Hydrothermal Vent Shrimp Rimicaris Exoculata Research Articles

Characterization of DNA polymerase δ from deep-sea hydrothermal vent shrimp Rimicaris exoculata

Characterization of DNA polymerase δ from deep-sea hydrothermal vent shrimp Rimicaris exoculata

Identification and characterization of a symbiotic agglutination-related C-type lectin from the hydrothermal vent shrimp Rimicaris exoculata

Rimicaris exoculata (Decapoda: Bresiliidae) is one of the dominant species of hydrothermal vent communities, which inside its gill chamber harbors ectosymbioses with taxonomic invariability while compositional flexibility. Several studies have revealed that the establishment of symbiosis can be initiated and selected by innate immunity-related pattern recognition receptors (PRRs), such as C-type lectins (CTLs). In this research, a CTL was identified in R. exoculata (termed RCTL), which showed high expression at both mRNA and protein levels in the scaphognathite, an organ where the ectosymbionts are attached outside its setae. Linear correlationships were observed between the relative quantities of two major symbionts and the expression of RCTL based on analyzing different shrimp individuals. The recombinant protein of RCTL could recognize and agglutinate the cultivable γ-proteobacterium of Escherichia coli in a Ca2+-dependent manner, obeying a dose-dependent and time-cumulative pattern. Unlike conventional crustacean CTLs, the involvement of RCTL could not affect the bacterial growth, which is a key issue for the successful establishment of symbiosis. These results implied that RCTL might play a critical role in symbiotic recognition and attachment to R. exoculata. It also provides insights to understand how R. exoculata adapted to such a chemosynthesis-based environment.

An H-ferritin from the hydrothermal vent shrimp Rimicaris exoculata and its potential role in iron metabolism.

Rimicaris exoculata (Decapoda: Bresiliidae) is one of the dominant species among hydrothermal vent communities along the Mid-Atlantic Ridge. This shrimp can tolerate high concentrations of heavy metals such as iron, but the mechanisms used for detoxification and utilization of excess metals remain largely unknown. Ferritin is a major iron storage protein in most living organisms. The central heavy subunit of ferritin (H-ferritin) possesses ferroxidase activity and converts iron from Fe2+ to Fe3+, the non-toxic form used for storage. In the present study, the H-ferritin RexFrtH was identified in the hydrothermal vent shrimp R. exoculata, and found to be highly expressed in the gill, the main organ involved in bioaccumulation of metals, at both RNA and protein levels. Accumulation of RexFrtH decreased from efferent to afferent vessels, coinciding with the direction of water flow through the gills. Fe3+ was localized with RexFrtH, and in vitro iron-binding and ferroxidase assays using recombinant RexFrtH confirmed the high affinity for iron. Based on these results, we propose a model of iron metabolism in R. exoculata gills; ferrous iron from ambient hydrothermal water accumulates and is converted and stored in ferric form by RexFrtH as an iron reservoir when needed for metabolism, or excreted as an intermediate to prevent iron overload. The findings expand our understanding of the adaptation strategies used by shrimps inhabiting extreme hydrothermal vents to cope with extremely high heavy metal concentrations.

Highlighting of quorum sensing lux genes and their expression in the hydrothermal vent shrimp Rimicaris exoculata ectosymbiontic community. Possible use as biogeographic markers.

Rimicaris exoculata is a caridean shrimp that dominates the fauna at several hydrothermal vent sites of the Mid-Atlantic Ridge. It has two distinct and stable microbial communities. One of these epibiontic bacterial communities is located in the shrimp gut and has a distribution and role that are poorly understood. The second colonizes its enlarged gill chamber and is involved in host nutrition. It is eliminated after each molt, and has colonization processes reminiscent of those of a biofilm. The presence and expression of genes usually involved in quorum sensing (QS) were then studied. At four sites, Rainbow, TAG, Snake Pit and Logatchev, two lux genes were identified in the R. exoculata epibiontic community at different shrimp molt stages and life stages. RT-PCR experiments highlighted lux gene expression activity at TAG, Snake Pit and Rainbow vent sites. Their potential QS activity and their possible roles in epibiont colonization processes are discussed. Moreover, phylogenetic analysis has shown the presence of three clades for luxS (Epsilonproteobacteria) and four clades for luxR (Gammaproteobacteria) genes, each clade being restricted to a single site. These genes are more divergent than the 16S rRNA one. They could therefore be used as biogeographical genetic markers.

