Comparative Transcriptome Analysis of Two Oysters, Crassostrea gigas and Crassostrea hongkongensis Provides Insights into Adaptation to Hypo-Osmotic Conditions

Abstract

Environmental salinity creates a key barrier to limit the distribution of most aquatic organisms. Adaptation to osmotic fluctuation is believed to be a factor facilitating species diversification. Adaptive evolution often involves beneficial mutations at more than one locus. Bivalves hold great interest, with numerous species living in waters, as osmoconformers, who maintain the osmotic pressure balance mostly by free amino acids. In this study, 107,076,589 reads from two groups of Crassostrea hongkongensis were produced and the assembled into 130,629 contigs. Transcripts putatively involved in stress-response, innate immunity and cell processes were identified according to Gene ontology and KEGG pathway analyses. Comparing with the transcriptome of C. gigas to characterize the diversity of transcripts between species with osmotic divergence, we identified 182,806 high-quality single nucleotide polymorphisms (SNPs) for C. hongkongensis, and 196,779 SNPs for C. gigas. Comparison of 11,602 pairs of putative orthologs allowed for identification of 14 protein-coding genes that experienced strong positive selection (Ka/Ks>1). In addition, 45 genes that may show signs of moderate positive selection (1≥Ka/Ks>0.5) were also identified. Based on Ks ratios and divergence time between the two species published previously, we estimated a neutral transcriptome-wide substitution mutation rate of 1.39×10−9 per site per year. Several genes were differentially expressed across the control and treated groups of each species. This is the first time to sequence the transcriptome of C. hongkongensis and provide the most comprehensive transcriptomic resource available for it. The increasing amount of transcriptome data on Crassostrea provides an excellent resource for phylogenetic analysis. A large number of SNPs identified in this work are expected to provide valuable resources for future marker and genotyping assay development. The analysis of natural selection provides an innovative view on the adaptation within species and sets the basis for future genetic and evolutionary studies.

Genetic variation and population structure of the Pacific oyster Crassostrea gigas in the northwestern Pacific inferred from mitochondrial COI sequences

“…In contrast, the CDW seemingly fails to hinder the dispersal of the C. gigas larvae. No significant genetic differentiation of C. gigas was detected in line with the Changjiang River discharge, which may mainly benefit from its strong adaptability to various environments such as a euryhaline adaptation mechanism [60,61]. Obviously, weak genetic structure, as revealed by mtCOI data in this study, is consistent with the view that marine organisms with larval stages often show low genetic differentiation among populations as a result of high dispersal capabilities and large-scale oceanic mixture [62,63].…”

Transcriptomic responses to extreme low salinity among locally adapted populations of Olympia oyster (Ostrea lurida)

“…Relative to OP and M populations, laboratory‐raised oysters originating from LL increase and decrease transcripts encoding regulators of apoptosis and cell cycle progression at the control salinity. Modulating expression of apoptotic genes is a fundamental component of the hyposmotic stress response in oysters (Yan et al., ; Zhang et al., ; Zhao, Yu, Kong, & Li, ), suggesting natural selection could act upon apoptotic pathways to modify salinity tolerance in LL oysters (Zhao, Yu, Kong, Liu, & Li, ). Examination of the Pacific oyster genome reveals an expanded apoptosis regulatory system, which is thought to have evolved to deal with widespread environmental variation characteristic of estuary habitats.…”

Phenotypic and transcriptomic responses to salinity stress across genetically and geographically divergent Tigriopus californicus populations

“…For example, larvae of the Chinese mitten crab Eriocheir sinensis differentially expressed 33 genes related to transport processes during the migration from their natal sea water to adult freshwater habitat (Hui et al., ). Ion transport genes were up‐regulated under low salinity stress in the killifish Fundulus heteroclitus (Brennan et al., ) and showed evidence of being under positive selection in the oyster Crassostrea hongkongensis (Zhao, Yu, Kong, Liu, & Li, ). We did not observe functional enrichment for ion transport among our list of transcripts differentially regulated under low salinity.…”