Impacts of climate-driven upwelling intensification on the microbiota and health of cultivated scallops

Abstract

The scallop Argopecten purpuratus plays a pivotal role as an economic resource cultivated in regions where climate change may intensify the coastal upwelling. This process has the potential to impact host-microbiota interactions. Hence, we conducted a field study to investigate the effects of varying upwelling intensities on hemolymph and gill microbiota dynamics (utilizing 16S rRNA gene sequencing), as well as the pathological state of A. purpuratus maintained in culture systems. Helicobactereaceae and Arcobactereaceae emerged as the prevailing families within both the hemolymph and gills. In contrast to the period of weak upwelling, the phase characterized by intensified upwelling revealed notable shifts in the abundance of bacterial community members, thereby leading to implications for the functional potential of the hemolymph microbiota. Notably, environmental factors played a substantial role in shaping the microbial community, accounting for 82–96% of the observed variation. Among these factors, wind, oxygen, and temperature exerted the most influence. During intensified upwelling, the abundance of Arcobactereaceae increased from 27% to 36% within gills and from 43% to 55% within hemolymph. Conversely, Helicobactereaceae decreased, particularly within gills, from 15% to 8% during the same period. Significantly, bacteria with fermentation capabilities, such as Colwellia, along with those involved in sulfur cycle processes, such as Arcobactereaceae, Desulfobulbaceae, and Desulfobacteraceae, exhibited an elevated representation during the period of intensified upwelling. This suggests potential nutritional advantages for A. purpuratus. However, the intense upwelling phase also saw an overrepresentation of potentially pathogenic bacteria for mollusks, including Francisella halioticida, Vibrio, and Photobacterium. Moreover, histopathological examination revealed heightened hemocytic infiltration, the presence of granulomatous “swirl” lesions, and a potential Apicomplexan parasite during this intensified upwelling period. These findings underscore the importance of the adaptability of host-microbiota interactions and the potential risks of pathogenicity for cultivated A. purpuratus within the context of ongoing and future environmental changes. Therefore, continuous monitoring of pathogen emergence and immune status evaluation during intensified upwelling periods are crucial for successful A. purpuratus aquaculture.