Is It First the Egg or the Shrimp? – Diversity and Variation in Microbial Communities Colonizing Broods of the Vent Shrimp Rimicaris exoculata During Embryonic Development

Type Article
Date 2019-04
Language English
Author(s) Methou Pierre1, 2, Hernández-Ávila Ivan1, 2, Aube Johanne1, Cueff-Gauchard Valerie1, Gayet Nicolas2, Amand Louis3, Shillito Bruce3, Pradillon Florence2, Cambon-Bonavita Marie-Anne1
Affiliation(s) 1 : Univ Brest, CNRS, Ifremer, Laboratoire de Microbiologie des Environnements Extrêmes, Plouzané, France
2 : Ifremer, Laboratoire Environnement Profond (REM/EEP/LEP), Plouzané, France
3 : Unité Biologie des Organismes et Ecosystèmes Aquatiques, Muséum National d’Histoire Naturelle, Eq. Adaptations aux Milieux Extrêmes (BOREA), CNRS, IRD, Sorbonne Université, Université de Caen Normandie, Université des Antilles, Paris, France
Source Frontiers In Microbiology (1664-302X) (Frontiers Media SA), 2019-04 , Vol. 10 , N. 808 , P. 19p.
DOI 10.3389/fmicb.2019.00808
Keyword(s) hydrothermal, shrimp, microbial colonization, Alvinocarididae, egg development
Abstract

Rimicaris exoculata is one of the most well-known and emblematic species of endemic vent fauna. Like many other species from these ecosystems, Rimicaris shrimps host important communities of chemosynthetic bacteria living in symbiosis with their host inside the cephalothorax and gut. For many of these symbiotic partners, the mode of transmission remains to be elucidated and the starting point of the symbiotic relationship is not yet defined, but could begin with the egg. In this study, we explored the proliferation of microbial communities on R. exoculata broods through embryonic development using a combination of NGS sequencing and microscopy approaches. Variations in abundance and diversity of egg microbial communities were analyzed in broods at different developmental stages and collected from mothers at two distinct vent fields on the Mid-Atlantic Ridge (TAG and Snake Pit). We also assessed the specificity of the egg microbiome by comparing communities developing on egg surfaces with those developing on the cuticle of pleopods, which are thought to be exposed to similar environmental conditions because the brood is held under the female’s abdomen. In terms of abundance, bacterial colonization clearly increases with both egg developmental stage and the position of the egg within the brood: those closest to the exterior having a higher bacterial coverage. Bacterial biomass increase also accompanies an increase of mineral precipitations and thus clearly relates to the degree of exposure to vent fluids. In terms of diversity, most bacterial lineages were found in all samples and were also those found in the cephalothorax of adults. However, significant variation occurs in the relative abundance of these lineages, most of this variation being explained by body surface (egg vs. pleopod), vent field, and developmental stage. The occurrence of symbiont-related lineages of Epsilonbacteraeota, Gammaproteobacteria, Zetaproteobacteria, and Mollicutes provide a basis for discussion on both the acquisition of symbionts and the potential roles of these bacterial communities during egg development.

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Publisher's official version 19 4 MB Open access
FIGURE S1 | X-Ray Spectrophotometric analysis (EDX) showing SEM analyzed areas of mineral crusts or mineral deposits for each sample with the corresponding spectrum.... 5 817 KB Open access
FIGURE S2 | Venn diagrams representing the numbers of shared OTUs across all samples. Affiliations of taxa representative of a body structure, vent field, or developmental stage are indicated. 1 194 KB Open access
FIGURE S3 | Alpha diversity measures of OTU number (Richness) and Inverse Simpson index (Evenness) compared (A) between eggs and pleopods, (B) between TAG and Snake Pit egg samples,... 1 929 KB Open access
FIGURE S4 | Mean relative abundances per categories of 16S rRNA gene sequence reads according to their classification (Silva 132 database). Groups are at the family level for the .... 1 87 KB Open access
FIGURE S5 | Ranked LDA scores of the differentially abundant bacterial taxa, with taxa with highest relative abundance at TAG in orange, and taxa with highest relative abundance at Snake Pit in blue.. 1 1 MB Open access
FIGURE S6 | Ranked LDA scores of the differentially abundant bacterial taxa, with taxa with highest relative abundance at early stage in yellow, at mid stage in brown and at late stage in purple for.. 1 902 KB Open access
FIGURE S7 | Additional FISH observations of Rimicaris exoculata eggs. Observations were performed on semi-thin sections (2 μm) stained with DAPI (blue) (A) Early stage egg hybridized with 1 7 MB Open access
TABLE S1 | List of samples used in this study. 11 KB Open access
TABLE S2 | List of FISH probes used in this study. 9 KB Open access
TABLE S3 | PERMANOVA analysis. 10 KB Open access
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How to cite 

Methou Pierre, Hernández-Ávila Ivan, Aube Johanne, Cueff-Gauchard Valerie, Gayet Nicolas, Amand Louis, Shillito Bruce, Pradillon Florence, Cambon-Bonavita Marie-Anne (2019). Is It First the Egg or the Shrimp? – Diversity and Variation in Microbial Communities Colonizing Broods of the Vent Shrimp Rimicaris exoculata During Embryonic Development. Frontiers In Microbiology, 10(808), 19p. Publisher's official version : https://doi.org/10.3389/fmicb.2019.00808 , Open Access version : https://archimer.ifremer.fr/doc/00489/60067/