Investigation of bacterial communities within the digestive organs of the hydrothermal vent shrimp Rimicaris exoculata provide insights into holobiont geographic clustering.

Prokaryotic communities forming symbiotic relationships with the vent shrimp, Rimicaris exoculata, are well studied components of hydrothermal ecosystems at the Mid-Atlantic Ridge (MAR). Despite the tight link between host and symbiont, the observed lack of spatial genetic structure seen in R. exoculata contrasts with the geographic differentiation detected in specific bacterial ectosymbionts. The geographic clustering of bacterial lineages within a seemingly panmictic host suggests either the presence of finer scale restriction to gene flow not yet detected in the host, horizontal transmission (environmental selection) of its endosymbionts as a consequence of unique vent geochemistry, or vertically transmitted endosymbionts that exhibit genetic differentiation. To identify which hypothesis best fits, we tested whether bacterial assemblages exhibit differentiation across sites or host populations by performing a 16S rRNA metabarcoding survey on R. exoculata digestive prokaryote samples (n = 31) taken from three geochemically distinct vents across MAR: Rainbow, Trans-Atlantic Geotraverse (TAG) and Logatchev. Analysis of communities across two organs (digestive tract, stomach), three molt colors (white, red, black) and three life stages (eggs, juveniles, adults) also provided insights into symbiont transmission mode. Examining both whole communities and operational taxonomic units (OTUs) confirmed the presence of three main epibionts: Epsilonproteobacteria, Mollicutes and Deferribacteres. With these findings, we identified a clear pattern of geographic segregation by vent in OTUs assigned to Epsilonproteobacteria. Additionally, we detected evidence for differentiation among all communities associated to vents and life stages. Overall, results suggest a combination of environmental selection and vertical inheritance of some of the symbiotic lineages.

Development of an ecotoxicological protocol for the deep-sea fauna using the hydrothermal vent shrimp Rimicaris exoculata

In light of deep-sea mining industry development, particularly interested in massive-sulphide deposits enriched in metals with high commercial value, efforts are increasing to better understand potential environmental impacts to local fauna. The aim of this study was to assess the natural background levels of biomarkers in the hydrothermal vent shrimp Rimicaris exoculata and their responses to copper exposure at in situ pressure (30MPa) as well as the effects of depressurization and pressurization of the high-pressure aquarium IPOCAMP. R. exoculata were collected from the chimney walls of the hydrothermal vent site TAG (Mid Atlantic Ridge) at 3630m depth during the BICOSE cruise in 2014. Tissue metal accumulation was quantified in different tissues (gills, hepatopancreas and muscle) and a battery of biomarkers was measured: metal exposure (metallothioneins), oxidative stress (catalase, superoxide dismutase, glutathione-S-transferase and glutathione peroxidase) and oxidative damage (lipid peroxidation). Data show a higher concentration of Cu in the hepatopancreas and a slight increase in the gills after incubations (for both exposed groups). Significant induction of metallothioneins was observed in the gills of shrimps exposed to 4μM of Cu compared to the control group. Moreover, activities of enzymes were detected for the in situ group, showing a background protection against metal toxicity. Results suggest that the proposed method, including a physiologically critical step of pressurizing and depressurizing the test chamber to enable the seawater exchange during exposure to contaminants, is not affecting metal accumulation and biomarkers response and may prove a useful method to assess toxicity of contaminants in deep-sea species.

Characterization of miRNAs from hydrothermal vent shrimp Rimicaris exoculata

Deep-sea hydrothermal vent shrimp Rimicaris exoculata is a dominant species aggregating in vent fields along the Mid-Atlantic Ocean Ridge. MicroRNAs play important roles in life cycles of eukaryotes. However, little is known about miRNAs of vent animals. In the present study, a small RNA cDNA library from the muscle of R. exoculata was constructed and the miRNA sequencing was performed. The results indicated that a total of 7,983,331 raw reads were obtained, representing 569,354 unique sequences. Based on sequence analysis, R. exoculata contained 159 conserved miRNAs and 34 novel miRNAs. The conserved miRNAs included 54 families belonging to three different taxonomic units (bilaterian, protostomes and arthropods). The results also showed that miR-2001, a lost miRNA in crustaceans, existed in R. exoculata. Among the conserved miRNAs, iso-miRs were detected. Therefore, this study presented the first insight into the miRNAs of deep-sea hydrothermal vent animals.

