Characterization of water microbiota and their relationship with resident oysters during an oyster mortality event.

Microorganisms are vital for the health of marine invertebrates, and their assembly is driven by both deterministic and stochastic factors that regulate residents (innate to the host) and transients (from ambient water). However, the role of water microbiota and the significance of deterministic and stochastic processes in aquatic hosts facing mortality threats are largely unknown. This study examines the shifts in water microbiota during an oyster mortality event using amplicon sequencing and compared with those of resident oysters to disentangle the balance of the deterministic and stochastic factors involved. Water temperature and dissolved oxygen significantly shape the microbial community with a distinct monthly pattern, and Cyanobacteria blooms might exacerbate oyster mortality. The comparative analysis of microbial communities in oysters and water revealed that ≤ 21% of the genera were shared between oysters and water, implying that water microbiota cannot easily transfer into oysters. Furthermore, these shared genera had different functions, with oysters more involved in promoting host digestion and nutrient acquisition and water bacteria enriched more in functions promoting their own growth and survival. These findings illustrate that oysters may possess specific selection or barrier mechanisms that permit a small percentage of transients, controlled by stochastic factors and having a minimal effect on oyster mortality, to enter, whereas the majority of oyster microbiota are residents governed by deterministic factors. Consequently, oysters exhibit some plasticity in their symbiotic microbiota, enabling them to maintain microbial homeostasis and adapt to complex microbial surroundings. This may be a shared mechanism among marine invertebrates for survival in complex marine environments.IMPORTANCEPacific oysters are widely cultured and play vital ecological roles. However, the summer mortality hinders sustainable oyster farming. Untangling causative mechanisms of oyster mortality is a complex task due to the intricate "interactome" involving environmental factors, hosts, and pathogens. Interactions between hosts and microorganisms offer an ideal avenue for investigating the truth. We systematically investigated the microbial community in water and resident oysters during a summer mortality event and proposed that the assembly of oyster microbiota is primarily governed by deterministic processes independent of mortality. Pathogens mainly originate from resident members of the oyster microbiota, with a limited influence from the microbial community in the water. Additionally, environmental degraders, such as Cyanobacteria blooms, cannot be overlooked as a contributing factor of oyster mortality. This study evaluated the weight of deterministic and stochastic factors in microbial assembly during an oyster mortality event and greatly broadened our understanding of the "interactome" through the interaction between oysters and water in microbiota.

Host-microbiota interactions play a crucial role in oyster adaptation to rising seawater temperature in summer.

Climate change, represented by rising and fluctuating temperature, induces systematic changes in marine organisms and in their bacterial symbionts. However, the role of host-microbiota interactions in the host's response to rising temperature and the underlying mechanisms are incompletely understood in marine organisms. Here, the symbiotic intestinal microbiota and transcriptional responses between diploid and triploid oysters that displayed susceptible and resistant performance under the stress of rising temperature during a summer mortality event were compared to investigate the host-microbiota interactions. The rising and fluctuating temperatures triggered an earlier onset and higher mortality in susceptible oysters (46.7%) than in resistant oysters (17.3%). Correlation analysis between microbial properties and environmental factors showed temperature was strongly correlated with indices of α-diversity and the abundance of top 10 phyla, indicating that temperature significantly shaped the intestinal microbiota of oysters. The microbiota structure of resistant oysters exhibited more rapid changes in composition and diversity compared to susceptible oysters before peak mortality, indicating that resistant oysters possessed a stronger ability to regulate their symbiotic microbiota. Meanwhile, linear discriminant analysis effect size (LefSe) analysis found that the probiotics Verrucomicrobiales and Clostridiales were highly enriched in resistant oysters, and that potential pathogens Betaproteobacteriales and Acidobacteriales were enriched in susceptible oysters. These results implied that the symbiotic microbiota played a significant role in the oysters' adaptation to rising temperature. Accompanying the decrease in unfavorable bacteria before peak mortality, genes related to phagocytosis and lysozymes were upregulated and the xenobiotics elimination pathway was exclusively expressed in resistant oysters, demonstrating the validity of these immunological functions in controlling proliferation of pathogens driven by rising temperature. Compromised immunological functions might lead to proliferation of pathogens in susceptible oysters. This study might uncover a conserved mechanism of adaptation to rising temperature in marine invertebrates from the perspective of interactions between host and symbiotic microbiota.