Abstract
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.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
Accession codes
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ . (1990). Basic local alignment search tool. J Mol Biol 215: 403–410.
Amann RI, Krumholz L, Stahl DA . (1990). Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172: 762–770.
Bates AE, Harmer TL, Roeselers G, Cavanaugh CM . (2011). Phylogenetic characterization of episymbiotic bacteria hosted by a hydrothermal vent limpet (Lepetodrilidae, Vetigastropoda). Biol Bull 220: 118–127.
Bent SJ, Forney LJ . (2008). The tragedy of the uncommon: understanding limitations in the analysis of microbial diversity. ISME J 2: 689–695.
Brazelton WJ, Schrenk MO, Kelley DS, Baross JA . (2006). Methane- and sulfur-metabolizing microbial communities dominate the Lost City hydrothermal field ecosystem. Appl Environ Microbiol 72: 6257–6270.
Bright M, Bulgheresi S . (2010). A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8: 218–230.
Casanova B, Brunet M, Segonzac M . (1993). Impact of bacterial epibiosis on functional-morphology of shrimp associated with the Mid-Atlantic hydrothermal conditions. Cah Biol Mar 34: 573–588.
Charlou JL, Donval JP, Fouquet Y, Jean-Baptiste P, Holm N . (2002). Geochemistry of high H2 and CH4 vent fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36°14′N, MAR). Chem Geol 191: 345–359.
Chaston J, Goodrich-Blair H . (2010). Common trends in mutualism revealed by model associations between invertebrates and bacteria. FEMS Microbiol Rev 34: 41–58.
Copley CEA, Tyler PA, Varney MS . (1998). Lipid profiles of hydrothermal vent shrimps. Cah Biol Mar 39: 229–231.
Corbari L, Zbinden M, Cambon-Bonavita MA, Gaill F, Compère P . (2008). Bacterial symbionts and mineral deposits in the branchial chamber of the hydrothermal vent shrimp Rimicaris exoculata: relationship to moult cycle. Aquat Biol 1: 225–238.
Costello AM, Lidstrom ME . (1999). Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65: 5066–5074.
Davies JM, Viney C . (1998). Water–mucin phases: conditions for mucus liquid crystallinity. Thermochim Acta 315: 39–49.
Desbruyères D, Biscoito M, Caprais JC, Colaço A, Comtet T, Crassous P et al. (2001). Variations in deep-sea hydrothermal vent communities on the Mid-Atlantic Ridge near the Azores plateau. Deep Sea Res I 48: 1325–1346.
Douville E, Charlou JL, Oelkers EH, Bienvenu P, Colon CFJ, Donval JP et al. (2002). The Rainbow vent fluids (36°14′N, MAR): the influence of ultramafic rocks and phase separation on trace metal content in Mid-Atlantic Ridge hydrothermal fluids. Chem Geol 184: 37–48.
Dubilier N, Bergin C, Lott C . (2008). Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6: 725–740.
Duperron S, De Beer D, Zbinden M, Boetius A, Schipani V, Kahil N et al. (2009a). Molecular characterization of bacteria associated with the trophosome and the tube of Lamellibrachia sp., a siboglinid annelid fromcold seeps in the eastern Mediterranean. FEMS Microbiol Ecol 69: 395–409.
Duperron S, Lorion J, Samadi S, Gros O, Gaill F . (2009b). Symbioses between deep-sea mussels (Mytilidae: Bathymodiolinae) and chemosynthetic bacteria: diversity, function and evolution. C R Biol 332: 298–310.
Duperron S, Nadalig T, Caprais JC, Sibuet M, Fiala-Medioni A, Amann R et al. (2005). Dual symbiosis in a Bathymodiolus sp mussel from a methane seep on the Gabon continental margin (southeast Atlantic): 16S rRNA phylogeny and distribution of the symbionts in gills. Appl Environ Microbiol 71: 1694–1700.
Durand L, Zbinden M, Cueff-Gauchard V, Duperron S, Roussel EG, Shillito B et al. (2010). Microbial diversity associated with the hydrothermal shrimp Rimicaris exoculata gut and occurrence of a resident microbial community. FEMS Microbiol Ecol 71: 291–303.
