Abstract

Elucidating the role of prokaryotic symbionts in mediating host physiology has emerged as an important area of research. Since oysters are the world’s most heavily cultivated bivalve molluscs, numerous studies have applied molecular techniques to understand the taxonomic and functional diversity of their associated bacteria. Here, we expand on this research by assessing the composition and putative functional profiles of prokaryotic communities from different organs/compartments of the black-lipped pearl oyster Pinctada margaritifera, a commercially important shellfish valued for cultured pearl production in the Pacific region. Seven tissues, in addition to mucous secretions, were targeted from P. margaritifera individuals: the gill, gonad, byssus gland, haemolymph, mantle, adductor muscle, mucus, and gut. Richness of bacterial Operational Taxonomic Units (OTUs) and phylogenetic diversity differed between host tissues, with mucous layers displaying the highest richness and diversity. This multi-tissues approach permitted the identification of consistent microbial members, together constituting the core microbiome of P. margaritifera, including Alpha- and Gammaproteobacteria, Flavobacteriia, and Spirochaetes. We also found a high representation of Endozoicimonaceae symbionts, indicating that they may be of particular importance to oyster health, survival and homeostasis, as in many other coral reef animals. Our study demonstrates that the microbial communities and their associated predicted functional profiles are tissue specific. Inferred physiological functions were supported by current physiological data available for the associated bacterial taxa specific to each tissue. This work provides the first baseline of microbial community composition in P. margaritifera, providing a solid foundation for future research into this commercially important species and emphasises the important effects of tissue differentiation in structuring the oyster microbiome.

Highlights

  • Microbial symbionts play key roles in the survival, homeostasis and development of eukaryotic organisms (McFall-Ngai et al, 2013; Bang et al, 2018)

  • Our study shows that bacterial community composition and underlying functional profiles can be readily distinguished across P. margaritifera tissues

  • Bacterial DNA was isolated from eight tissues and secretions collected from twelve individuals of P. margaritifera, totalling 95 samples. 16S rRNA gene sequencing yielded to 4,331,391 sequences that were further clustered into 4,085 distinct Operational Taxonomic Units (OTUs) (Supplementary Data S1)

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Summary

Introduction

Microbial symbionts play key roles in the survival, homeostasis and development of eukaryotic organisms (McFall-Ngai et al, 2013; Bang et al, 2018). The microbiota of marine invertebrates, including crustaceans, polychaetes, echinoderms, tunicates, sponges and corals, have been investigated extensively over the last two decades. These studies have demonstrated that many marine invertebrates host diverse, core microbial communities that are phylogenetically distinct from those of surrounding waters (Moitinho-Silva et al, 2014; Lokmer et al, 2016b; Zhang et al, 2016; Lu et al, 2017), and that these microbial associations can be host-specific regardless of geography (Reveillaud et al, 2014; van de Water et al, 2016; Brener-Raffalli et al, 2018). There are several biological factors that can contribute to specific variation in microbial communities, such as host genetics and physiology (Jaenike, 2012; Wegner et al, 2013; Kohl and Carey, 2016; Amato et al, 2018), host health (Cárdenas et al, 2012; Lu et al, 2013; Sweet and Bulling, 2017), diet (Carrier et al, 2018), life stages (Trabal et al, 2012; Lema et al, 2014), and host–tissue differentiation (Meisterhans et al, 2016; Engelen et al, 2018; Høj et al, 2018)

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