The complete mitogenome of the Atlantic hydrothermal vent shrimp Rimicaris exoculata Williams & Rona 1986 (Crustacea: Decapoda: Alvinocarididae)

In this study we completely determined and analyzed the mitochondrial genome of the Mid-Atlantic Ridge hydrothermal-vent shrimp Rimicaris exoculata (Crustacea: Decapoda: Alvinocarididae). The circular molecule is 15,902 bp in size with an AT content of 65.7%, composed of the same 37 mitochondrial genes as in all other known metazoan mitogenomes. Sequence composition of the R. exoculata mitogenome is exceptionally similar to that of its Indian-Ocean congener R. kairei, which suggests the fact that they might diverge at a quite recent age. The genome exhibits an ancestral pancrustacean arrangement of mitochondrial genes that presents only the translocation/inversion of trnL-UUR from the ancestral arthropod pattern. Determination of the R. exoculata mitogenome can help to resolve the consensus Decapoda tree of life. It also provides more genetic information available for phylogenetics as well as population genetics on this extensively studied species from hydrothermal vents.

The gill chamber epibiosis of deep‐sea shrimp Rimicaris exoculata: an in‐depth metagenomic investigation and discovery of Zetaproteobacteria

The gill chamber of deep-sea hydrothermal vent shrimp Rimicaris exoculata hosts a dense community of epibiotic bacteria dominated by filamentous Epsilonproteobacteria and Gammaproteobacteria. Using metagenomics on shrimp from the Rainbow hydrothermal vent field, we showed that both epibiont groups have the potential to grow autotrophically and oxidize reduced sulfur compounds or hydrogen with oxygen or nitrate. For carbon fixation, the Epsilonproteobacteria use the reductive tricarboxylic acid cycle, whereas the Gammaproteobacteria use the Calvin-Benson-Bassham cycle. Only the epsilonproteobacterial epibionts had the genes necessary for producing ammonium. This ability likely minimizes direct competition between epibionts and also broadens the spectrum of environmental conditions that the shrimp may successfully inhabit. We identified genes likely to be involved in shrimp-epibiont interactions, as well as genes for nutritional and detoxification processes that might benefit the host. Shrimp epibionts at Rainbow are often coated with iron oxyhydroxides, whose origin is intensely debated. We identified 16S rRNA sequences and functional genes affiliated with iron-oxidizing Zetaproteobacteria, which indicates that biological iron oxidation might play a role in forming these deposits. Fluorescence in situ hybridizations confirmed the presence of active Zetaproteobacteria in the R. exoculata gill chamber, thus providing the first evidence for a Zetaproteobacteria-invertebrate association.

Pathways of Carbon and Energy Metabolism of the Epibiotic Community Associated with the Deep-Sea Hydrothermal Vent Shrimp Rimicaris exoculata

BackgroundThe shrimp Rimicaris exoculata dominates the faunal biomass at many deep-sea hydrothermal vent sites at the Mid-Atlantic Ridge. In its enlarged gill chamber it harbors a specialized epibiotic bacterial community for which a nutritional role has been proposed.Methodology/Principal FindingsWe analyzed specimens from the Snake Pit hydrothermal vent field on the Mid-Atlantic Ridge by complementing a 16S rRNA gene survey with the analysis of genes involved in carbon, sulfur and hydrogen metabolism. In addition to Epsilon- and Gammaproteobacteria, the epibiotic community unexpectedly also consists of Deltaproteobacteria of a single phylotype, closely related to the genus Desulfocapsa. The association of these phylogenetic groups with the shrimp was confirmed by fluorescence in situ hybridization. Based on functional gene analyses, we hypothesize that the Gamma- and Epsilonproteobacteria are capable of autotrophic growth by oxidizing reduced sulfur compounds, and that the Deltaproteobacteria are also involved in sulfur metabolism. In addition, the detection of proteobacterial hydrogenases indicates the potential for hydrogen oxidation in these communities. Interestingly, the frequency of these phylotypes in 16S rRNA gene clone libraries from the mouthparts differ from that of the inner lining of the gill chamber, indicating potential functional compartmentalization.ConclusionsOur data show the specific association of autotrophic bacteria with Rimicaris exoculata from the Snake Pit hydrothermal vent field, and suggest that autotrophic carbon fixation is contributing to the productivity of the epibiotic community with the reductive tricarboxylic acid cycle as one important carbon fixation pathway. This has not been considered in previous studies of carbon fixation and stable carbon isotope composition of the shrimp and its epibionts. Furthermore, the co-occurrence of sulfur-oxidizing and sulfur-reducing epibionts raises the possibility that both may be involved in the syntrophic exchange of sulfur compounds, which could increase the overall efficiency of this epibiotic community.

