Dataset Information

Transgenerational plasticity and the capacity to adapt to low salinity in the eastern oyster, Crassostrea virginica.

ABSTRACT: Salinity conditions in oyster breeding grounds in the Gulf of Mexico are expected to drastically change due to increased precipitation from climate change and anthropogenic changes to local hydrology. We determined the capacity of the eastern oyster, Crassostrea virginica, to adapt via standing genetic variation or acclimate through transgenerational plasticity (TGP). We outplanted oysters to either a low- or medium-salinity site in Louisiana for 2 years. We then crossed adult parents using a North Carolina II breeding design, and measured body size and survival of larvae 5 dpf raised under low or ambient salinity. We found that TGP is unlikely to significantly contribute to low-salinity tolerance since we did not observe increased growth or survival in offspring reared in low salinity when their parents were also acclimated at a low-salinity site. However, we detected genetic variation for body size, with an estimated heritability of 0.68 ± 0.25 (95% CI). This suggests there is ample genetic variation for this trait to evolve, and that evolutionary adaptation is a possible mechanism through which oysters will persist with future declines in salinity. The results of this experiment provide valuable insights into successfully breeding low-salinity tolerance in this commercially important species.

SUBMITTER: Griffiths JS

PROVIDER: S-EPMC8131124 | biostudies-literature | 2021 May

REPOSITORIES: biostudies-literature

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Transgenerational plasticity and the capacity to adapt to low salinity in the eastern oyster, <i>Crassostrea virginica</i>.

Griffiths Joanna S JS Johnson Kevin M KM Sirovy Kyle A KA Yeats Mark S MS Pan Francis T C FTC La Peyre Jerome F JF Kelly Morgan W MW

Proceedings. Biological sciences 20210519 1951

Salinity conditions in oyster breeding grounds in the Gulf of Mexico are expected to drastically change due to increased precipitation from climate change and anthropogenic changes to local hydrology. We determined the capacity of the eastern oyster, <i>Crassostrea virginica</i>, to adapt via standing genetic variation or acclimate through transgenerational plasticity (TGP). We outplanted oysters to either a low- or medium-salinity site in Louisiana for 2 years. We then crossed adult parents usi ...[more]

PMID: 34004136

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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:Anthropogenic carbon emissions have resulted in drastic oceanic changes, including increased acidity, increased temperature, and decreased salinity. Anthropogenic carbon emissions have resulted in drastic oceanic changes, including increased acidity, increased temperature, and decreased salinity. Few studies have directly assessed the compounded impact of alterations to oceanic conditions on oyster physiology and the relation to the presence of V. parahaemolyticus. This project investigated the relationship between projected climate scenarios and their influence on both eastern oyster, Crassostrea virginica, and the aquatic bacteria, Vibrio parahaemolyticus. Specifically, we examined whether an increase in water temperature and/or decrease in salinity would impair oyster resistance to V. parahaemolyticus, a human food and waterborne pathogen. Using a culture-dependent approach, our data revealed that the alterations in environmental conditions did not significantly impact the numbers of V. parahaemolyticus numbers within oyster hemolymph or tissues. However, we did observe a dramatic increase in the total amount of bacteria and pathogenic native Vibrio species, Vibrio aestuarianus and Vibrio harveyi. Despite detecting V. parahaemolyticus in most tissues at 7 days post-challenge, oysters were able to reduce bacterial levels below our limit of detection by 28 days of exposure. Furthermore, in our second experimental trial exploring single vs. multiple inoculation of bacteria, we observed that oysters were either able to reduce total bacterial levels to pre-treatment burdens (i.e., below our limit of detection) or die. This study demonstrates that the synergistic effects of elevated temperature and decreased salinity do not inhibit oysters from preventing the long-term colonization of exogenous V. parahaemolyticus. However, our data do show these environmental stressors impact oyster physiology and the native microbiota. This can lead to the proliferation of opportunistic pathogens, which could have impacts on oyster population numbers and ecosystem and human health.

Project description:Marine invertebrate microbiomes play important roles in diverse host and ecological processes. However, a mechanistic understanding of host-microbe interactions is currently available for a small number of model organisms. Here, an integrated taxonomic and functional analysis of the microbiome of the eastern oyster, Crassostrea virginica, was performed using 16S rRNA gene-based amplicon profiling, shotgun metagenomics, and genome-scale metabolic reconstruction. Relatively high variability of the microbiome was observed across individual oysters and among different tissue types. Specifically, a significantly higher alpha diversity was observed in the inner shell than in the gut, gill, mantle, and pallial fluid samples, and a distinct microbiome composition was revealed in the gut compared to other tissues examined in this study. Targeted metagenomic sequencing of the gut microbiota led to further characterization of a dominant bacterial taxon, the class Mollicutes, which was captured by the reconstruction of a metagenome-assembled genome (MAG). Genome-scale metabolic reconstruction of the oyster Mollicutes MAG revealed a reduced set of metabolic functions and a high reliance on the uptake of host-derived nutrients. A chitin degradation and an arginine deiminase pathway were unique to the MAG compared to closely related genomes of Mollicutes isolates, indicating distinct mechanisms of carbon and energy acquisition by the oyster-associated Mollicutes A systematic reanalysis of public eastern oyster-derived microbiome data revealed a high prevalence of the Mollicutes among adult oyster guts and a significantly lower relative abundance of the Mollicutes in oyster larvae and adult oyster biodeposits.IMPORTANCE Despite their biological and ecological significance, a mechanistic characterization of microbiome function is frequently missing from many nonmodel marine invertebrates. As an initial step toward filling this gap for the eastern oyster, Crassostrea virginica, this study provides an integrated taxonomic and functional analysis of the oyster microbiome using samples from a coastal salt pond in August 2017. The study identified high variability of the microbiome across tissue types and among individual oysters, with some dominant taxa showing higher relative abundance in specific tissues. A high prevalence of Mollicutes in the adult oyster gut was revealed by comparative analysis of the gut, biodeposit, and larva microbiomes. Phylogenomic analysis and metabolic reconstruction suggested the oyster-associated Mollicutes is closely related but functionally distinct from Mollicutes isolated from other marine invertebrates. To the best of our knowledge, this study represents the first metagenomics-derived functional inference of Mollicutes in the eastern oyster microbiome.

Dataset Information

Transgenerational plasticity and the capacity to adapt to low salinity in the eastern oyster, Crassostrea virginica.

Publications

Transgenerational plasticity and the capacity to adapt to low salinity in the eastern oyster, <i>Crassostrea virginica</i>.

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