Abstract
The interaction between host immune response and the associated microbiota has recently become a fundamental aspect of vertebrate and invertebrate animal health. This interaction allows the specific association of microbial communities, which participate in a variety of processes in the host including protection against pathogens. Marine aquatic invertebrates such as scallops are also colonized by diverse microbial communities. Scallops remain healthy most of the time, and in general, only a few species are fatally affected on adult stage by viral and bacterial pathogens. Still, high mortalities at larval stages are widely reported and they are associated with pathogenic Vibrio. Thus, to give new insights into the interaction between scallop immune response and its associated microbiota, we assessed the involvement of two host antimicrobial effectors in shaping the abundances of bacterial communities present in the scallop Argopecten purpuratus hemolymph. To do this, we first characterized the microbiota composition in the hemolymph from non-stimulated scallops, finding both common and distinct bacterial communities dominated by the Proteobacteria, Spirochaetes and Bacteroidetes phyla. Next, we identified dynamic shifts of certain bacterial communities in the scallop hemolymph along immune response progression, where host antimicrobial effectors were expressed at basal level and early induced after a bacterial challenge. Finally, the transcript silencing of the antimicrobial peptide big defensin ApBD1 and the bactericidal/permeability-increasing protein ApLBP/BPI1 by RNA interference led to an imbalance of target bacterial groups from scallop hemolymph. Specifically, a significant increase in the class Gammaproteobacteria and the proliferation of Vibrio spp. was observed in scallops silenced for each antimicrobial. Overall, our results strongly suggest that scallop antimicrobial peptides and proteins are implicated in the maintenance of microbial homeostasis and are key molecules in orchestrating host-microbiota interactions. This new evidence depicts the delicate balance that exists between the immune response of A. purpuratus and the hemolymph microbiota.
Highlights
Scallops are a cosmopolitan family of bivalve mollusks
The genomic DNA (gDNA) extracted from bacteria present in the hemolymph of i) heat-inactivated Vibrio-injected scallops, ii) SW-injected scallops, and iii) non-stimulated control scallops was analyzed by 16S rDNA deep amplicon sequencing
We first focused on the analysis of bacterial groups present in non-stimulated scallops to determine how variable was the scallop microbiota between control individuals
Summary
Scallops are a cosmopolitan family of bivalve mollusks. In recent years, interest in scallop immunity has increased due to its economic importance for aquaculture, and because the group occupies a key position within the phylogeny and evolution of the animal kingdom [1]. Bivalves have a semi-open circulatory system where the hemolymph, the analogue of vertebrate blood, and the organs are constantly exposed to high and diverse bacterial loads (~106 cfu/ml) [2]. The immunocompetent cells, circulate within hemolymph and infiltrate tissues, constantly producing a great diversity of antimicrobial effectors [7]. When scallops are exposed to microorganisms, many of these effectors are released by the hemocytes to the hemolymph or into infiltrated tissues, where they classically inactivate or destroy foreign invaders [8, 9]. The recent genome sequencing and de novo assemblies of transcriptomes from several scallop species suggests the existence of many other gene candidates for antimicrobial effectors [17,18,19,20]
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