scholarly journals High rates of apoptosis visualized in the symbiont-bearing gills of deep-sea Bathymodiolus mussels

2018 ◽  
Author(s):  
Piquet Bérénice ◽  
Shillito Bruce ◽  
H. Lallier François ◽  
Duperron Sébastien ◽  
C. Andersen Ann

AbstractSymbiosis between Bathymodiolus and Gammaproteobacteria enables these deep-sea mussels to live in toxic environments like hydrothermal vents and cold seeps. The quantity of endosymbionts within the gill-bacteriocytes appears to vary according to the hosts environment. We investigated the hypothesis of a control of the endosymbionts density by apoptosis, a programmed cell death. We used fluorometric TUNEL-method and active Caspase-3-targeting antibodies to visualize and quantify apoptotic cells in mussel gills. To avoid artefacts due to depressurization upon specimen recovery from the deep-sea, we compared the apoptotic rates between mussels recovered unpressurised, versus mussels recovered in a pressure-maintaining device, in two species from hydrothermal vents on the Mid-Atlantic Ridge: Bathymodiolus azoricus and B. puteoserpentis. Our results show that pressurized recovery had no significant effect on the apoptotic rate in the gill filaments. Apoptotic levels were highest in the ciliated zone and in the circulating hemocytes, compared to the bacteriocyte zone. Apoptotic gill-cells in B. aff. boomerang from the pockmarks off the Gulf of Guinea, show similar distribution patterns. Deep-sea symbiotic mussels have much higher rates of apoptosis in their gills than the coastal mussel Mytilus edulis without chemolithoautotrophic symbionts. We discuss how apoptosis might be one of the mechanisms that contribute to the adaptation of deep-sea mussels to toxic environments and/or to symbiosis.

PalZ ◽  
2021 ◽  
Author(s):  
Luis Somoza ◽  
José Luis Rueda ◽  
Francisco J. González ◽  
Blanca Rincón-Tomás ◽  
Teresa Medialdea ◽  
...  

AbstractExtensive beds of the deep-sea mussel Bathymodiolus mauritanicus (currently also known as Gigantidas mauritanicus) linked to active cold seeps related to fissure-like activity on Al Gacel mud volcano, Gulf of Cádiz, were filmed and sampled for the first time during the oceanographic expedition SUBVENT-2 aboard R/V Sarmiento de Gamboa. Al Gacel mud volcano is one of up to 80 fluid venting submarine structures (mud volcanoes and mud volcano/diapir complexes) identified in the Gulf of Cádiz as result of explosive venting of hydrocarbon-enriched fluids sourced from deep seated reservoirs. This mud volcano is a cone-shaped edifice, 107 m high, 944 m in diameter constituted by mud breccias and, partially covered by pavements of seep carbonates. Extensive beds of this deep-sea mussel were detected at the northern flank at 810–815 m water depth associated with bacterial mats around intermittent buoyant vertical bubble methane plumes. High methane concentrations were measured in the water column above living mussel beds. Other chemosymbiotic species (Siboglinum sp., Solemya elarraichensis, Isorropodon sp., Thyasira vulcolutre and Lucinoma asapheus) were also found in different parts of Al Gacel mud volcano. Al Gacel mud volcano may currently represent one of the most active mud volcanoes in the Gulf of Cádiz, delivering significant amounts of thermogenic hydrocarbon fluids which contribute to foster the extensive chemosynthesis-based communities detected. This finding is of paramount importance for linking extremophile bivalve populations along the North Atlantic, including cold seeps of the Gulf of México, hydrothermal vents of the Mid-Atlantic Ridge and now, detailed documented at the Gulf of Cádiz.


