Shotgun metagenomic analysis of bacterial symbionts associated with "Chromodoris quadricolor" mantle

Abstract

Nudibranchs are colorful marine invertebrates having a diverse group of understudied animals. Recently, some nudibranch members have acquired some attention while others still have not. Chromodoris quadricolor is a member of the Red Sea nudibranch, which did not have the chance to get significant attention. Unlike various invertebrates, it lacks a shell suggesting that it must defend itself in other ways. Therefore, in the present study, we were concerned about the mantle-associated bacterial communities. Being essential partners of this dorid nudibranch system, we investigated their taxonomic and functional profiles. We performed a whole metagenomic shotgun approach for the mantle bacterial cells after a differential pelleting procedure. In this procedure, we separated most of the prokaryotic cells from the eukaryotic host cells. Our findings showed that the mantle-body part holds a diverse group of bacterial species relating mainly to Proteobacteria and Tenericutes phyla. There were novel findings regarding the bacterial members associated with the nudibranch mollusks group. Various species were not previously recorded as bacterial symbionts with nudibranchs. Those members were Bathymodiolus brooksi thiotrophic gill symbiont (23.2%), Mycoplasma marinum (7.4%), Mycoplasma todarodis (5%), and Solemya velum gill symbiont (2.6%). The presence of these bacterial species assumed a nutritional role to the host. However, some of these species were present in a high abundance, suggesting their important symbiosis with Chromodoris quadricolor. In addition, exploring the bacterial ability to produce valuable products resulted in the prediction of 2088 biosynthetic gene clusters (BGCs). We identified different gene cluster classes. Polyketide BGC class was the most represented. Others were related to fatty acid BGCs, RiPP, saccharide, terpene, and NRP BGC classes. Prediction of the activity of these gene clusters resulted in, mainly, an antibacterial activity. In addition, different antimicrobial secondary metabolites were also detected. These secondary metabolites are considered key components regulating the bacterial species interactions in their ecosystem. This suggested the significant contribution of these bacterial symbionts to protect the nudibranch host against predators and pathogens. Globally, it is the first detailed study concerned with both the taxonomic diversity and functional potentials of the bacterial symbionts associated with Chromodoris quadricolor mantle.

Keywords: Bacterial symbionts; Biosynthetic gene clusters; Chromodoris; Metagenome shotgun; Nudibranch.