Carole Decker

Phylogeny and Diversification Patterns among Vesicomyid Bivalves

Vesicomyid bivalves are among the most abundant and diverse symbiotic taxa in chemosynthetic-based ecosystems: more than 100 different vesicomyid species have been described so far. In the present study, we investigated the phylogenetic positioning of recently described vesicomyid species from the Gulf of Guinea and their western Atlantic and Pacific counterparts using mitochondrial DNA sequence data. The maximum-likelihood (ML) tree provided limited support for the recent taxonomic revision of vesicomyids based on morphological criteria; nevertheless, most of the newly sequenced specimens did not cluster with their morphological conspecifics. Moreover, the observed lack of geographic clustering suggests the occurrence of independent radiations followed by worldwide dispersal. Ancestral character state reconstruction showed a significant correlation between the characters “depth” and “habitat” and the reconstructed ML phylogeny suggesting possible recurrent events of ‘stepwise speciation’ from shallow to deep waters in different ocean basins. This is consistent with genus or species bathymetric segregation observed from recent taxonomic studies. Altogether, our results highlight the need for ongoing re-evaluation of the morphological characters used to identify vesicomyid bivalves.

High connectivity across the fragmented chemosynthetic ecosystems of the deep Atlantic Equatorial Belt: efficient dispersal mechanisms or questionable endemism?

Chemosynthetic ecosystems are distributed worldwide in fragmented habitats harbouring seemingly highly specialized communities. Yet, shared taxa have been reported from highly distant chemosynthetic communities. These habitats are distributed in distinct biogeographical regions, one of these being the so‐called Atlantic Equatorial Belt (AEB). Here, we combined genetic data (COI) from several taxa to assess the possible existence of cryptic or synonymous species and to detect the possible occurrence of contemporary gene flow among populations of chemosynthetic species located on both sides of the Atlantic. Several Evolutionary Significant Units (ESUs) of Alvinocarididae shrimp and Vesicomyidae bivalves were found to be shared across seeps of the AEB. Some were also common to hydrothermal vent communities of the Mid‐Atlantic Ridge (MAR), encompassing taxa morphologically described as distinct species or even genera. The hypothesis of current or very recent large‐scale gene flow among seeps and vents was supported by microsatellite analysis of the shrimp species Alvinocaris muricola/Alvinocaris markensis across the AEB and MAR. Two nonmutually exclusive hypotheses may explain these findings. The dispersion of larvae or adults following strong deep‐sea currents, possibly combined with biochemical cues influencing the duration of larval development and timing of metamorphosis, may result in large‐scale effective migration among distant spots scattered on the oceanic seafloor. Alternatively, these results may arise from the prevailing lack of knowledge on the ocean seabed, apart from emblematic ecosystems (chemosynthetic ecosystems, coral reefs or seamounts), where the widespread classification of endemism associated with many chemosynthetic taxa might hide wider distributions in overlooked parts of the deep sea.

Physical Proximity May Promote Lateral Acquisition of Bacterial Symbionts in Vesicomyid Clams

Vesicomyid clams harbor intracellular sulfur-oxidizing bacteria that are predominantly maternally inherited and co-speciate with their hosts. Genome recombination and the occurrence of non-parental strains were recently demonstrated in symbionts. However, mechanisms favoring such events remain to be identified. In this study, we investigated symbionts in two phylogenetically distant vesicomyid species, Christineconcha regab and Laubiericoncha chuni, which sometimes co-occur at a cold-seep site in the Gulf of Guinea. We showed that each of the two species harbored a single dominant bacterial symbiont strain. However, for both vesicomyid species, the symbiont from the other species was occasionally detected in the gills using fluorescence in situ hybridization and gene sequences analyses based on six symbiont marker genes. Symbiont strains co-occurred within a single host only at sites where both host species were found; whereas one single symbiont strain was detected in C. regab specimens from a site where no L. chuni individuals had been observed. These results suggest that physical proximity favored the acquisition of non-parental symbiont strains in Vesicomyidae. Over evolutionary time, this could potentially lead to genetic exchanges among symbiont species and eventually symbiont displacement. Symbiont densities estimated using 3D fluorescence in situ hybridization varied among host species and sites, suggesting flexibility in the association despite the fact that a similar type of metabolism is expected in all symbionts.

