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Dual symbiosis of the vent shrimp Rimicaris exoculata with filamentous gamma‐ and epsilonproteobacteria at four Mid‐Atlantic Ridge hydrothermal vent fields
Abstract
The shrimp Rimicaris exoculata from hydrothermal vents on the Mid-Atlantic Ridge (MAR) harbours bacterial epibionts on specialized appendages and the inner surfaces of its gill chamber. Using comparative 16S rRNA sequence analysis and fluorescence in situ hybridization (FISH), we examined the R. exoculata epibiosis from four vents sites along the known distribution range of the shrimp on the MAR. Our results show that R. exoculata lives in symbiosis with two types of filamentous epibionts. One belongs to the Epsilonproteobacteria, and was previously identified as the dominant symbiont of R. exoculata. The second is a novel gammaproteobacterial symbiont that belongs to a clade consisting exclusively of sequences from epibiotic bacteria of hydrothermal vent animals, with the filamentous sulfur oxidizer Leucothrix mucor as the closest free-living relative. Both the epsilon- and the gammaproteobacterial symbionts dominated the R. exoculata epibiosis at all four MAR vent sites despite striking differences between vent fluid chemistry and distances between sites of up to 8500 km, indicating that the symbiosis is highly stable and specific. Phylogenetic analyses of two mitochondrial host genes showed little to no differences between hosts from the four vent sites. In contrast, there was significant spatial structuring of both the gamma- and the epsilonproteobacterial symbiont populations based on their 16S rRNA gene sequences that was correlated with geographic distance along the MAR. We hypothesize that biogeography and host-symbiont selectivity play a role in structuring the epibiosis of R. exoculata.
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“The symbiotic bacterial assemblages are diverse in both cephalothorax and gut compartments, but are usually dominated by Epsilonbacteraeota and Gammaproteobacteria in the cephalothorax (Zbinden et al., 2008; Petersen et al., 2010; Jan et al., 2014) and by Deferribacteres, Entomoplamatales, and Epsilonbacteraeota in the gut (Durand et al., 2010, 2015; Cowart et al., 2017).”
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 Petersen et al., 2010
In the citing paper
“Whereas Epsilonbacteraeota- and Gammaproteobacteria-related lineages have been found in abundance in the surrounding fluids (Petersen 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 Petersen et al., 2010
In the citing paper
“Epsilonbacteraeota and thiotrophic Gammaproteobacteria are often described as sulfur oxidizers thriving in close but differing environmental niches due to their metabolic capacities (Petersen et al., 2010; Meier et al., 2017).”
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 Petersen et al., 2010
In the citing paper
“Surprisingly, although they have been reported as the dominant symbionts within the R. exoculata cephalothorax in many studies (Petersen et al., 2010; Hügler et al., 2011; Guri et al., 2012), establishment of Epsilonbacteraeota from the Sulfurovaceae family was not as favored on egg envelopes as it was on pleopods.”
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 Petersen et al., 2010
In the citing paper
“Occurrence of Epsilonbacteraeota, Gammaproteobacteria and Zetaproteobacteria symbiont-related lineages in vent fluids and microbial mats of vent sites where R. exoculata also lives (Petersen et al., 2010; Scott et al., 2015) supports the hypothesis of a horizontal transmission mode for these three groups.”
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 Petersen et al., 2010
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Metadata
- Authors
- Petersen, J. M., Ramette, A., Lott, C., Cambon‐Bonavita, M., Zbinden, M., & Dubilier, N.
- Affiliations
- Max Planck Institute for Marine Microbiology (DE)
- Centre National de la Recherche Scientifique (FR)
- Évolution Paris Seine (FR)
- Corresponding author
- Dubilier, Nicole
- ORCID
- Venue
- Environmental Microbiology
- Publisher
- Wiley
- Published
- 2010-08
- Volume
- 12
- Issue
- 8
- Pages
- 2204-2218
- ISSN
- 1462-2912 (ISSN-L)
- 1462-2920
- OpenAlex
- W2045870877
- Cited by
- 107
- References
- 79
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 3 · 2023: 4 · 2022: 10 · 2021: 9 · 2020: 7 · 2019: 9 · 2018: 5 · 2017: 9 · 2016: 6 · 2015: 5 · 2014: 8 · 2013: 7 · 2012: 7
- FWCI
- 5.53
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Environmental Microbiology (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Topics
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine Biology and Ecology Research
- Physical Sciences › Environmental Science › Environmental Chemistry › Methane Hydrates and Related Phenomena
- Keywords
- Rimicaris exoculata, epibiosis, Mid-Atlantic Ridge, Gammaproteobacteria, Epsilonproteobacteria, Leucothrix mucor, sulfur-oxidizing bacteria, bacterial biogeography, host-symbiont specificity
- MeSH terms
- Animals, DNA, Bacterial, DNA, Mitochondrial, Gills, Molecular Sequence Data, Phylogeny, RNA, Ribosomal, 16S, Symbiosis, In Situ Hybridization, Fluorescence, Sequence Analysis, DNA, Gammaproteobacteria, Epsilonproteobacteria, Decapoda, Hydrothermal Vents
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