Fabri MC, Bargain A, Briand P, Gebruk A, Fouquet Y, Morineaux M et al. (2011). The hydrothermal vent community of a new deep-sea field, Ashadze-1, 12°58′N on the Mid-Atlantic Ridge. J Mar Biol Assoc UK 91: 1–13.
Felsenstein J . (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.
Galtier N, Gouy M, Gautier C . (1996). SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12: 543–548.
Gebruk AV, Pimenov NV, Savvichev AS . (1993). Feeding specialization of bresilid shrimps in the TAG site hydrothermal community. Mar Ecol Prog Ser 98: 247–253.
Gilturnes MS, Fenical W . (1992). Embryos of Homarius americanus are protected by epibiotic bacteria. Biol BuII 182: 105–108.
Goffredi SK . (2010). Indigenous ectosymbiotic bacteria associated with diverse hydrothermal vent invertebrates. Environ Microbiol Rep 2: 479–488.
Goffredi SK, Waren A, Orphan VJ, Van Dover CL, Vrijenhoek RC . (2004). Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean. Appl Environ Microbiol 70: 3082–3090.
Good IJ . (1953). The population frequencies of species and the estimation of population parameters. Biometrika 40: 237–264.
Grabovich MY, Muntyan MS, Lebedeva VY, Ustiyan VS, Dubinina GA . (1999). Lithoheterotrophic growth and electron transfer chain components of the filamentous gliding bacterium Leucothrix mucor DSM 2157 during oxidation of sulfur compounds. FEMS Microbiol Lett 178: 155–161.
Hanson RS, Hanson TE . (1996). Methanotrophic bacteria. Microbiol Rev 60: 439–471.
Hügler M, Petersen JM, Dubilier N, Imhoff JF, Sievert SM . (2011). Pathways of carbon and energy metabolism of the epibiotic community associated with the deep-sea hydrothermal vent shrimp Rimicaris exoculata. PLoS Biol 6: e16018.
Inagaki F, Takai K, Nealson KH, Horikoshi K . (2004). Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the e-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. Int J Syst Evol Microbiol 54: 1477–1482.
Komai T, Segonzac M . (2008). Taxonomic review of the hydrothermal vent shrimp genera Rimicaris Williams & Rona and Chorocaris Martin & Hessler (Crustacea: Decapoda: Caridea: Alvinocarididae). J Shellfish Res 27: 21–41.
Lane D . (1991). 16S/23S rRNA sequencing. Nucleic Acid Techn Bact Syst 1: 115–176.
Lin X, Wakeham SG, Putnam IF, Astor YM, Scranton MI, Chistoserdov AY et al. (2006). Comparison of vertical distributions of prokaryotic assemblages in the anoxic Cariaco Basin and Black Sea by use of fluorescence in situ hybridization. Appl Environ Microbiol 72: 2679–2690.
Llodra ER, Tyler PA, Copley JTP . (2000). Reproductive biology of three caridean shrimp, Rimicaris exoculata, Chorocaris chacei and Mirocaris fortunata (Carudea: Decapoda), from hydrothermal vents. J Mar Biol Assoc UK 80: 473–484.
Lopez-Garcia P, Duperron S, Philippot P, Foriel J, Susini J, Moreira D . (2003). Bacterial diversity in hydrothermal sediment and epsilon proteobacterial dominance in experimental microcolonizers at the Mid-Atlantic Ridge. Environ Microbiol 5: 961–976.
Loy A, Lehner A, Lee N, Adamczyk J, Meier H, Ernst J et al. (2002). Oligonucleotide microarray for 16S rRNA gene-based detection of all recognized lineages of sulfate-reducing prokaryotes in the environment. Appl Environ Microbiol 68: 5064–5081.
Manz W, Amann R, Ludwig W, Vancanneyt M, Schleifer KH . (1996). Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Microbiology 142: 1097–1106.
Manz W, Amann R, Ludwig W, Wagner M, Schleifer KH . (1992). Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst Appl Microbiol 15: 593–600.
Mira A, Moran NA . (2002). Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microbial Ecol 44: 137–143.
Muyzer G, Teske A, Wirsen CO, Jannasch HW . (1995). Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164: 165–172.
Nussbaumer AD, Bright M, Baranyi C, Beisser CJ, Ott JA . (2004). Attachment mechanism in a highly specific association between ectosymbiotic bacteria and marine nematodes. Aquat Microb Ecol 34: 239–246.
