Acquisition of epibiotic bacteria along the life cycle of the hydrothermal shrimp Rimicaris exoculata
Open accessAbstract
The caridean shrimp Rimicaris exoculata dominates the fauna at several Mid-Atlantic Ridge hydrothermal vent sites. This shrimp has an enlarged gill chamber, harboring a dense ectosymbiotic community of chemoautotrophic bacteria associated with mineral oxide deposits. Until now, their acquisition is not fully understood. At three hydrothermal vent sites, we analyzed the epibionts diversity at different moult stages and also in the first stages of the shrimp life (eggs, hatched eggs (with larvae) and juveniles). Hatched eggs associated with young larvae were collected for the first time directly from gravid females at the Logachev vent site during the Serpentine cruise. An approach using 16S rRNA clone libraries, scanning and transmission electron microscopy, and fluorescent in situ hybridization was used. Molecular results and microscope observations indicated a switch in the composition of the bacterial community between early R. exoculata life cycle stage (egg libraries dominated by the Gammaproteobacteria) and later stages (juvenile/adult libraries dominated by the Epsilonproteobacteria). We hypothesized that the epibiotic phylotype composition could vary according to the life stage of the shrimp. Our results confirmed the occurrence of a symbiosis with Gammaproteobacteria and Epsilonproteobacteria, but more complex than previously assumed. We revealed the presence of active type-I methanotrophic bacteria colonizing the cephalothorax of shrimps from the Rainbow site. They were also present on the eggs from the Logachev site. This could be the first ‘epibiotic’ association between methanotrophic bacteria and hydrothermal vent crustacean. We discuss possible transmission pathways for epibionts linked to the shrimp life cycle.
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Mother to offspring bacterial transmission has been strongly hypothesized to modulate the microbiota of the eggs of the vent shrimp Rimicaris exoculata.
“Furthermore, mother to offspring bacterial transmission has been strongly hypothesized to modulate the microbiota of the eggs of the vent shrimp Rimicaris exoculata (Guri et al., 2012; Methou et al., 2019).”
From The Active Microbiota of the Eggs and the Nauplii of the Pacific Blue Shrimp Litopenaeus stylirostris Partially Shaped by a Potential Vertical Transmission (2022) · cites this paper as Guri et al., 2012
In “Epibiont diversity and acquisition,” the paper proposes that bacteria in egg mucus could result from mother-to-offspring transmission. But it presents this as a possibility, not a strong hypothesis, and says the egg mucus probably facilitates horizontal transmission instead. (LLM, conf=0.87)
Experimental — accuracy not yet measuredColonization of eggs of R. exoculata by epibiotic bacteria was recently described, and the lineages of Gammaproteobacteria and Epsilonbacteraeota found were the same as those retrieved within the cephalothorax of adults.
“Colonization of eggs of this species by epibiotic bacteria was recently described, and the lineages of Gammaproteobacteria and Epsilonbacteraeota found were the same as those retrieved within the cephalothorax of adults (Guri et al., 2012).”
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 Guri et al., 2012
Our SEM observations confirmed the presence of a mucus-like material surrounding the eggs at every developmental stage.
“As stated in a previous study (Guri et al., 2012), our SEM observations confirmed the presence of a mucus-like material surrounding the eggs at every developmental stage (Figure 2G).”
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 Guri et al., 2012
Similar variations according to vent fluid composition were also described for symbiont communities within the cephalothorax of adult R. exoculata and are not uncommon even in endosymbiotic communities of other vent species.
“Similar variations according to vent fluid composition were also described for symbiont communities within the cephalothorax of adult R. exoculata (Guri et al., 2012; Jan et al., 2014) and are not uncommon even in endosymbiotic communities of other vent species.”
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 Guri et al., 2012
Establishment of Epsilonbacteraeota from the Sulfurovaceae family was not as favored on egg envelopes as it was on pleopods.
“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 Guri et al., 2012
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- Authors
- Guri, M., Durand, L., Cueff-Gauchard, V., Zbinden, M., Crassous, P., Shillito, B., & Cambon-Bonavita, M.-A.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Ifremer (FR)
- Ifremer, DEEP/Laboratoire de Microbiologie des Environnements Extrêmes, UMR6197 , Technopôle Brest Iroise, BP70, Plouzané , France
- Corresponding author
- Guri, Mathieu
- Venue
- The ISME Journal
- Publisher
- Oxford University Press (OUP)
- Published
- 2011-10-13
- Volume
- 6
- Issue
- 3
- Pages
- 597-609
- ISSN
- 1751-7362 (ISSN-L)
- 1751-7370
- PMC
- PMC3280129
- OpenAlex
- W2107696115
- Semantic Scholar
- 1c27cbc2d4b9b6c25172fcbe98becfa51b12f4ff
- Cited by
- 87
- References
- 77
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 6 · 2023: 4 · 2022: 11 · 2021: 19 · 2020: 4 · 2019: 6 · 2018: 2 · 2017: 8 · 2016: 2 · 2015: 7 · 2014: 7 · 2013: 3 · 2012: 2
- FWCI
- 3.38
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The ISME Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Institutional Archive of Ifremer (French Research Institute for Exploitation of the Sea) (submittedVersion)
- Funders
- Institut Français de Recherche pour l'Exploitation de la Mer
- Agence Nationale de la Recherche (ANR-06-BDIV-0005)
- Centre National de la Recherche Scientifique
- 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, epibiotic bacteria, hydrothermal vent shrimp, life stages, bacterial community composition, Gammaproteobacteria, Epsilonproteobacteria, ectosymbiosis, chemoautotrophic bacteria, Mid-Atlantic Ridge
- MeSH terms
- Animals, DNA, Bacterial, Female, Gills, Life Cycle Stages, Phylogeny, RNA, Ribosomal, 16S, Symbiosis, In Situ Hybridization, Fluorescence, Gammaproteobacteria, Epsilonproteobacteria, Decapoda, Hydrothermal Vents
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