Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria

• DOI: 10.1186/s40168-021-01045-6
• Publication Date: 2021-04-12T16:03:34Z
• Authors: Marie-Anne Cambon...; Johanne Aubé; Valérie Cueff-Gau...; Julie Reveillaud
• Keywords: 0301 basic medicine; 570; Metagenome-assembled genomes; Rimicaris; Holobiont; Microbial ecology; 03 medical and health sciences; Hydrothermal Vents; Niche partitioning; Decapoda; RNA, Ribosomal, 16S; environment/Symbiosis; Proteobacteria; Animals; 14. Life underwater; Symbiosis; Phylogeny; Zetaproteobacteria; Research; QR100-130; 15. Life on land; [SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology; [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology; Hydrothermal vents; 13. Climate action; [SDV.EE.IEO]Life Sciences [q-bio]/Ecology; [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis

AbstractBackgroundFree-living and symbiotic chemosynthetic microbial communities support primary production and higher trophic levels in deep-sea hydrothermal vents. The shrimpRimicaris 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 groupsCampylobacteria,Desulfobulbia(formerlyDeltaproteobacteria),Alphaproteobacteria,Gammaproteobacteria, and some recently discovered iron oxyhydroxide-coatedZetaproteobacteria. This epibiotic consortium uses iron, sulfide, methane, and hydrogen as energy sources. Here, we generated shotgun metagenomes fromRimicaris exoculatacephalothoracic 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 ofRimicaris–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 dominantCampylobacteria,Desulfobulbia,Thiotrichaceae, and some novel candidate phyla radiation (CPR) lineages. In addition, most importantly, two MAGs in our collection were affiliated toZetaproteobacteriaand had no close relatives (average nucleotide identity ANI < 77% with the closest relativeGhiorsea bivoraisolated 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 novelZetaproteobacteriasymbiotic 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 theRimicarisholobiont and support recent studies showing that functional diversity enables multiple symbiont strains to coexist in animals colonizing hydrothermal vents.