Synergistic interaction of hyposalinity stress with Vibrio infection causes mass mortalities in oysters by inducing host microflora imbalance and immune dysregulation

A sudden drop in salinity following extreme precipitation events usually causes mass mortalities of oysters exposed to pathogens in ocean environment. While how hyposalinity stress interacts with pathogens to cause mass mortality remains obscure. In this study, we performed an experiment by mimicking hyposalinity stress and pathogen infection with V. alginolyticus to investigate their synergistic effect on the mortality of infected oysters toward understanding of the interaction among environment, host, and pathogen. We showed that hyposalinity stress (10{per thousand}, 20{per thousand} versus 30{per thousand}) did not significantly affect proliferation and virulence of V. alginolyticus, but significantly altered microbial composition and diversity in infected oysters. Microbial community profiling by 16S rRNA sequencing revealed disrupted homeostasis of digestive bacterial microbiota with increased abundance of several pathogenic bacteria, which may affect the pathogenesis in oysters. Transcriptome profiling of infected oysters revealed that a large number of genes associated with apoptosis and inflammation were significantly induced under hyposalinity, suggesting that hyposalinity stress may have triggered immune dysregulation in infected oysters. This work provides significant information in decoding mechanisms of synergistic interaction among environment factors, host genetics, and digestive microbiota, and how they contribute to pathogenesis. IMPORTANCERevealing the response of oyster host and microbial community to the interference of multiple environmental factors is an important aspect of deciphering the complex pathogenic mechanism in oysters. We evaluated the synergistic effects of hyposalinity stress and Vibrio alginolyticus infection in oysters. Results showed that hyposalinity stress significantly caused mass mortalities of infected oysters by destroying digestive microbial community structure, and triggering excessive immune response in oysters. This work provides valuable information for deciphering the mechanisms of synergistic interaction among environmental factors, host, and pathogens, and how they contribute to pathogenesis.