Host Defense Effectors Expressed by Hemocytes Shape the Bacterial Microbiota From the Scallop Hemolymph

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.

The Gill Microbiota of Argopecten purpuratus Scallop Is Dominated by Symbiotic Campylobacterota and Upwelling Intensification Differentially Affects Their Abundance

“…On the other hand, a decrease in bacteria from the phylum Bacteroidota under laboratory conditions was observed, in particular those of the order Flavobacteriales (genus Winogradskyella) from 4.5% in farm to 0.7% under laboratory conditions (Supplementary files, Figure S3). The genus Winogradskyella is commonly found in numerous marine organisms [44,45], including marine bivalves [9,16]. Interestingly, the genus Winogradskyella is a consistent member across most ostreid herpesvirus-1 microvariant (OsHV-1 µvar) resistant oyster families [9].…”

“…Interestingly, the genus Winogradskyella is a consistent member across most ostreid herpesvirus-1 microvariant (OsHV-1 µvar) resistant oyster families [9]. In A. purpuratus, Winogradskyella is the most abundant genus of the hemolymph [16]. However, it is uncertain what function(s) the Winogradskyella species could play in bivalve mollusks.…”

“…This symbiont may have a closer association with A. purpuratus and a lower adaptive capacity to the assessed climate change scenario. On the other hand, the host s effect on the relative composition of its microbiota has been demonstrated for A. purpuratus [16,58]. Specifically, it has been shown that the expression level of some immune response effectors modulates the abundance of bacterial groups present in the hemolymph of this scallop [16,58].…”

“…On the other hand, the host s effect on the relative composition of its microbiota has been demonstrated for A. purpuratus [16,58]. Specifically, it has been shown that the expression level of some immune response effectors modulates the abundance of bacterial groups present in the hemolymph of this scallop [16,58]. The climate changes constitute a gradually increasing and persistent stress with an overall negative effect on host immunity [59].…”

“…Similarly, a new family of filamentous bacteria of the phylum Campylobacterota was described as a gill epibiont of mussels from the Bathymodiolus genus inhabiting several hydrothermal marine environments, and this association was proposed as a nascent stage of an endosymbiosis [15]. Campylobacterota (previously known as Epsilonproteobacteria) have been also found in the hemolymph of the scallop Argopecten purpuratus [16].…”