Dataset Information

Complete mitochondrial genome of the hydrothermal vent shrimp Rimicaris variabilis (Decapoda: Caridea: Alvinocarididae) from the North Fiji basin.

ABSTRACT: The family Alvinocarididae is the monophyletic taxon which lives restrictively at chemosynthesis-based environments in the deep-sea. Here, for the first time, we report the complete mitogenome of the alvinocaridid vent shrimp Rimicaris variabilis from the North Fiji Basin. The mitogenome was 15,909 bp in length, with 65.6% AT content. Its protein-coding gene organization was typical of other alvinocaridid shrimps. Based on the phylogenetic tree, R. variabilis was most closely related to Shinkaicaris leurokolos, rather than with other Rimicaris species. To resolve this incongruence between traditional morphological classification and molecular analyses, further mitogenomic analysis of undetermined alvinocaridid taxa is necessary.

SUBMITTER: Lee WK

PROVIDER: S-EPMC7707337 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Complete mitochondrial genome of the hydrothermal vent shrimp Rimicaris variabilis (Decapoda: Caridea: Alvinocarididae) from the North Fiji basin.

Lee Won-Kyung WK Kim Se-Joo SJ Ju Se-Jong SJ Hou Bo Kyeng BK

Mitochondrial DNA. Part B, Resources 20191011 2

The family Alvinocarididae is the monophyletic taxon which lives restrictively at chemosynthesis-based environments in the deep-sea. Here, for the first time, we report the complete mitogenome of the alvinocaridid vent shrimp Rimicaris variabilis from the North Fiji Basin. The mitogenome was 15,909 bp in length, with 65.6% AT content. Its protein-coding gene organization was typical of other alvinocaridid shrimps. Based on the phylogenetic tree, R. variabilis was most closely relat ...[more]

PMID: 33366046

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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.

Dataset Information

Complete mitochondrial genome of the hydrothermal vent shrimp Rimicaris variabilis (Decapoda: Caridea: Alvinocarididae) from the North Fiji basin.

Publications

Complete mitochondrial genome of the hydrothermal vent shrimp <i>Rimicaris variabilis</i> (Decapoda: Caridea: Alvinocarididae) from the North Fiji basin.

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