Author(s):  
Sabine Stöhr ◽  
Michel Segonzac

The animal communities associated with the deep-sea reducing environment have been studied for almost 30 years, but until now only a single species of ophiuroid, Ophioctenella acies, has been found at both hydrothermal vents and methane cold seeps. Since the faunal overlap between vent and seep communities is small and many endemic species have been found among other taxa (e.g. Mollusca, Crustacea), additional species of ophiuroids were expected at previously unstudied sites. Chemical compositions at reducing sites differ greatly from the nearby bathyal environment. Generally, species adapted to chemosynthetic environments are not found in non-chemosynthetic habitats, but occasional visitors of other bathyal species to vent and seep sites have been recorded among many taxa except ophiuroids. This paper presents an analysis of the ophiuroid fauna found at hydrothermal vents and non-reducing nearby sites on the Mid-Atlantic Ridge and on methane cold seeps in the Gulf of Mexico, at Blake Ridge off South Carolina and south of Barbados. In addition to O. acies, four species were found at vents, Ophiactis tyleri sp. nov., Ophiocten centobi, Ophiomitra spinea and Ophiotreta valenciennesi rufescens. While Ophioctenella acies appears to be restricted to chemosynthetic areas, the other four species were also found in other bathyal habitats. They also occur in low numbers (mostly single individuals), whereas species adapted to hydrothermal areas typically occur in large numbers. Ophioscolex tripapillatus sp. nov. and Ophiophyllum atlanticum sp. nov. are described from nearby non-chemosynthetic sites. In a cold seep south of Barbados, three species of ophiuroids were found, including Ophioctenella acies, Amphiura sp., Ophiacantha longispina sp. nov. and Ophioplinthaca chelys. From the cold seeps at Blake Ridge and the Gulf of Mexico, Ophienigma spinilimbatum gen. et sp. nov. is described, likely restricted to the reducing environment. Ophiotreta valenciennesi rufescens occurred abundantly among Lophelia corals in the Gulf of Mexico seeps, which is the first record of this species from the West Atlantic. Habitat descriptions complement the taxonomic considerations, and the distribution of the animals in reducing environments is discussed.


1991 ◽  
Vol 159 (1) ◽  
pp. 473-487 ◽  
Author(s):  
ELIZABETH DAHLHOFF ◽  
GEORGE N. SOMERO

Effects of temperature and hydrostatic pressure were measured on cytosolic malate dehydrogenases (cMDHs) from muscle tissue of a variety of shallow- and deep-living benthic marine invertebrates, including seven species endemic to the deep-sea hydrothermal vents. The apparent Michaelis-Menten constant (Km) of coenzyme (nicotinamide adenine dinucleotide, NADH), used to index temperature and pressure effects, was conserved within a narrow range (approximately 15–25 μmoll−1) at physiological temperatures and pressures for all species. However, at elevated pressures, the Km of NADH rose sharply for cMDHs of shallow species (depths of occurrence >Approximately 500 m), but not for the cMDHs of deep-sea species. Cytosolic MDHs of invertebrates from the deep-sea hydrothermal vents generally were not perturbed by elevated temperatures (15–25°C) at in situ pressures, but cMDHs of cold-adapted deep-sea species were. At a single measurement temperature, the Km of NADH for cMDHs from invertebrates from habitats with well-characterized temperatures was inversely related to maximal sustained body temperature. This correlation was used to predict the maximal sustained body temperatures of vent invertebrates for which maximal habitat and body temperatures are difficult to estimate. Species occurring on the ‘smoker chimneys’, which emit waters with temperatures up to 380°C, are predicted to have sustained body temperatures that are approximately 20–25°C higher than vent species living in cooler vent microhabitats. We conclude that, just as adaptation of enzymes to elevated pressures is important in establishing species’ depth distribution patterns, adaptation of pressure-adapted enzymes to temperature is critical in enabling certain vent species to exploit warm-water microhabitats in the vent environment.


2020 ◽  
pp. 238-292 ◽  
Author(s):  
Richard J. Léveillé ◽  
S. Kim Juniper

2020 ◽  
Vol 50 (6) ◽  
Author(s):  
Elin A. Thomas ◽  
Ruoyu Liu ◽  
Diva Amon ◽  
Jon T. Copley ◽  
Adrian G. Glover ◽  
...  

AbstractChemosynthetic ecosystems have long been acknowledged as key areas of enrichment for deep-sea life, supporting hundreds of endemic species. Echinoderms are among the most common taxa inhabiting the periphery of chemosynthetic environments, and of these, chiridotid holothurians are often the most frequently observed. Yet, published records of chiridotids in these habitats are often noted only as supplemental information to larger ecological studies and several remain taxonomically unverified. This study therefore aimed to collate and review all known records attributed to Chiridota Eschscholtz, 1829, and to conduct the first phylogenetic analysis into the relationship of these chiridotid holothurians across global chemosynthetic habitats. We show that Chiridota heheva Pawson & Vance, 2004 is a globally widespread, cosmopolitan holothurian that occupies all three types of deep-sea chemosynthetic ecosystem—hydrothermal vents, cold seeps and organic falls—as an organic-enrichment opportunist. Furthermore, we hypothesise that C. heheva may be synonymous with another vent-endemic chiridotid, Chiridota hydrothermica Smirnov et al., 2000, owing to the strong morphological, ecological and biogeographical parallels between the two species, and predict that any chiridotid holothurians subsequently discovered at global reducing environments will belong to this novel species complex. This study highlights the importance of understudied, peripheral taxa, such as holothurians, to provide insights to biogeography, connectivity and speciation at insular deep-sea habitats.


