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

Abstract

Background Free-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. Results Our 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. Conclusion These 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.

Reduced chemodiversity suppresses rhizosphere microbiome functioning in the mono-cropped agroecosystems

“…6 C). Although microbes are highly functionally redundant [ 58 , 59 ], the massive loss of microbial species, especially rare microbial species, which play a key role in maintaining the microbial functional pool [ 60 ], may also result in the functional loss [ 61 , 62 ]. Consequently, the significant decrease in the microbial biodiversity may suppress microbiome functional potential during continuous cropping.…”

Comparative Analysis of Intestinal Microflora Between Two Developmental Stages of Rimicaris kairei, a Hydrothermal Shrimp From the Central Indian Ridge

“…Lipids and stable carbon isotope analyses of R. exoculata indicated that these animals possess a high level of polyunsaturated fatty acids, which can be mobilized to enable growth and maturation of the vent shrimp at a suitable site ( Pond et al, 2000 ). Previous studies have shown that R. exoculata harbors two symbioses: epibiotic communities located at branchiostegites, including a wide diversity of Epsilon-, Gamma-, Alpha-, Beta-, Delta-, Zetaproteobacteria, and Bacteroidetes ( Zbinden et al, 2008 ; Petersen et al, 2010 ; Hügler et al, 2011 ; Guri et al, 2012 ; Jan et al, 2014 ; Cambon-Bonavita et al, 2021 ), and bacterial communities colonized in guts, which are composed of Deferribacteres, Mollicutes, Campylobacteria, and, to a lesser extent, Gammaproteobacteria ( Zbinden and Cambon-Bonavita, 2003 ; Durand et al, 2010 , 2015 ). These results are consistent with the intestinal microflora of R. kairei from the CIR in this study, which is also mainly composed of Deferribacteres, Mollicutes, and Campylobacteria.…”

Full-length 16S rRNA amplicon sequencing reveals the variation of epibiotic microbiota associated with two shrimp species of Alvinocarididae: possibly co-determined by environmental heterogeneity and specific recognition of hosts

“…The best research example of alvinocaridid species is Rimicaris exoculata from the Mid Atlantic Ridge. Recent studies have demonstrated that R. exoculata epibiotic communities consist of two major groups, Campylobacteria (previously Epsilonproteobacteria) and Gammaproteobacteria, and lower abundances of Deltaproteobacteria, Alphaproteobacteria, Zetaproteobacteria, Betaproteobacteria, and Bacteroidetes ( Zbinden et al, 2008 ; Petersen et al, 2010 ; Hügler et al, 2011 ; Guri et al, 2012 ; Jan et al, 2014 ; Cambon-Bonavita et al, 2021 ). It has been evidenced that the chemosynthetic ectosymbionts of R. exoculata can directly transfer nutrients to the host ( Ponsard et al, 2013 ).…”