Petersen JM, Dubilier N . (2009). Methanotrophic symbioses in marine invertebrates. Environ Microbiol 1: 319–335.
Petersen JM, Ramette A, Lott C, Cambon-Bonavita MA, Zbinden M, Dubilier N . (2009). Dual symbiosis of the vent shrimp Rimicaris exoculata with filamentous gamma- and epsilonproteobacteria at four Mid-Atlantic Ridge hydrothermal vent fields. Environ Microbiol 12: 2204–2218.
Polz MF, Cavanaugh CM . (1995). Dominance of one bacterial phylotype at a Mid-Atlantic Ridge hydrothermal vent site. Proc Natl Acad Sci USA 92: 7232–7236.
Polz MF, Robinson JJ, Cavanaugh CM, Van Dover CL . (1998). Trophic ecology of massive shrimp aggregations at a Mid-Atlantic Ridge hydrothermal vent site. Limnol Oceanogr 43: 1631–1638.
Pond DW, Gebruk A, Southward EC, Southward AJ, Fallick AE, Bell MV et al. (2000). Unusual fatty acid composition of storage lipids in the bresilioid shrimp Rimicaris exoculata couples the photic zone with MAR hydrothermal vent sites. Mar Ecol Prog Ser 198: 171–179.
Pond DW, Segonzac M, Bell MV, Dixon DR, Fallick AE, Sargent JR . (1997). Lipid and lipid carbon stable isotope composition of the hydrothermal vent shrimp Mirocaris fortunata: evidence for nutritional dependence on photosynthetically fixed carbon. Mar Ecol Prog Ser 157: 221–231.
Priede IG, Froese R, Bailey DM, Bergstad OA, Collins MA, Dyb JE et al. (2006). The absence of sharks from abyssal regions of the world's oceans. Proc Biol Sci 273: 1435–1441.
Qiu XY, Wu LY, Huang HS, McDonel PE, Palumbo AV, Tiedje JM et al. (2001). Evaluation of PCR-generated chimeras: mutations, and heteroduplexes with 16S rRNA gene-based cloning. Appl Environ Microbiol 67: 880–887.
Ravenschlag K, Sahm K, Pernthaler J, Amann R . (1999). High bacterial diversity in permanently cold marine sediments. Appl Environ Microbiol 65: 3982–3989.
Rieley G, Van Dover CL, Hedrick DB, Eglinton G . (1999). Trophic ecology of Rimicaris exoculata: a combined lipid abundance stable isotope approach. Mar Biol 133: 495–499.
Ruehland C, Dubilier N . (2010). Gamma- and epsilonproteobacterial ectosymbionts of a shallow-water marine worm are related to deep-sea hydrothermal vent ectosymbionts. Environ Microbiol 12: 2312–2326.
Saitou N, Nei M . (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.
Schloss PD, Handelsman J . (2005). Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71: 1501–1506.
Schmidt C, Le Bris N, Gaill F . (2008). Interactions of deep-sea vent invertebrates with their environment: the case of Rimicaris exoculata. J Shellfish Res 27: 79–90.
Schmidt K, Koschinsky A, Garbe-Schönberg D, de Carvalho LM, Seifert R . (2007). Geochemistry of hydrothermal fluids from the ultramafic-hosted Logatchev hydrothermal field, 15°N on the Mid-Atlantic Ridge: temporal and spatial investigation. Chem Geol 242: 1–21.
Segonzac M . (1992). The hydrothermal vent communities of Snake Pit area (Mid-Atlantic Ridge, 23°N, 3480 m)—megafaunal composition and distribution. C R Acad Sci Paris Life Sci 314: 593–600.
Segonzac M, Saint-Laurent M, Casanova B . (1993). Enigma of the trophic adaptation of the shrimp Alvinocarididae in hydrothermal areas along the Mid-Atlantic Ridge. Cah Biol Mar 34: 535–571.
Shillito B, Le Bris N, Gaill A, Rees JF, Zal F . (2004). First access to live Alvinella. High Pressure Res 24: 169–172.
Stahl D, Amann R . (1991). Development and application of nucleic acid probes. In: Stackebrandt E, Goodfellow M (eds). Nucleic Acid Techniques in Bacterial Systematics. Wiley Inc.: New York, pp 205–247.