Diversity of symbioses between chemosynthetic bacteria and metazoans at the Guiness cold seep site (Gulf of Guinea, West Africa)

Fauna from deep‐sea cold seeps worldwide is dominated by chemosymbiotic metazoans. Recently, investigation of new sites in the Gulf of Guinea yielded numerous new species for which symbiosis was strongly suspected. In this study, symbioses are characterized in five seep‐specialist metazoans recently collected from the Guiness site located at ∼600 m depth. Four bivalve and one annelid species belonging to families previously documented to harbor chemosynthetic bacteria were investigated using bacterial marker gene sequencing, fluorescence in situ hybridization, and stable isotope analyses. Results support that all five species display chemosynthetic, sulfur‐oxidizing γ‐proteobacteria. Bacteria are abundant in the gills of bivalves, and in the trophosome of the siboglinid annelid. As observed for their relatives occurring at deeper sites, chemoautotrophy is a major source of carbon for animal nutrition. Although symbionts found in each host species are related to symbionts found in other metazoans from the same families, several incongruencies are observed among phylogenetic trees obtained from the different bacterial genes, suggesting a certain level of heterogeneity in symbiont strains present. Results provide new insights into the diversity, biogeography, and role of symbiotic bacteria in metazoans from the Gulf of Guinea, at a site located at an intermediate depth between the continental shelf and the deep sea.

First respiration estimates of cold-seep vesicomyid bivalves from in situ total oxygen uptake measurements.

Vesicomyid bivalves are one of the most abundant symbiont-bearing species inhabiting deep-sea reducing ecosystems. Nevertheless, except for the hydrothermal vent clam Calyptogena magnifica, their metabolic rates have not been documented, and only assessed with ex situ experiments. In this study, gathering benthic chamber measurements and biomass estimation, we give the first in situ assessment of the respiration rate of these bivalves. The giant pockmark Regab, located at 3160m depth along the Congo-Angola margin, is a cold-seep site characterised by dense assemblages of two species of vesicomyids: Christineconcha regab and Laubiericoncha chuni with high dominance of C. regab. Two sites with dense aggregates of vesicomyids were selected to measure total oxygen uptake (TOU), and methane fluxes using IFREMERs benthic chamber CALMAR deployed by the ROV Quest 4000 (MARUM). Photographs were taken and bivalves were sampled using blade corers to estimate density and biomass. Total oxygen uptake was higher at Site 2 compared to Site 1 (respectively 492 mmol.m(-2).d(-1) and 332 mmol.m(-2).d(-1)). However, given vesicomyid densities and biomass, mean oxygen consumption rates were similar at both sites (1.9 to 2.5 μmol.g total dry mass(-1).h(-1) at the Site 1 and 1.8 to 2.3 μmol.g total dry mass(-1).h(-1) at Site 2). These respiration rates are higher than published ex situ estimates for cold-seep or hydrothermal vent bivalves. Although methane fluxes at the base of sulphide production were clearly higher at Site 2 (14.6 mmol.m(-2).d(-1)) than at Site 1 (0.3 mmol.m(-2).d(-1)), they do not seem to influence the respiration rates of these bivalves associated to sulphide-oxidizing symbionts.

Globin’s Structure and Function in Vesicomyid Bivalves from the Gulf of Guinea Cold Seeps as an Adaptation to Life in Reduced Sediments

Vesicomyid bivalves form dense clam beds in both deep-sea cold seeps and hydrothermal vents. The species diversity within this family raises questions about niche separation and specific adaptations. To compare their abilities to withstand hypoxia, we have studied the structure and function of erythrocyte hemoglobin (Hb) and foot myoglobin (Mb) from two vesicomyid species, Christineconcha regab and Laubiericoncha chuni, collected from the Regab pockmark in the Gulf of Guinea at a depth of 3,000 m. Laubiericoncha chuni possesses three monomeric globins, G1 (15,361 Da), G2 (15,668 Da), and G3 (15,682 Da) in circulating erythrocytes (Hb), and also three globins, G1, G3, and G4 (14,786 Da) in foot muscle (Mb). Therefore, globins G2 and G4 appear to be specific for erythrocytes and muscle, respectively, but globins G1 and G3 are common. In contrast, C. regab lacks erythrocyte Hb completely and possesses only globin monomers G1′ (14,941 Da), G2′ (15,169 Da), and G3′ (15,683 Da) in foot muscle. Thus, these two vesicomyid species, C. regab and L. chuni, show a remarkable diversity in globin expression when examined by electrospray ionization mass spectrometry. Oxygen-binding affinities reveal extremely high oxygen affinities (P50 < 1 Torr, from 5° to 15°C at pH 7.5), in particular L. chuni globins, which might be an advantage allowing L. chuni to dig deeply for sulfides and remain buried for long periods in reduced sediments.