Microbial diversity associated with the hydrothermal shrimp Rimicaris exoculata gut and occurrence of a resident microbial community

Durand, Lucile; Zbinden, Magali; Cueff-Gauchard, ValÃ©rie; Duperron, SÃ©bastien; Roussel, Erwan G.; Shillito, Bruce; Cambon-Bonavita, Marie-Anne

doi:10.1111/j.1574-6941.2009.00806.x

Cited by 100Microbial Community Ecology and PhysiologyMarine Biology and Ecology ResearchAquaculture disease management and microbiota

Microbial diversity associated with the hydrothermal shrimp Rimicaris exoculata gut and occurrence of a resident microbial community

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Durand, Lucile, Zbinden, Magali, Cueff-Gauchard, ValÃ©rie, Duperron, SÃ©bastien, Roussel, Erwan G., Shillito, Bruce, Cambon-Bonavita, Marie-Anne·2010·FEMS Microbiology Ecology

DOI 10.1111/j.1574-6941.2009.00806.x

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Abstract

Rimicaris exoculata dominates the megafauna of several Mid-Atlantic Ridge hydrothermal sites. Its gut is full of sulphides and iron-oxide particles and harbours microbial communities. Although a trophic symbiosis has been suggested, their role remains unclear. In vivo starvation experiments in pressurized vessels were performed on shrimps from Rainbow and Trans-Atlantic Geotraverse sites in order to expel the transient gut contents. Microbial communities associated with the gut of starved and reference shrimps were compared using 16S rRNA gene libraries and microscopic observations (light, transmission and scanning electron microscopy and FISH analyses). We show that the gut microbiota of shrimps from both sites included mainly Deferribacteres, Mollicutes, Epsilon- and Gammaproteobacteria. For the first time, we have observed filamentous bacteria, inserted between microvilli of gut epithelial cells. They remained after starvation periods in empty guts, suggesting the occurrence of a resident microbial community. The bacterial community composition was the same regardless of the site, except for Gammaproteobacteria retrieved only in Rainbow specimens. We observed a shift in the composition of the microbiota of long-starved specimens, from the dominance of Deferribacteres to the dominance of Gammaproteobacteria. These results reinforce the hypothesis of a symbiotic relationship between R. exoculata and its gut epibionts.

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As the gut has no cuticle layer and is not subjected to surface renewal during molting, symbionts in the gut are supposedly maintained throughout the life of the animal following their acquisition.
“In contrast, as the gut has no cuticle layer and is thus not subjected to surface renewal during molting, symbionts in this part of the body are supposedly maintained throughout the life of the animal following their acquisition (Durand et al., 2010).”
From 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 (2019) · cites this paper as Durand et al., 2010
The gut-anatomy section (lines 264–266) describes the R. exoculata midgut as lacking a cuticle, and the microbial-communities section (lines 314–316) says it does not undergo exuviation, probably favouring long-term colonization. The paper does not establish that acquired symbionts persist throughout the animal’s life; it supports long-term residence as a possibility, not lifetime maintenance. (LLM, conf=0.86)
Experimental — accuracy not yet measured
R. exoculata hosts a distinct epibiotic microbial community in their gut.
“Moreover, shrimps host a distinct epibiotic microbial community in their gut (Zbinden and Cambon-Bonavita, 2003; Durand et al., 2010, 2015).”
From 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 (2019) · cites this paper as Durand et al., 2010