Teixeira S, Cambon-Bonavita MA, Serrão EA, Desbruyéres D, Arnaud-Haond S . (2011). Recent population expansion and connectivity in the hydrothermal shrimp Rimicaris exoculata along the Mid-Atlantic Ridge. J Biogeography 38: 564–574.
Thompson JD, Higgins DG, Gibson TJ . (1994). ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680.
Tokuda G, Yamada A, Nakano K, Arita NO, Yamasaki H . (2008). Colonization of Sulfurovum sp on the gill surfaces of Alvinocaris longirostris, a deep-sea hydrothermal vent shrimp. Mar Ecol 29: 106–114.
Tyler PA, Young CM . (1999). Reproduction and dispersal at vents and cold seeps. J Mar Biol Assoc UK 79: 193–208.
Van Dover CL, Fry B, Grassle JF, Humphris S, Rona PA . (1988). Feeding biology of the shrimp Rimicaris exoculata at hydrothermal vents on the Mid-Atlantic Ridge. Mar Biol 98: 209–216.
Vereshchaka AL, Vinogradov GM, Ivanenko VN . (1998). General properties of the reproductive biology of some hydrothermal crustacea (shrimp, Amphipods, Copepods). Doklady Biol Sci 360: 269–270.
Williams AB, Rona PA . (1986). Two new caridean shrimps (Bresilidae) from a hydrothermal field on the Mid-Atlantic Ridge. J Crust Biol 6: 446–462.
Zbinden M, Cambon-Bonavita MA . (2003). Occurrence of Deferribacterales and Entomoplasmatales in the deep-sea Alvinocarid shrimp Rimicaris exoculata gut. FEMS Microbiol Ecol 46: 23–30.
Zbinden M, Le Bris N, Gaill F, Compère P . (2004). Distribution of bacteria and associated minerals in the gill chamber of the vent shrimp Rimicaris exoculata and related biogeochemical processes. Mar Ecol Prog Ser 284: 237–251.
Zbinden M, Shillito B, Le Bris N, Villardi de Montlaur C, Roussel E, Guyot F et al. (2008). New insights on the metabolic diversity among the epibiotic microbial community of the hydrothermal shrimp Rimicaris exoculata. J Exp Mar Biol Ecol 359: 131–140.
Acknowledgements
We thank Y Fouquet and F Gaill, respectively, chief scientists of the Serpentine and MoMARDREAM-Naut cruises, as well as the captain and the crew of the Pourquoi pas? and Nautile/Victor teams. We also thank M Perennou and S Romac from the ‘Plateforme Biogenouest’ for sequencing work. TEM was undertaken by the Service de Microscopie Electronique, IFR 83 de Biologie Integrative—CNRS/Paris VI. We also thank I Probert and M Segonzac for advice and comments. This work was supported by Ifremer, CNRS, Brest Metropole Oceane, GDR ECCHIS and ANR Deep Oases.
Author information
Authors and Affiliations
Corresponding author
Additional information
Supplementary Information accompanies the paper on The ISME Journal website
Supplementary information
Rights and permissions
About this article
Cite this article
Guri, M., Durand, L., Cueff-Gauchard, V. et al. Acquisition of epibiotic bacteria along the life cycle of the hydrothermal shrimp Rimicaris exoculata. ISME J 6, 597–609 (2012). https://doi.org/10.1038/ismej.2011.133
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2011.133
Keywords
This article is cited by
-
Shrimp Antimicrobial Peptides: A Multitude of Possibilities
International Journal of Peptide Research and Therapeutics (2022)
-
An H-ferritin from the hydrothermal vent shrimp Rimicaris exoculata and its potential role in iron metabolism
BioMetals (2019)
-
Bacterial biota of shrimp intestine is significantly modified by the use of a probiotic mixture: a high throughput sequencing approach
Helgoland Marine Research (2017)
-
Comparative transcriptome analysis of Rimicaris sp. reveals novel molecular features associated with survival in deep-sea hydrothermal vent
Scientific Reports (2017)
-
Variation in virome diversity in wild populations of Penaeus monodon (Fabricius 1798) with emphasis on pathogenic viruses
VirusDisease (2017)
