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

Type Article
Acceptance Date 2022-01 IN PRESS
Language English
Author(s) Aubé Johanne1, Cambon-Bonavita Marie-AnneORCID1, Velo-Suárez Lourdes3, Cueff-Gauchard Valerie1, Lesongeur Francoise1, Guéganton Marion1, Durand Lucile1, Reveillaud Julie2
Affiliation(s) 1 : Univ Brest, Ifremer, CNRS, Unité Biologie des Environnements Extrêmes marins Profonds, F-29280, Plouzané, France
2 : MIVEGEC, Univ. Montpellier, INRAe, CNRS, IRD, Montpellier, France
3 : Univ Brest, INSERM, EFS, UMR 1078, GGB, F-29200 Brest, France andCentre Brestois d’Analyse du Microbiote (CBAM), Brest University Hospital, Brest, France
Source Preprint (Research Square Platform LLC) In Press
DOI 10.21203/rs.3.rs-1584541/v1
Note This is a preprint ; it has not been peer reviewed by a journal
Keyword(s) Rimicaris exoculata, symbiosis, digestif system, 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.

Full Text
File Pages Size Access
Preprint 28 653 KB Open access
Supplementary Material 6 MB Open access
Table S1 42 KB Open access
Table S2 26 KB Open access
Table S3 17 KB Open access
Table S4 37 KB Open access
Table S5 9 KB Open access
Table S6 26 KB Open access
Top of the page

How to cite 

Aubé Johanne, Cambon-Bonavita Marie-Anne, Velo-Suárez Lourdes, Cueff-Gauchard Valerie, Lesongeur Francoise, Guéganton Marion, Durand Lucile, Reveillaud Julie A novel and dual digestive symbiosis scales up the nutrition and immune system of the holobiont Rimicaris exoculata. Preprint IN PRESS. Publisher's official version : https://doi.org/10.21203/rs.3.rs-1584541/v1 , Open Access version : https://archimer.ifremer.fr/doc/00768/87957/