The gill chamber epibiosis of deep‐sea shrimp R imicaris exoculata : an in‐depth metagenomic investigation and discovery of Z etaproteobacteria

Jan, Cyrielle; Petersen, Jillian M.; Werner, Johannes; Teeling, Hanno; Huang, Sixing; Glöckner, Frank Oliver; Golyshina, Olga V.; Dubilier, Nicole; Golyshin, Peter N.; Jebbar, Mohamed; Cambon‐Bonavita, Marie‐Anne

doi:10.1111/1462-2920.12406

Cited by 83Microbial Community Ecology and PhysiologyMarine Biology and Ecology ResearchMetal Extraction and Bioleaching

The gill chamber epibiosis of deep‐sea shrimp R imicaris exoculata : an in‐depth metagenomic investigation and discovery of Z etaproteobacteria

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Jan, Cyrielle, Petersen, Jillian M., Werner, Johannes, Teeling, Hanno, Huang, Sixing, Glöckner, Frank Oliver, Golyshina, Olga V., Dubilier, Nicole +3 more·2014·Environmental Microbiology

DOI 10.1111/1462-2920.12406

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Abstract

The gill chamber of deep-sea hydrothermal vent shrimp Rimicaris exoculata hosts a dense community of epibiotic bacteria dominated by filamentous Epsilonproteobacteria and Gammaproteobacteria. Using metagenomics on shrimp from the Rainbow hydrothermal vent field, we showed that both epibiont groups have the potential to grow autotrophically and oxidize reduced sulfur compounds or hydrogen with oxygen or nitrate. For carbon fixation, the Epsilonproteobacteria use the reductive tricarboxylic acid cycle, whereas the Gammaproteobacteria use the Calvin-Benson-Bassham cycle. Only the epsilonproteobacterial epibionts had the genes necessary for producing ammonium. This ability likely minimizes direct competition between epibionts and also broadens the spectrum of environmental conditions that the shrimp may successfully inhabit. We identified genes likely to be involved in shrimp-epibiont interactions, as well as genes for nutritional and detoxification processes that might benefit the host. Shrimp epibionts at Rainbow are often coated with iron oxyhydroxides, whose origin is intensely debated. We identified 16S rRNA sequences and functional genes affiliated with iron-oxidizing Zetaproteobacteria, which indicates that biological iron oxidation might play a role in forming these deposits. Fluorescence in situ hybridizations confirmed the presence of active Zetaproteobacteria in the R. exoculata gill chamber, thus providing the first evidence for a Zetaproteobacteria-invertebrate association.

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Zetaproteobacteria are iron oxidizers that also use the CBB cycle.
“Zetaproteobacteria are iron oxidizers that also use the CBB cycle (Field et al., 2014; Jan et al., 2014).”
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 Jan et al., 2014
Section 2.2.6 states that characterized Zetaproteobacteria are iron oxidizers, but says the shrimp-gill epibionts are only *likely* to oxidize iron. The Carbon fixation section reports CBB-cycle genes in the zetaproteobacterial taxobin and says these indicate the *potential* for autotrophic growth; it does not establish that these epibionts use the cycle. (LLM, conf=0.84)
Experimental — accuracy not yet measured
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 Jan et al., 2014
The Introduction (page unavailable) identifies an epibiotic community in the adult shrimp’s cephalothorax. The Conclusions (page unavailable) suggest that oxygen or sulfide availability might influence how its symbionts coexist, but do not describe observed differences in community composition according to vent-fluid composition. The Jan et al. citation is attached to the shrimp claim, not the separate statement about other vent species. (LLM, conf=0.78)
Experimental — accuracy not yet measured
Symbiotic bacterial assemblages are diverse in both cephalothorax and gut compartments, but are usually dominated by Epsilonbacteraeota and Gammaproteobacteria in the cephalothorax and by Deferribacteres, Entomoplamatales, and Epsilonbacteraeota in the gut.
“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 Jan et al., 2014
In the present study, symbiont-related lineages of Zetaproteobacteria or Entomoplasmatales previously reported in R. exoculata cephalothorax or gut were also retrieved.
“In our present study, in addition to the previous ones, symbiont-related lineages of Zetaproteobacteria or Entomoplasmatales previously reported in R. exoculata, cephalothorax or gut were also retrieved (Zbinden and Cambon-Bonavita, 2003; Jan et al., 2014).”
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 Jan et al., 2014
Zetaproteobacteria have already been reported in close association with R. exoculata but never in such high relative abundance.
“Zetaproteobacteria have already been reported in close association with R. exoculata but never in such high relative abundance (Jan et al., 2014).”
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 Jan et al., 2014