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“Re-crustin was slightly detected in the digestive tract, which is colonized by a microbial community different from the one of the cephalothoracic cavity (28, 29).”
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PROTOCOLO PARA LA EXTRACCIÓN DE ADN METAGENÓMICO BACTERIANO DEL LANGOSTINO Macrobrachium carcinus L (PROTOCOL FOR EXTRACTION OF BACTERIAL METAGENOME DNA TO PRAWN Macrobrachium carcinus L)
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Images de science : Survivre à des fumerolles toxiques… grâce à son microbiote
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Additional file 15 of Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria
Cambon‐Bonavita, M., Aubé, J., Cueff‐Gauchard, V., & Réveillaud, J. (2021) · Figshare · doi:10.6084/m9.figshare.14404267
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Additional file 14 of Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria
Cambon‐Bonavita, M., Aubé, J., Cueff‐Gauchard, V., & Réveillaud, J. (2021) · Figshare · doi:10.6084/m9.figshare.14404264
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Additional file 9 of Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria
Cambon‐Bonavita, M., Aubé, J., Cueff‐Gauchard, V., & Réveillaud, J. (2021) · Figshare · doi:10.6084/m9.figshare.14404294
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Additional file 3 of Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria
Cambon‐Bonavita, M., Aubé, J., Cueff‐Gauchard, V., & Réveillaud, J. (2021) · Figshare · doi:10.6084/m9.figshare.14404276
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Additional file 2 of Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria
Cambon‐Bonavita, M., Aubé, J., Cueff‐Gauchard, V., & Réveillaud, J. (2021) · Figshare · doi:10.6084/m9.figshare.14404273
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Additional file 8 of Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria
Cambon‐Bonavita, M., Aubé, J., Cueff‐Gauchard, V., & Réveillaud, J. (2021) · Figshare · doi:10.6084/m9.figshare.14404291
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Additional file 13 of Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria
Cambon‐Bonavita, M., Aubé, J., Cueff‐Gauchard, V., & Réveillaud, J. (2021) · Figshare · doi:10.6084/m9.figshare.14404261
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Additional file 16 of Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria
Cambon‐Bonavita, M., Aubé, J., Cueff‐Gauchard, V., & Réveillaud, J. (2021) · Figshare · doi:10.6084/m9.figshare.14404270
Self-citation
Additional file 7 of Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria
Cambon‐Bonavita, M., Aubé, J., Cueff‐Gauchard, V., & Réveillaud, J. (2021) · Figshare · doi:10.6084/m9.figshare.14404288
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Additional file 5 of Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria
Cambon‐Bonavita, M., Aubé, J., Cueff‐Gauchard, V., & Réveillaud, J. (2021) · Figshare · doi:10.6084/m9.figshare.14404282
Self-citation
Additional file 4 of Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria
Cambon‐Bonavita, M., Aubé, J., Cueff‐Gauchard, V., & Réveillaud, J. (2021) · Figshare · doi:10.6084/m9.figshare.14404279
Self-citation
Additional file 10 of Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria
Cambon‐Bonavita, M., Aubé, J., Cueff‐Gauchard, V., & Réveillaud, J. (2021) · Figshare · doi:10.6084/m9.figshare.14404252
Self-citation
Additional file 11 of Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria
Cambon‐Bonavita, M., Aubé, J., Cueff‐Gauchard, V., & Réveillaud, J. (2021) · Figshare · doi:10.6084/m9.figshare.14404255
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Georgieva, M. N., Durand, L., Cambon‐Bonavita, M., Little, C. T. S., Bribiesca‐Contreras, G., Copley, J., Stewart, E. C. D., Eliès, P., Svavarsson, J., Bogason, E., et al. (2026) · Biology Letters · doi:10.1098/rsbl.2026.0111
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Biogeographical distribution ofRimicaris exoculataresident gut epibiont communities along the Mid-Atlantic Ridge hydrothermal vent sites
Durand, L., Roumagnac, M., Cueff-Gauchard, V., Jan, C., Guri, M., Tessier, C., Haond, M., Crassous, P., Zbinden, M., Arnaud-Haond, S., et al. (2015) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiv101 · Cited by 32 · see citing works
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Occurrence of Deferribacterales and Entomoplasmatales in the deep-sea Alvinocarid shrimp Rimicaris exoculata gut.
Zbinden, M., & Cambon-Bonavita, M.-A. (2003) · FEMS Microbiology Ecology · doi:10.1016/s0168-6496(03)00176-4 · Cited by 101 · see citing works
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Archive Institutionnelle de l’Ifremer Occurrence of Deferribacterales and Entomoplasmatales in the deep-sea Alvinocarid shrimp Rimicaris exoculata gut
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Analysis on the diversity of culturable epibiotic microbes on the gills of hydrothermal shrimp Rimicaris sp.from the South Mid-Atlantic Ridge
Zong-ze, S. (2013) · Journal of Applied Oceanography
New insigths on the metabolic diversity among the epibiotic microbial community of the hydrothermal shrimp Rimicaris exoculata.
Zbinden, M., Shillito, B., Bris, N. L., de Montlaur, C. D. V., Roussel, E. G., Guyot, F., Gaill, F., & Cambon‐Bonavita, M. (2008) · HAL
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Authors: Durand, L., Zbinden, M., Cueff-Gauchard, V., Duperron, S., Roussel, E. G., Shillito, B., & Cambon-Bonavita, M.-A.
Affiliations: Ifremer (FR)
Centre National de la Recherche Scientifique (FR)
ORCID: Durand, Lucile
Zbinden, Magali
Roussel, Erwan G.
Shillito, Bruce
Venue: FEMS Microbiology Ecology
Publisher: Oxford University Press (OUP)
Published: 2010-02
Volume: 71
Issue: 2
Pages: 291-303
ISSN: 0168-6496 (ISSN-L)
1574-6941
DOI: 10.1111/j.1574-6941.2009.00806.x
OpenAlex: W2140734550
Cited by: 100
References: 66
Citations by year: 2026: 2 · 2025: 1 · 2024: 4 · 2023: 3 · 2022: 6 · 2021: 18 · 2020: 5 · 2019: 8 · 2018: 8 · 2017: 9 · 2016: 6 · 2015: 7 · 2014: 6 · 2013: 2 · 2012: 6
FWCI: 4.37
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: FEMS Microbiology Ecology (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Institutional Archive of Ifremer (French Research Institute for Exploitation of the Sea) (submittedVersion)
ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
Funders: Agence Nationale de la Recherche (ANR-06-BDIV-0005)
Centre National de la Recherche Scientifique
Région Bretagne
Topics: Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine Biology and Ecology Research
Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
Keywords: Rimicaris exoculata, gut microbiota, symbiosis, starvation, Deferribacteres, Gammaproteobacteria, Mollicutes, filamentous bacteria, epibionts, Mid-Atlantic Ridge, hydrothermal vents
MeSH terms: Animals, Bacteria, DNA, Bacterial, Phylogeny, RNA, Ribosomal, 16S, Symbiosis, Gene Library, In Situ Hybridization, Fluorescence, Sequence Analysis, DNA, Decapoda, Gastrointestinal Tract

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Microbial diversity associated with the hydrothermal shrimp Rimicaris exoculata gut and occurrence of a resident microbial community

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