Heterogeneous microbiomes associate with shell-boring Polydora hoplura (Polychaeta, Spionidae) affecting the commercial flat oyster Ostrea edulis

Abstract

Shell-boring polychaetes belonging to the genus Polydora (Spionidae) infect commercially harvested bivalve molluscs worldwide, reducing their economic value. Due to their limited intraspecific variability, taxonomic identification becomes challenging without molecular approaches. In this study, we identified Polydora hoplura worms infecting flat oysters (Ostrea edulis) in the Gulf of Naples (Italy), providing the first DNA barcode data on the cytochrome c oxidase subunit 1 mitochondrial gene (COI) from its type locality. Three haplotypes with up to ten mutational step differences were detected, suggesting recent introductions from distant populations, including South Africa. The characterization of Polydora associated prokaryotic communities revealed a diverse and fluctuating microbiome linked to these worms, deviating from the usual species-specific pattern observed in other invertebrates. Core and some non-core bacteria could be playing symbiotic roles in nutrient provision, removal of waste products, and antioxidant and detoxifying processes to allow endolithic lifestyle within the borrowed valve chambers. The majority of these microbes though, seem to be acquired horizontally, from an interconnection between the environment and the flat oyster cavity. Indeed, there was a notable detection of opportunistic and potentially pathogenic taxa clusters, including Mycobacterium, Vibrio, Aliiroseovarius and Halarcobacter spp., which in concomitance with the prevalent polydorid infections may prompt implications for the health of the flat oyster host, and for its commercial market, including human consumption. Our study is novel in characterizing bacterial communities associated with shell-boring polychaetes, and sets the bases to propose these parasitic worms as vectors of alterable microbial exchange between oyster hosts and the environment.