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Intracellular Oceanospirillales Inhabit the Gills of the Hydrothermal Vent Snail Alviniconcha with Chemosynthetic, Proteobacteri

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Intracellular Oceanospirillales Inhabit the Gills of the Hydrothermal Vent Snail Alviniconcha with Chemosynthetic, Proteobacteri bs_bs_banner Environmental Microbiology Reports (2014) doi:10.1111/1758-2229.12183 Intracellular Oceanospirillales inhabit the gills of the hydrothermal vent snail Alviniconcha with chemosynthetic, γ-Proteobacterial symbionts R. A. Beinart,1 S. V. Nyholm,2 N. Dubilier3 and could play a significant ecological role either as a P. R. Girguis1* host parasite or as an additional symbiont with 1Department of Organismic and Evolutionary Biology, unknown physiological capacities. Harvard University, Cambridge, MA 02138, USA. 2Department of Molecular and Cell Biology, University of Introduction Connecticut, Storrs, CT 06269, USA. In recent years, lineages from the γ-Proteobacterial order 3Symbiosis Group, Max Planck Institute for Marine Oceanospirillales have emerged as widespread associ- Microbiology, Bremen 28359, Germany. ates of marine invertebrates. In shallow-water habitats, Oceanospirillales are common and even dominant Summary members of the tissue and mucus-associated microbiota of temperate and tropical corals (Sunagawa et al., 2010; Associations between bacteria from the γ- Bayer et al., 2013a,b; Bourne et al., 2013; Chen et al., Proteobacterial order Oceanospirillales and marine 2013; La Rivière et al., 2013) and sponges (Kennedy invertebrates are quite common. Members of the et al., 2008; Sunagawa et al., 2010; Flemer et al., 2011; Oceanospirillales exhibit a diversity of interac- Bayer et al., 2013a,b; Bourne et al., 2013; Chen et al., tions with their various hosts, ranging from the 2013; La Rivière et al., 2013; Nishijima et al., 2013), and catabolism of complex compounds that benefit host they have been detected in the gills of commercially growth to attacking and bursting host nuclei. Here, important shellfish (Costa et al., 2012), as well as invasive we describe the association between a novel oysters (Zurel et al., 2011). In deep-water habitats, Oceanospirillales phylotype and the hydrothermal Oceanospirillales have been found in association with vent snail Alviniconcha. Alviniconcha typically hydrothermal vent and hydrocarbon seep bivalves harbour chemoautotrophic γ-orε-Proteobacterial (Zielinski et al., 2009; Jensen et al., 2010), polychaete symbionts inside their gill cells. Via fluorescence in worms, and gastropods from whale carcasses (Goffredi situ hybridization and transmission electron micros- et al., 2005; Johnson et al., 2010; Verna et al., 2010). In copy, we observed an Oceanospirillales phylotype almost all cases, the nature of these animal-bacterial rela- (named AOP for ‘Alviniconcha Oceanospirillales tionships remains undetermined. All cultivated members phylotype’) in membrane-bound vacuoles that were of the Oceanospirillales are heterotrophs known for their separate from the known γ-orε-Proteobacterial abilities to degrade complex organic compounds (Garrity symbionts. Using quantitative polymerase chain et al., 2005). Thus, hypotheses about the function of reaction, we surveyed 181 Alviniconcha hosting animal-associated Oceanospirillales have ranged from γ-Proteobacterial symbionts and 102 hosting parasitic consumers of host tissue to beneficial symbionts ε-Proteobacterial symbionts, and found that the popu- that assist in the metabolism or cycling of organic lation size of AOP was always minor relative to compounds. the canonical symbionts (median 0.53% of the total Here, we report a novel Oceanospirillales phylotype quantified 16S rRNA genes). Additionally, we detected discovered in a survey of the bacterial communities asso- AOP more frequently in Alviniconcha hosting ciated with gill tissues of the hydrothermal vent snail γ-Proteobacterial symbionts than in those hosting Alviniconcha. Alviniconcha are dominant members of the ε-Proteobacterial symbionts (96% and 5% of individ- animal communities at hydrothermal vents in the south- uals respectively). The high incidence of AOP in western Pacific and Indian Ocean (Desbruyeres et al., γ-Proteobacteria hosting Alviniconcha implies that it 1994; Van Dover et al., 2001; Ramirez-Llodra et al., 2007; Podowski et al., 2009; 2010). This symbiotic host genus Received 18 July, 2013; accepted 30 May, 2014. *For correspond- ence. E-mail [email protected]; Tel. (+1) 617 496 8328; Fax comprised at least five lineages (likely species) that (+1) 617 495 8848. are supported by the productivity of chemoautotrophic © 2014 Society for Applied Microbiology and John Wiley & Sons Ltd 2 R. A. Beinart, S. V. Nyholm, N. Dubilier and P. R. Girguis bacterial symbionts, which use the reductants in vent To ascertain the relationship of AOP to other Oceano- fluids for the energy to fix inorganic carbon (Suzuki et