A Nematode of the Mid-Atlantic Ridge Hydrothermal Vents Harbors a Possible Symbiotic Relationship

Deep-sea hydrothermal vent meiofauna have been the focus of recent research and the discovery of an abundant well-adapted free-living marine nematode on the Mid-Atlantic Ridge offers new perspectives on adaptations to the vent environment. Indeed, knowledge concerning biological interactions of microbes and meiofauna in marine extreme environments is scarce, especially for nematodes. In this study, we used microscopic observations [fluorescence in situ hybridization (FISH) and scanning electron microscopy (SEM)] and metabarcoding of 16S rRNA to characterize the bacterial community of the nematode species Oncholaimus dyvae, an overlooked but ecologically important vent organism. Detection of bacteria in the buccal cavity and on the cuticle (SEM) and epibionts in its intestine (FISH) suggests that O. dyvae harbors its own bacterial community. Molecular results and phylogenetic analysis show that bacteria associated with this species are related to symbiotic lineages typical of hydrothermal vent fauna, such as sulfur-oxidizing bacteria related to Epsilonproteobacteria and Gammaproteobacteria. This multi-approach study suggests a potential symbiotic role of bacteria with its nematode host and opens new research perspectives on vent meiofauna

Microbial diversity associated with the hydrothermal shrimp Rimicaris exoculata gut and occurrence of a resident microbial community

En libre-accès sur Archimer : http://archimer.ifremer.fr/doc/00000/11142/7919.pdfInternational audienceRimicaris exoculata dominates the megafauna of several Mid-Atlantic Ridge hydrothermal sites. Its gut is full of sulphides and iron-oxide particles and harbours microbial communities. Although a trophic symbiosis has been suggested, their role remains unclear. In vivo starvation experiments in pressurized vessels were performed on shrimps from Rainbow and Trans-Atlantic Geotraverse sites in order to expel the transient gut contents. Microbial communities associated with the gut of starved and reference shrimps were compared using 16S rRNA gene libraries and microscopic observations (light, transmission and scanning electron microscopy and FISH analyses). We show that the gut microbiota of shrimps from both sites included mainly Deferribacteres, Mollicutes, Epsilon- and Gammaproteobacteria. For the first time, we have observed filamentous bacteria, inserted between microvilli of gut epithelial cells. They remained after starvation periods in empty guts, suggesting the occurrence of a resident microbial community. The bacterial community composition was the same regardless of the site, except for Gammaproteobacteria retrieved only in Rainbow specimens. We observed a shift in the composition of the microbiota of long-starved specimens, from the dominance of Deferribacteres to the dominance of Gammaproteobacteria. These results reinforce the hypothesis of a symbiotic relationship between R. exoculata and its gut epibionts

Diversity of western pacific back-arc basins invertebrates reevaluated through a barcode approach – Results on decapods and polychaetes

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Reconstructing the hydrothermal shrimp <em>Rimicaris exoculata</em> symbiotic genomes using advanced analysis and visualization metagenomic methods

International audienceLife around deep hydrothermal vents is based on chemosynthetic primary production, and symbiotic associations with chemosynthetic bacteria are widespread in the deep-sea . The shrimp Rimicaris exoculata dominates the fauna of hydrothermal sites along the Mid Atlantic ridge. The species harbors a complex bacterial community including Epsilon-, Gamma- and some recently discovered Zetaproteobacteria within its gill chamber, as well as long microbial filaments within the digestive tract. While in vivo experiments provide evidence for direct nutritional transfers from bacteria to the host across the gill chamber and therefore show a true mutualistic association, in silico analyses suggest four metabolic pathways (iron, sulfide, methane and hydrogen oxidation) may co-occur within this community. Here, we build on these previous studies and use shotgun metagenomics to reconstruct novel Rimicaris exoculata symbiotic genomes, and unravel their metabolic potential. By comparing four metagenomes originating from the contrasted ultramafic Rainbow and the mafic TAG sites along the Mid Atlantic Ridge, we could detect and recover seven abundant and site-specific draft genomes. Bacterial single-copy genes predict a relatively complex environment, with the presence of 48 bacterial genomes above our detection limit in the raw metagenomic assembly. The characterization of these vital, energy-harvesting symbionts, will likely provide new and important insights into the fundamental ecological and evolutionary mechanisms underlying the intimate host-microbe associations and geobiological interactions in extreme environments

A Nematode of the Mid-Atlantic Ridge Hydrothermal Vents Harbors a Possible Symbiotic Relationship