Comparison of heat-shock responses between the hydrothermal vent shrimp Rimicaris exoculata and the related coastal shrimp Palaemonetes varians

The deep-sea vent shrimp Rimicaris exoculata is believed to occur at the hot end of the hydrothermal biotope in order to provide essential elements to its epibiosis. Because it is found close to hot venting water, R. exoculata lives in a highly fluctuating environment where temperature (2–40 °C in the swarms) can exceed its critical maximal temperature (33–38.5 ± 2 °C). In order to understand how this vent shrimp copes with hyperthermia, we compared its molecular heat stress response following an acute but non-lethal heat-shock (1 h at 30 °C) with that of its monophyletic shallow-water relative, the shrimp Palaemonetes varians, known to frequently undergo prolonged exposure at temperatures up to 30 °C in its natural environment during summer. We isolated four isoforms of heat-shock proteins 70 (HSP70) in R. exoculata (2 constitutive and 2 inducible isoforms) and two isoforms in P. varians (1 constitutive and 1 inducible isoform) and quantitatively compared their magnitude of induction at mRNA level, using real-time PCR, in the case of experimentally heat-stressed shrimps, with respect to control (unstressed) animals. Here, we report the first quantification of the expression of multiple hsp70 genes following heat stress in a deep-sea vent species living at 2300 m depth. Our results show a strong increase of hsp70 inducible genes in the vent shrimp (∼ 400-fold) compared to the coastal shrimp (∼ 15-fold). We therefore propose that, the highly inducible molecular response observed in R. exoculata may contribute to the ability of this species to tolerate thermal extremes.

Bacterial symbionts and mineral deposits in the branchial chamber of the hydrothermal vent shrimp Rimicaris exoculata: relationship to moult cycle

AB Aquatic Biology Contact the journal Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections AB 1:225-238 (2008) - DOI: https://doi.org/10.3354/ab00024 Bacterial symbionts and mineral deposits in the branchial chamber of the hydrothermal vent shrimp Rimicaris exoculata: relationship to moult cycle Laure Corbari1,*, Magali Zbinden2, Marie-Anne Cambon-Bonavita3, Françoise Gaill2, Philippe Compère1 1Université de Liège, Laboratoire de Morphologie Fonctionnelle et Évolutive, Unité de Morphologie Ultrastructurale, Allée de la Chimie, 3, 4000 Liège, Belgium 2UMR CNRS 7138 ‘Systématique, Adaptation et Evolution’, Université Pierre et Marie Curie, 7 Quai St Bernard, Bâtiment A, 75252 Paris Cedex 05, France 3Laboratoire de Microbiologie et Biotechnologie des Extrêmophiles, IFREMER, Centre de Brest, BP 70, 29280 Plouzané, France *Email: lcorbari@ulg.ac.be ABSTRACT: The shrimp Rimicaris exoculata is considered a primary consumer that dominates the fauna of most Mid-Atlantic Ridge hydrothermal ecosystems. The shrimps harbour in their gill chamber an important ectosymbiotic community of chemoautotrophic bacteria associated with iron oxide deposits. The settlement and development of this ectosymbiosis was investigated using microscopy techniques (light microscopy, LM; and scanning, transmission and environmental scanning electron microscopy: SEM and ESEM, respectively) for shrimps from 2 different vent fields (Rainbow, 36°14.0’N and TAG, 26°08.0’N). The results revealed a bacterial re-colonisation after each exuviation and a development of the bacterial community in 5 steps in relation to the moult stages, which were used as a reference time scale. In 287 shrimps from both vent fields, pre-ecdysial stages prevailed in the population, suggesting a short anecdysis and high moulting rate, probably to renew the ectosymbiosis. Comparisons with moult cycles of littoral shrimps suggest that the interval between successive exuviations in R. exoculata may be as short as 10 d. The colours of R. exoculata result from accumulation of iron oxide, which forms a bacteria-associated mineral crust in the gill chambers. The close correspondence between moult stages, the development of the ectosymbiont community and shrimp colours indicate that colour could be used to rapidly determine shrimp moult stages. KEY WORDS: Hydrothermal vents · Shrimp · Moult cycle · Ectosymbiosis · Iron oxides Full text in pdf format PreviousNextCite this article as: Corbari L, Zbinden M, Cambon-Bonavita M, Gaill F, Compère P (2008) Bacterial symbionts and mineral deposits in the branchial chamber of the hydrothermal vent shrimp Rimicaris exoculata: relationship to moult cycle. Aquat Biol 1:225-238. https://doi.org/10.3354/ab00024 Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in AB Vol. 1, No. 3. Online publication date: January 15, 2008 Print ISSN: 1864-7782; Online ISSN: 1864-7790 Copyright © 2008 Inter-Research.

