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

The Olympia oyster (Ostrea lurida) is a foundation species inhabiting estuaries along the North American west coast. In California estuaries, O. lurida is adapted to local salinity regimes and populations differ in low salinity tolerance. In this study, oysters from three California populations were reared for two generations in a laboratory common garden and subsequently exposed to low salinity seawater. Comparative transcriptomics was then used to understand species-level responses to hyposmotic stress and population-level mechanisms underlying divergent salinity tolerances. Gene expression patterns indicate Olympia oysters are sensitive to hyposmotic stress: All populations respond to low salinity by up-regulating transcripts indicative of protein unfolding, DNA damage and cell cycle arrest after sub-lethal exposure. Among O. lurida populations, transcriptomic profiles differed constitutively and in response to low salinity. Despite two generations in common-garden conditions, transcripts encoding apoptosis modulators were constitutively expressed at significantly different levels in the most tolerant population. Expression of cell death regulators may facilitate cell fate decisions when salinity declines. Following low salinity exposure, oysters from the more tolerant population expressed a small number of mRNAs at significantly higher levels than less tolerant populations. Proteins encoded by these transcripts regulate ciliary activity within the mantle cavity and may function to prolong valve closure and reduce mortality in low salinity seawater. Collectively, gene expression patterns suggest sub-lethal impacts of hyposmotic stress in Olympia oysters are considerable and that even oysters with greater low salinity tolerance may be vulnerable to future freshwater flooding events.