Zootaxa ◽  
2018 ◽  
Vol 4441 (1) ◽  
pp. 59 ◽  
Author(s):  
PAULO BONIFÁCIO ◽  
YANN LELIÈVRE ◽  
EMMANUELLE OMNES

Hesionids are a very speciose group of polychaetes. In the deep sea, they occur in different environments such as hydrothermal vents, cold seeps, abyssal depths or whale falls. In the present study, a new species of Hesionidae, Hesiospina legendrei sp. nov. has been identified based on morphological and molecular (16S and COI genes) data from hydrothermal vents located in Juan de Fuca Ridge (NE Pacific Ocean). This new species is characterized by trapezoid prostomium; proboscis with high number of distal papillae (20–27), a pair of sac-like structures inserted ventro-laterally in proboscis; notopodia lobe reduced with multiple, slender aciculae on segments 1–5; and neuropodia developed with single, simple chaeta, and numerous, heterogomph falcigers, with 1–2 inferiormost having elongated hood. Hesiospina legendrei sp. nov. is the third described species in the genus. Sequences from the two previously described Hesiospina species are included in the molecular analyses, and although the genes used in this study are not sufficient to resolve the relationships on genus level, the result raises questions about the cosmopolitan aspect of H. vestimentifera. 


2021 ◽  
Vol 12 ◽  
Author(s):  
Yue Zhang ◽  
Ning Huang ◽  
Minxiao Wang ◽  
Hongbin Liu ◽  
Hongmei Jing

Microbial eukaryotes are key components of the marine food web, but their distribution in deep-sea chemosynthetic ecosystems has not been well studied. Here, high-throughput sequencing of the 18S rRNA gene and network analysis were applied to investigate the diversity, distribution and potential relationships between microbial eukaryotes in samples collected from two cold seeps and one trough in the northern South China Sea. SAR (i.e., Stramenopiles, Alveolata, and Rhizaria) was the predominant group in all the samples, and it was highly affiliated to genotypes with potential symbiotic and parasitic strategies identified from other deep-sea extreme environments (e.g., oxygen deficient zones, bathypelagic waters, and hydrothermal vents). Our findings indicated that specialized lineages of deep-sea microbial eukaryotes exist in chemosynthetic cold seeps, where microbial eukaryotes affiliated with parasitic/symbiotic taxa were prevalent in the community. The biogeographic pattern of the total community was best represented by the intermediate operational taxonomic unit (OTU) category, whose relative abundance ranged 0.01–1% within a sample, and the communities of the two cold seeps were distinct from the trough, which suggests that geographical proximity has no critical impact on the distribution of deep-sea microbial eukaryotes. Overall, this study has laid the foundations for future investigations regarding the ecological function and in situ trophic relationships of microbial eukaryotes in deep-sea ecosystems.


2022 ◽  
Author(s):  
Kai Zhang ◽  
Yao Xiao ◽  
Jin Sun ◽  
Ting Xu ◽  
Kun Zhou ◽  
...  

Abstract Background Symbiosis with chemosynthetic bacteria has allowed many invertebrates to flourish in ‘extreme’ deep-sea chemosynthesis-based ecosystems, such as hydrothermal vents and cold seeps. Bathymodioline mussels are considered as models of deep-sea animal-bacteria symbiosis, but the diversity of molecular mechanisms governing host-symbiont interactions remains understudied owing to the lack of hologenomes. In this study, we adopted a total hologenome approach in sequencing the hydrothermal vent mussel Bathymodiolus marisindicus and the endosymbiont genomes combined with a transcriptomic and proteomic approach that explore the mechanisms of symbiosis. Results Here, we provide the first coupled mussel-endosymbiont genome assembly. Comparative genome analysis revealed that both Bathymodiolus marisindicus and its endosymbiont reshape their genomes through the expansion of gene families, likely due to chemosymbiotic adaptation. Functional differentiation of host immune-related genes and attributes of symbiont self-protection that likely facilitate the establishment of endosymbiosis. Hologenomic analyses offer new evidence that metabolic complementarity between the host and endosymbionts enables the host to compensate for its inability to synthesize some essential nutrients, and two pathways (digestion of symbionts and molecular leakage of symbionts) that can supply the host with symbiontderived nutrients. Results also showed that bacteriocin and abundant toxins of symbiont may contribute to the defense of the B. marisindicus holobiont. Moreover, an exceptionally large number of anti-virus systems were identified in the B. marisindicus symbiont, which likely work synergistically to efficiently protect their hosts from phage infection, indicating virus-bacteria interactions in intracellular environments of a deepsea vent mussel. Conclusions Our study provides novel insights into the mechanisms of symbiosis enabling deep-sea mussels to successfully colonize the special hydrothermal vent habitats.


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