International audienceDeep-sea hydrothermal vent meiofauna have been the focus of recent research and the discovery of an abundant well-adapted free-living marine nematode on the Mid-Atlantic Ridge offers new perspectives on adaptations to the vent environment. Indeed, knowledge concerning biological interactions of microbes and meiofauna in marine extreme environments is scarce, especially for nematodes. In this study, we used microscopic observations [fluorescence in situ hybridization (FISH) and scanning electron microscopy (SEM)] and metabarcoding of 16S rRNA to characterize the bacterial community of the nematode species Oncholaimus dyvae, an overlooked but ecologically important vent organism. Detection of bacteria in the buccal cavity and on the cuticle (SEM) and epibionts in its intestine (FISH) suggests that O. dyvae harbors its own bacterial community. Molecular results and phylogenetic analysis show that bacteria associated with this species are related to symbiotic lineages typical of hydrothermal vent fauna, such as sulfur-oxidizing bacteria related to Epsilonproteobacteria and Gammaproteobacteria. This multi-approach study suggests a potential symbiotic role of bacteria with its nematode host and opens new research perspectives on vent meiofauna

Gill chamber and gut microbial communities of the hydrothermal shrimp Rimicaris chacei Williams and Rona 1986: A possible symbiosis

International audienceRimicaris chacei Williams and Rona 1986, formerly named as Chorocaris chacei, is a caridean shrimp living in deep-sea hydrothermal ecosystems. This shrimp is endemic to the Mid Atlantic Ridge (MAR) and lives at the periphery of aggregates of its well-known congeneric R. exoculata Williams and Rona 1986. Contrasting with the very dense and mobile clusters formed by R. exoculata, R. chacei lives in small groups of several individuals that are not very mobile. Although devoid of the characteristic hypertrophied cephalothorax of R. exoculata, which harbors the ectosymbionts, a microbial community has also been reported in the cephalothorax of R. chacei. Previous data on morphology, behavior and isotopic values indicate a diet based on a combination of feeding on its epibiotic bacteria and scavenging or occasional predation. In this study, our objective was to describe, for the first time, the distribution, morphology and phylogeny of the microbial communities associated with R. chacei. This species is significantly less studied than R. exoculata, but nevertheless represents the only other known example of symbiosis in crustaceans of MAR hydrothermal vent sites. Microbial communities have been observed at the same locations as in R. exoculata (mouthparts, branchiostegites and digestive tract). However, in R. chacei, the surfaces occupied by the bacteria are smaller. The main lineages are affiliated to Epsilon and Gammaproteobacteria in the cephalothorax and to Deferribacteres, Mollicutes, Epsilon and Gammaproteobacteria in the digestive tract. Comparison with the well-described bacterial communities of R. exoculata and hypotheses about the role of these communities in R. chacei are discussed

A novel and dual digestive symbiosis scales up the nutrition and immune system of the holobiont Rimicaris exoculata

Abstract Background In deep-sea hydrothermal vent areas, deprived of light, most animals rely on chemosynthetic symbionts for their nutrition. These symbionts may be located on their cuticle, inside modified organs, or in specialized cells. Nonetheless, many of these animals have an open and functional digestive tract. The vent shrimp Rimicaris exoculata is fueled mainly by its gill chamber symbionts, but also has a complete digestive system with symbionts. These are found in the shrimp foregut and midgut, but their roles remain unknown. We used genome-resolved metagenomics on separate foregut and midgut samples, taken from specimens living at three contrasted sites along the Mid-Atlantic Ridge (TAG, Rainbow, and Snake Pit) to reveal their genetic potential. Results We reconstructed and studied 20 Metagenome-Assembled Genomes (MAGs), including novel lineages of Hepatoplasmataceae and Deferribacteres , abundant in the shrimp foregut and midgut, respectively. Although the former showed streamlined reduced genomes capable of using mostly broken-down complex molecules, Deferribacteres showed the ability to degrade complex polymers, synthesize vitamins, and encode numerous flagellar and chemotaxis genes for host-symbiont sensing. Both symbionts harbor a diverse set of immune system genes favoring holobiont defense. In addition, Deferribacteres were observed to particularly colonize the bacteria-free ectoperitrophic space, in direct contact with the host, elongating but not dividing despite possessing the complete genetic machinery necessary for this. Conclusion Overall, these data suggest that these digestive symbionts have key communication and defense roles, which contribute to the overall fitness of the Rimicaris holobiont

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

Additional file 7 of A novel and dual digestive symbiosis scales up the nutrition and immune system of the holobiont Rimicaris exoculata

Additional file 7: Supplementary Table 4. List and copy numbers of the genes featured in Figure 4