al., spirillales (and, more broadly, the γ-Proteobacteria, 2005; 2006; Henry et al., 2008; Sanders et al., 2013). including the γ-Proteobacterial symbionts of Alvini- Dense populations of the bacterial symbionts reside concha), Bayesian inference was used to construct a intracellularly in Alviniconcha gill tissue and provide the phylogeny of 16S rRNA genes (see Supporting Informa- bulk of host nutrition (Suzuki et al., 2005). Alviniconcha tion Appendix S1; Fig. 1), including one fully sequenced snails are typically dominated by either a γ-or AOP clone. The AOP sequence falls within a well- ε-Proteobacterial phylotype according to their species, supported clade of Oceanospirillales that all have, with although some individuals from one of these species, the exception of one clone, been found in association with currently called host type III, harbour relatively equal diverse marine invertebrates from various habitats. The populations of two distinct γ-Proteobacterial phylotypes phylotypes that were closest to AOP were recovered (Beinart et al., 2012). Here, via molecular surveys from tropical, shallow-water corals from the Caribbean and microscopic examination, we identified a novel (Sunagawa et al., 2010) and the Great Barrier Reef Alviniconcha-associated Oceanospirillales phylotype and (Bourne and Munn, 2005). The few cultivated representa- localized it inside the gill cells of Alviniconcha. Addition- tives from this clade are members of the genera ally, we quantified its frequency and abundance in popu- Endozoicomonas and Spongiobacter, which were iso- lations of three Alviniconcha host types (I–III), relative to lated from sea slugs (Kurahashi and Yokota, 2007), corals the canonical symbiont phylotypes that associate with (Raina et al., 2009; Yang et al., 2010; Bayer et al., 2013a) these hosts (γ-1, γ-Lau and an ε-Proteobacteria), from and sponges (Flemer et al., 2011; Nishijima et al., 2013). vents at the Eastern Lau Spreading Center (ELSC). Although there is increasing evidence that this clade of Oceanospirillales phylotypes is specific to marine inver- Results and discussion tebrates (Fig. 1), the relationships among their members and their animal hosts, as well as their location in or on Identification and phylogeny of an Oceanospirillales host tissue, have not yet been characterized. An excep- phylotype in Alviniconcha tion is ‘Candidatus Endonucleobacter bathymodiolii’, a Alviniconcha specimens were obtained from four Lau parasite of hydrothermal vent mussels that has been Basin hydrothermal vent fields, which are separated by shown to infect host nuclei, multiply and eventually burst 10 s of kilometres along the approximately 300 km north- from the organelle (Zielinski et al., 2009). The AOP 16S south ELSC. The bacterial communities associated with rRNA gene has 95% sequence identity to a ‘Ca.E. the gills of ELSC Alviniconcha were surveyed by amplify- bathymodiolii’ 16S rRNA gene sequence recovered from a ing and sequencing 20 16S rRNA gene clones from Gulf of Mexico cold seep mussel. libraries generated from the pooled tissue DNA of 30 individuals recovered from two vent fields (see Localization of AOP in Alviniconcha gill tissue Supporting Information Appendix S1). While sequences with affiliation to previously known Alviniconcha ε- and To localize AOP in Alviniconcha gill tissue, we examined γ-Proteobacterial symbiont phylotypes dominated the Alviniconcha individuals via fluorescence in situ hybridi- survey (Beinart et al., 2012), two identical clones repre- zation (FISH) using universal bacterial and AOP-specific sented a novel phylotype from the γ-Proteobacterial probes targeting 16S rRNA (see Supporting Information order Oceanospirillales (hereafter referred to as ‘AOP’ Appendix S1; Fig. 2). Additionally, we used transmission for ‘Alviniconcha Oceanospirillales phylotype’). Follow- electron microscopy (TEM) to describe its morphology in ing discovery of AOP in the clone library, we used association with Alviniconcha gills (see Supporting Infor- BLASTN (Altschul et al., 1990) to search for AOP mation Appendix S1; Figs 3 and 4). Gill tissue from three sequences in 16S rRNA gene pyrosequencing libraries animals from the vent field ABE and three animals (GenBank SRA:SRX450370, SRX450912, SRX450913, from the vent field Tow Cam were selected for these SRX450915) previously obtained from four Alviniconcha microscopic analyses (see Supporting Information individuals (Sanders et al., 2013). This revealed one Appendix S1). matching operational taxonomic unit (OTU) that com- Examination of Alviniconcha gills using FISH confirmed prised 72 sequence reads with ≥ 97% identity to our the presence of AOP in the gills of individuals recovered clones as well as to each other. Since only one other from the ABE vent field, but not in snails recovered from OTU, consisting of two comparatively short sequence the Tow Cam vent field (Fig. 2A and B). In snails with AOP, reads, was classified
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