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

Type Article
Date 2021-04
Language English
Author(s) Cambon-Bonavita Marie-AnneORCID1, Aubé JohanneORCID1, Cueff-Gauchard ValerieORCID1, Reveillaud JulieORCID2
Affiliation(s) 1 : Univ Brest, CNRS, IFREMER, Laboratoire de Microbiologie des Environnements Extrêmes, 29280, Plouzané, France
2 : MIVEGEC, Univ. Montpellier, INRAe, CNRS, IRD, Montpellier, France
Source Microbiome (2049-2618) (Springer Science and Business Media LLC), 2021-04 , Vol. 9 , N. 1 , P. 87 (16p.)
DOI 10.1186/s40168-021-01045-6
WOS© Times Cited 11
Keyword(s) Niche partitioning, Rimicaris, Metagenome-assembled genomes, Zetaproteobacteria, Holobiont, Hydrothermal vents
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.

Full Text
File Pages Size Access
Publisher's official version 16 3 MB Open access
Additional file 1. Details and scheme of the bioinformatics pipeline 74 KB Open access
Additional file 2. Quality trimming and filtering statistics for each individual, number of assembled contigs longer than 1 kbp for each site, and number of reads recruited by these contigs for ... 54 KB Open access
Additional file 3. MAG collection, estimates of completion and redundancy calculated based on the occurrence of Single-copy Core Genes (SCG),... 142 KB Open access
Additional file 4. GeTMM normalized counts of each MAG 69 KB Open access
Additional file 5. DESeq2 results table with baseMean, Log2FoldChange, lfcSE, stat, pvalue and padj for each of the 49 studied MAGs 47 KB Open access
Additional file 6. Differentially abundants MAGs between site identified through DESeq2. MAGs are indicated with the family they belong when they are affiliated until this level. Positive... 120 KB Open access
Additional file 7. PhyloFlash analysis results. Heatmap of taxonomic assignments (rows) for small-subunit rRNA reads in the six individual metagenomes (columns). The plot was generated using with ... 92 KB Open access
Additional file 8 BLAST of 16S rRNA genes for Zetaproteobacteria. BLASTN search were performed between the 16S ... 76 KB Open access
Additional file 9 A . Maximum-likelihood tree based on concatenated marker proteins according to the GTDB-Tk genome phylogeny visualized using anvi’o. Tree includes 600 genomes from GTDB ... 242 KB Open access
Additional file 10 Key gene predictions from Zetaproteobacterial MAGs RB_MAG_00008 and TAG_MAG_00014 and free-living Ghiorsea bivora reference... 189 KB Open access
Additional file 11. Table containing the names of all genes found per MAG using KEGG and COG annotation 5 MB Open access
Additional file 12 Iron genes and gene clusters identified by FeGenie for the 49 MAGs and reference genomes Ghiorsea bivora and Mariprofundus ferrooxydans PV-1... 84 KB Open access
Additional file 13 Differential coverage of contigs within Zetaproteobacteria bins. Static image from the anvi’o refine display for A. RB_MAG_00008 and B. TAG_MAG_00014. From inner... 181 KB Open access
Additional file 14 Analysis supplement: analysis details of metabolic potential among Rimicaris epibionts as depicted in Fig. 5 44 KB Open access
KEGG Decoder heat map representing metabolic pathway completeness of the MAGs based on the presence or absence of genes as determined by KEGG Decoder... 254 KB Open access
Correction - 10.1186/s40168-022-01257-4 1 687 KB Open access
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