Microbiome of the Black-Lipped Pearl Oyster Pinctada Margaritifera, a Multi-Tissue Description with Functional Profiling
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fmicb-10-01548 July 4, 2019 Time: 16:10 # 1 ORIGINAL RESEARCH published: 05 July 2019 doi: 10.3389/fmicb.2019.01548 Microbiome of the Black-Lipped Pearl Oyster Pinctada margaritifera, a Multi-Tissue Description With Functional Profiling Caroline Eve Dubé1,2*, Chin-Long Ky2,3,4 and Serge Planes1,2 1 PSL Research University: EPHE-UPVD-CNRS, USR 3278 CRIOBE, Université de Perpignan, Perpignan, France, 2 Laboratoire d’Excellence “CORAIL”, Mo’orea, French Polynesia, 3 Ifremer, UMR 241, Centre du Pacifique, Tahiti, French Polynesia, 4 Ifremer, UMR 5244 Interactions Hôtes Pathogènes Environnements, Université de Montpellier, Montpellier, France 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, Edited by: we expand on this research by assessing the composition and putative functional Sébastien Duperron, Muséum National d’Histoire Naturelle profiles of prokaryotic communities from different organs/compartments of the black- (France), France lipped pearl oyster Pinctada margaritifera, a commercially important shellfish valued Reviewed by: for cultured pearl production in the Pacific region. Seven tissues, in addition to Konstantinos Ar. Kormas, mucous secretions, were targeted from P. margaritifera individuals: the gill, gonad, University of Thessaly, Greece Sven Richard Laming, byssus gland, haemolymph, mantle, adductor muscle, mucus, and gut. Richness University of Aveiro, Portugal of bacterial Operational Taxonomic Units (OTUs) and phylogenetic diversity differed *Correspondence: between host tissues, with mucous layers displaying the highest richness and Caroline Eve Dubé [email protected] diversity. This multi-tissues approach permitted the identification of consistent microbial members, together constituting the core microbiome of P. margaritifera, including Specialty section: Alpha- and Gammaproteobacteria, Flavobacteriia, and Spirochaetes. We also found This article was submitted to Microbial Symbioses, a high representation of Endozoicimonaceae symbionts, indicating that they may a section of the journal be of particular importance to oyster health, survival and homeostasis, as in many Frontiers in Microbiology other coral reef animals. Our study demonstrates that the microbial communities and Received: 20 March 2019 Accepted: 20 June 2019 their associated predicted functional profiles are tissue specific. Inferred physiological Published: 05 July 2019 functions were supported by current physiological data available for the associated Citation: bacterial taxa specific to each tissue. This work provides the first baseline of microbial Dubé CE, Ky C-L and Planes S community composition in P. margaritifera, providing a solid foundation for future (2019) Microbiome of the Black-Lipped Pearl Oyster Pinctada research into this commercially important species and emphasises the important effects margaritifera, a Multi-Tissue of tissue differentiation in structuring the oyster microbiome. Description With Functional Profiling. Front. Microbiol. 10:1548. Keywords: pearl oyster, microbiome, tissue-specific bacterial communities, 16S rRNA gene sequencing, doi: 10.3389/fmicb.2019.01548 functional profiling prediction Frontiers in Microbiology| www.frontiersin.org 1 July 2019| Volume 10| Article 1548 fmicb-10-01548 July 4, 2019 Time: 16:10 # 2 Dubé et al. Black-Lipped Pearl Oyster Microbiome Differentiation INTRODUCTION pathogens (Lokmer and Wegner, 2015; Green et al., 2018; King et al., 2018; Laroche et al., 2018). Bacterial communities can Microbial symbionts play key roles in the survival, homeostasis vary as a function of tissue types in many organisms (e.g., and development of eukaryotic organisms (McFall-Ngai et al., bivalves, sponges, corals, plants, and humans) due, among others, 2013; Bang et al., 2018). Symbiotic associations between bacteria to differences in host cell functions and/or composition of (among other microbes) and macroorganisms are ubiquitous cellular components (Costello et al., 2009; Antunes et al., 2010; in nature and have been the focus of extensive research. Schmitt et al., 2012; Ainsworth et al., 2015; Coleman-Derr et al., For instance, bacterial communities have been found to have 2016). As a consequence, tissue differentiation is thought to profound impact on host nutrition, pathogen resistance and strongly influence the microbiome of oysters. Yet, most microbial development of immune function, as well as other beneficial surveys of oyster species have been performed on whole body processes (Taylor et al., 2007; Kamada et al., 2013; Mueller homogenates (Beleneva et al., 2007) or