Abstract

BackgroundFree-living and symbiotic chemosynthetic microbial communities support primary production and higher trophic levels in deep-sea hydrothermal vents. The shrimp Rimicaris exoculata, which dominates animal communities along the Mid-Atlantic Ridge, houses a complex bacterial community in its enlarged cephalothorax. The dominant bacteria present are from the taxonomic groups Campylobacteria, Desulfobulbia (formerly Deltaproteobacteria), Alphaproteobacteria, Gammaproteobacteria, and some recently discovered iron oxyhydroxide-coated Zetaproteobacteria. This epibiotic consortium uses iron, sulfide, methane, and hydrogen as energy sources. Here, we generated shotgun metagenomes from Rimicaris exoculata cephalothoracic epibiotic communities to reconstruct and investigate symbiotic genomes. We collected specimens from three geochemically contrasted vent fields, TAG, Rainbow, and Snake Pit, to unravel the specificity, variability, and adaptation of Rimicaris–microbe associations.ResultsOur data enabled us to reconstruct 49 metagenome-assembled genomes (MAGs) from the TAG and Rainbow vent fields, including 16 with more than 90% completion and less than 5% contamination based on single copy core genes. These MAGs belonged to the dominant Campylobacteria, Desulfobulbia, Thiotrichaceae, and some novel candidate phyla radiation (CPR) lineages. In addition, most importantly, two MAGs in our collection were affiliated to Zetaproteobacteria and had no close relatives (average nucleotide identity ANI < 77% with the closest relative Ghiorsea bivora isolated from TAG, and 88% with each other), suggesting potential novel species. Genes for Calvin-Benson Bassham (CBB) carbon fixation, iron, and sulfur oxidation, as well as nitrate reduction, occurred in both MAGs. However, genes for hydrogen oxidation and multicopper oxidases occurred in one MAG only, suggesting shared and specific potential functions for these two novel Zetaproteobacteria symbiotic lineages. Overall, we observed highly similar symbionts co-existing in a single shrimp at both the basaltic TAG and ultramafic Rainbow vent sites. Nevertheless, further examination of the seeming functional redundancy among these epibionts revealed important differences.ConclusionThese data highlight microniche partitioning in the Rimicaris holobiont and support recent studies showing that functional diversity enables multiple symbiont strains to coexist in animals colonizing hydrothermal vents.-8nav1G8-_VNYjLQa3sKayVideo

Highlights

  • Free-living and symbiotic chemosynthetic microbial communities support primary production and higher trophic levels in deep-sea hydrothermal vents

  • The reconstruction of 49 Rimicaris-associated metagenome-assembled genomes (MAGs) Shotgun sequencing of total community DNA recovered from the cephalothorax of six R. exoculata individuals (RE3, RE5, RE6, RE7, RE12, RE13) yielded 22–119 million paired-end sequences

  • We were unable to reconstruct bacterial MAGs for Snake Pit using these criteria, due to a much lower sequencing depth for shrimp samples from this site compared with the Rainbow and TAG ones

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Summary

Introduction

Free-living and symbiotic chemosynthetic microbial communities support primary production and higher trophic levels in deep-sea hydrothermal vents. In silico and microscopy analyses suggest that four potential metabolic pathways (iron, sulfide, methane, and hydrogen oxidation) may co-occur within this community [14, 15, 18, 21] This diversity of metabolisms indicates that the epibiotic community associated with R. exoculata is highly plastic, providing a potential adaptive advantage for the shrimp thriving in highly dynamic hydrothermal mixing zones. This diverse bacterial consortium could explain the clear success of the holobiont (i.e., the animal in interaction with its symbiotic partners) in colonizing these geochemically contrasted hydrothermal vents all along the Mid-Atlantic Ridge [4]. The functional capacities and evolutionary relationships of the remaining epibionts, notably the Zetaproteobacteria, under-recovered compared with their free-living counterparts, remain unknown

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