Dataset Information

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

ABSTRACT: Rimicaris 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.

SUBMITTER: Apremont V

PROVIDER: S-EPMC6214521 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Publications

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

Apremont Vincent V Cambon-Bonavita Marie-Anne MA Cueff-Gauchard Valérie V François David D Pradillon Florence F Corbari Laure L Zbinden Magali M

PloS one 20181102 11

Rimicaris 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 ...[more]

PMID: 30388125

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Project description:The deep-sea hydrothermal vent shrimp Rimicaris exoculata largely depends on a dense epibiotic chemoautotrophic bacterial community within its enlarged cephalothoracic chamber. However, our understanding of shrimp-bacterium interactions is limited. In this report, we focused on the deltaproteobacterial epibiont of R. exoculata from the relatively unexplored South Mid-Atlantic Ridge. A nearly complete genome of a Deltaproteobacteria epibiont was binned from the assembled metagenome. Whole-genome phylogenetic analysis reveals that it is affiliated with the genus Desulfobulbus, representing a potential novel species for which the name "Candidatus Desulfobulbus rimicarensis" is proposed. Genomic and transcriptomic analyses reveal that this bacterium utilizes the Wood-Ljungdahl pathway for carbon assimilation and harvests energy via sulfur disproportionation, which is significantly different from other shrimp epibionts. Additionally, this epibiont has putative nitrogen fixation activity, but it is extremely active in directly taking up ammonia and urea from the host or vent environments. Moreover, the epibiont could be distinguished from its free-living relatives by various features, such as the lack of chemotaxis and motility traits, a dramatic reduction in biosynthesis genes for capsular and extracellular polysaccharides, enrichment of genes required for carbon fixation and sulfur metabolism, and resistance to environmental toxins. Our study highlights the unique role and symbiotic adaptation of Deltaproteobacteria in deep-sea hydrothermal vent shrimps.IMPORTANCE The shrimp Rimicaris exoculata represents the dominant faunal biomass at many deep-sea hydrothermal vent ecosystems along the Mid-Atlantic Ridge. This organism harbors dense bacterial epibiont communities in its enlarged cephalothoracic chamber that play an important nutritional role. Deltaproteobacteria are ubiquitous in epibiotic communities of R. exoculata, and their functional roles as epibionts are based solely on the presence of functional genes. Here, we describe "Candidatus Desulfobulbus rimicarensis," an uncultivated deltaproteobacterial epibiont. Compared to campylobacterial and gammaproteobacterial epibionts of R. exoculata, this bacterium possessed unique metabolic pathways, such as the Wood-Ljungdahl pathway, as well as sulfur disproportionation and nitrogen fixation pathways. Furthermore, this epibiont can be distinguished from closely related free-living Desulfobulbus strains by its reduced genetic content and potential loss of functions, suggesting unique adaptations to the shrimp host. This study is a genomic and transcriptomic analysis of a deltaproteobacterial epibiont and largely expands the understanding of its metabolism and adaptation to the R. exoculata host.

Project description: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.

Project description:Rimicaris exoculata is one of the most well-known and emblematic species of endemic vent fauna. Like many other species from these ecosystems, Rimicaris shrimps host important communities of chemosynthetic bacteria living in symbiosis with their host inside the cephalothorax and gut. For many of these symbiotic partners, the mode of transmission remains to be elucidated and the starting point of the symbiotic relationship is not yet defined, but could begin with the egg. In this study, we explored the proliferation of microbial communities on R. exoculata broods through embryonic development using a combination of NGS sequencing and microscopy approaches. Variations in abundance and diversity of egg microbial communities were analyzed in broods at different developmental stages and collected from mothers at two distinct vent fields on the Mid-Atlantic Ridge (TAG and Snake Pit). We also assessed the specificity of the egg microbiome by comparing communities developing on egg surfaces with those developing on the cuticle of pleopods, which are thought to be exposed to similar environmental conditions because the brood is held under the female's abdomen. In terms of abundance, bacterial colonization clearly increases with both egg developmental stage and the position of the egg within the brood: those closest to the exterior having a higher bacterial coverage. Bacterial biomass increase also accompanies an increase of mineral precipitations and thus clearly relates to the degree of exposure to vent fluids. In terms of diversity, most bacterial lineages were found in all samples and were also those found in the cephalothorax of adults. However, significant variation occurs in the relative abundance of these lineages, most of this variation being explained by body surface (egg vs. pleopod), vent field, and developmental stage. The occurrence of symbiont-related lineages of Epsilonbacteraeota, Gammaproteobacteria, Zetaproteobacteria, and Mollicutes provide a basis for discussion on both the acquisition of symbionts and the potential roles of these bacterial communities during egg development.

Dataset Information

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

Publications

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

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