A novel and dual digestive symbiosis scales up the nutrition and immune system of the holobiont Rimicaris exoculata

Type Article
Date 2022-11
Language English
Author(s) Aubé Johanne1, Cambon-Bonavita Marie-AnneORCID1, Velo-Suárez Lourdes1, 2, Cueff-Gauchard Valerie1, Lesongeur Francoise1, Guéganton Marion1, Durand Lucile1, Reveillaud Julie1, 3
Affiliation(s) 1 : Univ Brest, Ifremer, CNRS, Unité Biologie des Environnements Extrêmes marins Profonds, F-29280, Plouzané, France
2 : Univ Brest, INSERM, EFS, UMR 1078, GGB, F-29200 Brest, France andCentre Brestois d’Analyse du Microbiote (CBAM), Brest University Hospital, Brest, France
3 : MIVEGEC, Univ. Montpellier, INRAe, CNRS, IRD, Montpellier, France
Source Microbiome (2049-2618) (BMC), 2022-11 , Vol. 10 , N. 1 , P. 189 (17p.)
DOI 10.1186/s40168-022-01380-2
Keyword(s) Rimicaris exoculata, Digestive symbiosis, Hepatoplasmataceae, Deferribacteres, Immunity, Metagenomics
Abstract

Background

In deep-sea hydrothermal vent areas, deprived of light, most animals rely on chemosynthetic symbionts for their nutrition. These symbionts may be located on their cuticle, inside modified organs, or in specialized cells. Nonetheless, many of these animals have an open and functional digestive tract. The vent shrimp Rimicaris exoculata is fueled mainly by its gill chamber symbionts, but also has a complete digestive system with symbionts. These are found in the shrimp foregut and midgut, but their roles remain unknown. We used genome-resolved metagenomics on separate foregut and midgut samples, taken from specimens living at three contrasted sites along the Mid-Atlantic Ridge (TAG, Rainbow, and Snake Pit) to reveal their genetic potential.

Results

We reconstructed and studied 20 Metagenome-Assembled Genomes (MAGs), including novel lineages of Hepatoplasmataceae and Deferribacteres, abundant in the shrimp foregut and midgut, respectively. Although the former showed streamlined reduced genomes capable of using mostly broken-down complex molecules, Deferribacteres showed the ability to degrade complex polymers, synthesize vitamins, and encode numerous flagellar and chemotaxis genes for host-symbiont sensing. Both symbionts harbor a diverse set of immune system genes favoring holobiont defense. In addition, Deferribacteres were observed to particularly colonize the bacteria-free ectoperitrophic space, in direct contact with the host, elongating but not dividing despite possessing the complete genetic machinery necessary for this.

Conclusion

Overall, these data suggest that these digestive symbionts have key communication and defense roles, which contribute to the overall fitness of the Rimicaris holobiont.

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Supplementary Figure 1. PhyloFlash heatmap of taxonomic assignments (rows, with prokaryotes in blue and eukaryotes in red) for small-subunit rRNA reads in the six individual foregut and midgut... 1 26 KB Open access
Supplementary Figure 2. KEGG Decoder heatmap showing the completeness of the metabolic pathways of the MAGs based on gene presence or absence. The top dendrogram represents the similarity between... 1 17 KB Open access
Supplementary Figure 3. Number of CAZYmes families observed for the different MAG families. 1 6 KB Open access
Supplementary Table 1. Description of metagenomes and assemblies. Number of metagenomic short reads sequenced and mapped to the different assemblies and MAGs. 42 KB Open access
Supplementary Table 2. Description of MAGs. Anvi’o statistics, mean coverage of MAGs and taxonomic assignments obtained with GTDB-Tk 37 KB Open access
Supplementary Table 3. MAG single-copy core genes for domain bacteria for each of the 20 studied MAGs. 17 KB Open access
Supplementary Table 4. List and copy numbers of the genes featured in Figure 4. 36 KB Open access
Supplementary Table 5. CRISPRs with evidence level 4 and their cas genes found in the MAG contigs. 9 KB Open access
Supplementary Table 6. gANI percent identity and percent alignment coverage between Deferribacteres and Hepatoplasmataceae MAGs and their most closely related GTDB genomes. 27 KB Open access
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How to cite 

Aubé Johanne, Cambon-Bonavita Marie-Anne, Velo-Suárez Lourdes, Cueff-Gauchard Valerie, Lesongeur Francoise, Guéganton Marion, Durand Lucile, Reveillaud Julie (2022). A novel and dual digestive symbiosis scales up the nutrition and immune system of the holobiont Rimicaris exoculata. Microbiome, 10(1), 189 (17p.). Publisher's official version : https://doi.org/10.1186/s40168-022-01380-2 , Open Access version : https://archimer.ifremer.fr/doc/00768/87957/