Tomography of bacteria–mineral associations within the deep-sea hydrothermal vent shrimp Rimicaris exoculata

Rimicaris exoculata flourishes around deep-sea hydrothermal vent environments along the Mid-Atlantic Ridge (MAR). Epibiotic bacteria and minerals found within the branchial chamber of the shrimp are of interest in the search for the metabolic energy pathways sustaining shrimp swarms at the Rainbow vent site (MAR). Here we examine the three-dimensional (3D) relationships between epibionts and their associated minerals. The morphology and chemical composition of the minerals were analysed by Energy Filtering Transmission Electron Microscopy (EFTEM) and the 3D organisation was determined by Transmission Electron Tomography (TET). The minerals are preferentially associated with small, rod-shaped bacteria. The iron oxide deposits exhibit three main associations with the bacterial exterior: (1) close, (2) zoned/layered and (3) distant. Iron is the most prevalent element, with a close association with the bacteria, and co-occurs with oxygen. 3D reconstructions reveal a discontinuous network of deposits around the bacteria, showing the intricate nature of these iron oxides. Rimicaris exoculata prospère autour des sources hydrothermales profonds de la ride Médio-Atlantique (MAR). Les bactéries épibiontes et les minéraux se trouvant dans la chambre branchiale de ces crevettes présentent un intérêt dans la recherche des voies métaboliques de transfert d'énergie vers les agrégations des crevettes à Rainbow (MAR). Nous avons examiné les relations tridimensionnelles entre les épibiontes et leurs minéraux associés. La morphologie et la composition chimique des minéraux ont été analysées par microscopie électronique à transmission en perte d'énergie (EFTEM), et l'organisation 3D a été déterminée par tomographie électronique à transmission (TET). Les minéraux sont préférentiellement associés à de petites bactéries en bâtonnet. Les dépôts d'oxyde de fer présentent trois types d'association avec la partie externe des bactéries : (1) proche, (2) en zones/en couches et (3) distante. Le fer est l'élément prédominant. Il présente une association proche avec les bactéries et est co-localisé avec l'oxygène. Les reconstructions en 3D révèlent un réseau discontinu de dépôts autour des bactéries, qui montre la complexité de ces oxydes de fer.

Does sulphide detoxication occur in the gills of the hydrothermal vent shrimp, Rimicaris exoculata?

Ultrastructural observations of the gills of the hydrothermal vent shrimp Rimicaris exoculata reveal that the epithelial cells contain numerous mitochondria clustered around unusual organelles (diameter of 0.7 to 2.5 μm) containing membrane stacks. These organelles were termed sulphide-oxidising bodies (SOBs) by structural analogy with organelles observed in the tissues of species adapted to sulphide-rich environments. Moreover, in the gills of R. exoculata, mitochondria display numerous electron-dense granules in their stroma. Such ultrastructural features suggest that sulphide detoxication may probably occur in the gills of R. exoculata. Comparable structures were also described in the gills of other hydrothermal vent species, as the alvinellid Pompeii worms that, as R. exoculata, are housing ectosymbiotic bacteria.