single tissues (Trabal and Sachs, 2015; Vandenkoornhuyse et al., 2015; Foster et al., 2012; Trabal-Fernández et al., 2014; Banker and Vermeij, et al., 2017), while the eukaryotic host provides a stable 2018). Understanding oyster-microbial associations requires an environment and a constant nutrient supply for their associated understanding of organ compartmentalisation, since different bacteria. Previous studies have demonstrated that host-associated oyster compartments (hereafter named tissues) may harbour microbial community compositions are not stochastic, but unique microbial assemblages that are linked to the physiological mostly determined by host phylogeny and habitat (Cardenas role of each host compartment. To date, variations in the et al., 2014; Pantos et al., 2015; Brooks et al., 2016; Carrier composition of microbial assemblages between oyster tissues and Reitzel, 2018), and can be unevenly distributed within an has rarely been considered (but see King et al., 2012; Lokmer individual host (Hernández-Agreda et al., 2016). Understanding et al., 2016b). To fill this gap, we investigated and compared the mechanics and importance of host-microbiome systems thus the prokaryote communities of different tissues in the black- requires prior knowledge of both the distribution of microbial lipped pearl oyster Pinctada margaritifera. This shellfish species communities at the scale of the individual, and some assessment is highly valued for cultured pearl production and its industry of the influence that microbiome composition may have on represents the second most valuable economic resource in French host functioning. Polynesia after tourism (Ky et al., 2019). This oyster species can Rapid advances in sequencing technology and a decline produce valuable black pearls by biomineralisation, following the in associated costs have spurred an increase in microbiome insertion of a mantle graft from a donor into the gonad of a research, targeting a multitude of organisms and environments recipient oyster, together with a nucleus (Gervis and Sims, 1992; (Caporaso et al., 2010). Of these, the microbiota of marine Taylor and Strack, 2008). While recent studies have investigated invertebrates, including crustaceans, polychaetes, echinoderms, the genome, transcriptome (Le Luyer et al., 2019) and phenome tunicates, sponges and corals, have been investigated extensively (Ky et al., 2018) to identify potential links to cultured pearl quality over the last two decades. These studies have demonstrated traits in P. margaritifera, no data relating to its microbiome exists that many marine invertebrates host diverse, core microbial at present. Characterising the microbial composition of symbiont communities that are phylogenetically distinct from those assemblages in P. margaritifera is critical, since these microbial of surrounding waters (Moitinho-Silva et al., 2014; Lokmer communities likely play a role in maintaining oyster fitness (e.g., et al., 2016b; Zhang et al., 2016; Lu et al., 2017), and that Lokmer et al., 2016b) and by extension, may subsequently impact these microbial associations can be host-specific regardless of upon pearl quality. geography (Reveillaud et al., 2014; van de Water et al., 2016; The aim of this study, therefore, is to provide a microbial Brener-Raffalli et al., 2018). Nonetheless, there are several baseline for P. margaritifera and determine the balance biological factors that can contribute to specific variation in between a stable core microbiome and transient microbial microbial communities, such as host genetics and physiology components between pearl oyster tissue types. To do so, we (Jaenike, 2012; Wegner et al., 2013; Kohl and Carey, 2016; characterised the composition, diversity and predicted functional Amato et al., 2018), host health (Cárdenas et al., 2012; Lu et al., roles of bacterial communities of eight tissues and secretions, 2013; Sweet and Bulling, 2017), diet (Carrier et al., 2018), life including the gill, gonad, byssus gland, haemolymph, mantle, stages (Trabal et al., 2012; Lema et al., 2014), and host–tissue adductor muscle, mucus, and gut. Our study shows that differentiation (Meisterhans et al., 2016; Engelen et al., 2018; bacterial community composition and underlying functional Høj et al., 2018). profiles can be readily distinguished across P. margaritifera Studies on microbiota of bivalves are of particular interest tissues. Although microbial communities of the gill, gut and because of their importance in ecosystem functioning, but also haemolymph have been well studied in oysters (among other due to their economic value and consumption by humans. bivalves), to our knowledge the present study provides the first Oysters are one of