ovarian heat shock protein-70 (HSP70), nitrotyrosine protein (NTP, an indicator of reactive nitrogen species (RNS)), and dinitrophenyl protein (DNP, an indicator of protein oxidation) expressions, in situ TUNEL assay for cellular apoptosis, biochemical analyses of ovarian caspase-3/7 activity and protein carbonyl (PC, a measure of reactive oxygen species (ROS)) contents, nitrate/nitrite (NOx) levels, and extrapallial fluid (EPF, an important body fluid) pH in the American oyster, Crassostrea virginica. Oysters were exposed to medium (28 °C) and high (32 °C) temperatures under controlled laboratory conditions for 1 week. Oysters exposed to higher temperatures significantly decreased the number and diameter of eggs, and EPF protein concentrations compared with controls (24 °C). In contrast, EPF pH, ovarian HSP70 mRNA levels, and protein expression were increased after heat exposure, consistent with increased ovarian apoptosis. The enhanced apoptosis in ovaries was associated with increased ovarian caspase-3/7 activity, PC contents, NOx levels, and NTP and DNP expressions in heat-exposed oysters. Collectively, these results suggest that higher temperatures drastically increase RNS and ROS levels, increasing incidence of apoptosis and subsequently reducing ovarian functions in oysters.

SUBMITTER: Nash S

PROVIDER: S-EPMC6717220 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Elevated temperature attenuates ovarian functions and induces apoptosis and oxidative stress in the American oyster, Crassostrea virginica: potential mechanisms and signaling pathways.

Nash Sarah S Johnstone Jackson J Rahman Md Saydur MS

Cell stress & chaperones 20190730 5

Global climate change is predicted to intensify thermal stress in marine and coastal organisms, affecting their development, growth, and reproductive functions. In this study, we performed histological observations on ovarian development, immunohistochemical analyses of ovarian heat shock protein-70 (HSP70), nitrotyrosine protein (NTP, an indicator of reactive nitrogen species (RNS)), and dinitrophenyl protein (DNP, an indicator of protein oxidation) expressions, in situ TUNEL assay for cellular ...[more]

PMID: 31363994

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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.

Project description:BackgroundChanges 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.MethodsWe 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).ResultsHost 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.DiscussionOur 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.

Dataset Information

Elevated temperature attenuates ovarian functions and induces apoptosis and oxidative stress in the American oyster, Crassostrea virginica: potential mechanisms and signaling pathways.

Publications

Elevated temperature attenuates ovarian functions and induces apoptosis and oxidative stress in the American oyster, Crassostrea virginica: potential mechanisms and signaling pathways.

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