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The RAST Server: Rapid Annotations using Subsystems Technology
Aziz, R. K., Bartels, D., Best, A. A., DeJongh, M., Disz, T. L., Edwards, R. A., Formsma, K., Gerdes, S., Glass, E. M., Kubal, M., et al. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-75 · Cited by 11,777 · see citing works
Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations
Amann, R., Binder, B. J., Olson, R. J., Chisholm, S. W., Devereux, R., & Stahl, D. A. (1990) · Applied and Environmental Microbiology · doi:10.1128/aem.56.6.1919-1925.1990 · Cited by 3,998 · see citing works
Evolution and classification of the CRISPR–Cas systems
Makarova, K. S., Haft, D. H., Barrangou, R., Brouns, S. J. J., Charpentier, E., Horvath, P., Moineau, S., Mojica, F. J. M., Wolf, Y. I., Yakunin, A. F., et al. (2011) · Nature Reviews Microbiology · doi:10.1038/nrmicro2577 · Cited by 2,512 · see citing works
CRISPR/Cas, the Immune System of Bacteria and Archaea
Horvath, P., & Barrangou, R. (2010) · Science · doi:10.1126/science.1179555 · Cited by 2,471 · see citing works
CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats
Grissa, I., Vergnaud, G., & Pourcel, C. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm360 · Cited by 1,877 · see citing works
Symbiotic diversity in marine animals: the art of harnessing chemosynthesis
Dubilier, N., Bergin, C., & Lott, C. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1992 · Cited by 1,073 · see citing works
Self-citation
CRISPR — a widespread system that provides acquired resistance against phages in bacteria and archaea
Sorek, R., Kunin, V., & Hugenholtz, P. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1793 · Cited by 909 · see citing works
Geochemistry of high H2 and CH4 vent fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36°14′N, MAR)
Charlou, J., Donval, J., Fouquet, Y., Jean‐Baptiste, P., & Holm, N. G. (2002) · Chemical Geology · doi:10.1016/s0009-2541(02)00134-1 · Cited by 909 · see citing works
Ecological Aspects of the Distribution of Different Autotrophic CO 2 Fixation Pathways
Berg, I. A. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.02473-10 · Cited by 821 · see citing works
Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere.
Whittaker, C., & Hynes, R. (2002) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-05-0259 · Cited by 788 · see citing works
Inter-kingdom signalling: Communication between bacteria and their hosts
Hughes, D. T., & Sperandio, V. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1836 · Cited by 761 · see citing works
Beyond the Calvin Cycle: Autotrophic Carbon Fixation in the Ocean
Hügler, M., & Sievert, S. M. (2010) · Annual Review of Marine Science · doi:10.1146/annurev-marine-120709-142712 · Cited by 683 · see citing works
The versatile ε-proteobacteria: key players in sulphidic habitats
Campbell, B. J., Engel, A. S., Porter, M. L., & Takai, K. (2006) · Nature Reviews Microbiology · doi:10.1038/nrmicro1414 · Cited by 681 · see citing works
GenDB--an open source genome annotation system for prokaryote genomes
Meyer, F. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg312 · Cited by 673 · see citing works
Oxidation of Reduced Inorganic Sulfur Compounds by Bacteria: Emergence of a Common Mechanism?
Friedrich, C. G., Röther, D., Bardischewsky, F., Quentmeier, A., & Fischer, J. (2001) · Applied and Environmental Microbiology · doi:10.1128/aem.67.7.2873-2882.2001 · Cited by 656 · see citing works
Exopolysaccharide Production Is Required for Development of Escherichia coli K-12 Biofilm Architecture
Danese, P. N., Pratt, L. A., & Kolter, R. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.12.3593-3596.2000 · Cited by 656 · see citing works
Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene
Zhu, F., Massana, R., Not, F., Marie, D., & Vaulot, D. (2004) · FEMS Microbiology Ecology · doi:10.1016/j.femsec.2004.10.006 · Cited by 643 · see citing works
The Prokaryotes: a handbook on the biology of bacteria
(2007) · Choice Reviews Online · doi:10.5860/choice.45-0025 · Cited by 638 · see citing works
Interspecies communication in bacteria
Federle, M. J., & Bassler, B. L. (2003) · Journal of Clinical Investigation · doi:10.1172/jci20195 · Cited by 601 · see citing works
Inorganic polyphosphate: toward making a forgotten polymer unforgettable
Kornberg, A. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.3.491-496.1995 · Cited by 583 · see citing works
Cyclic Diguanylate Is a Ubiquitous Signaling Molecule in Bacteria: Insights into Biochemistry of the GGDEF Protein Domain
Ryjenkov, D. A., Tarutina, M. G., Moskvin, O. V., & Gomelsky, M. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.5.1792-1798.2005 · Cited by 577 · see citing works
Structural Classification of Bacterial Response Regulators: Diversity of Output Domains and Domain Combinations
Galperin, M. Y. (2006) · Journal of Bacteriology · doi:10.1128/jb.01887-05 · Cited by 501 · see citing works
The Second Skin: Ecological Role of Epibiotic Biofilms on Marine Organisms
Wahl, M., Goecke, F., Labes, A., Dobretsov, S., & Weinberger, F. (2012) · Frontiers in Microbiology · doi:10.3389/fmicb.2012.00292 · Cited by 465 · see citing works
Methane and sulfate profiles within the subsurface of a tidal flat are reflected by the distribution of sulfate-reducing bacteria and methanogenic archaea
Wilms, R., Sass, H., Köpke, B., Cypionka, H., & Engelen, B. (2006) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2006.00225.x · Cited by 437 · see citing works
Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle
Badger, M. R., & Bek, E. J. (2008) · Journal of Experimental Botany · doi:10.1093/jxb/erm297 · Cited by 435 · see citing works
Nitrogen Excretion: Three End Products, Many Physiological Roles
Wright, P. A. (1995) · Journal of Experimental Biology · doi:10.1242/jeb.198.2.273 · Cited by 423 · see citing works
Evidence for a system of general protein glycosylation in Campylobacter jejuni
Szymanski, C. M., Yao, R., Ewing, C. P., Trevor J. TRUST, & Guerry, P. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01415.x · Cited by 414 · see citing works
Protein glycosylation in bacterial mucosal pathogens
Szymanski, C. M., & Wren, B. W. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1100 · Cited by 405 · see citing works
A Novel Lineage of Proteobacteria Involved in Formation of Marine Fe-Oxidizing Microbial Mat Communities
Emerson, D., Rentz, J. A., Lilburn, T., Davis, R. E., Aldrich, H. C., Chan, C. S., & Moyer, C. L. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000667 · Cited by 398 · see citing works
Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the ε-Proteobacteria isolated from Okinawa Trough hydrothermal sediments
Inagaki, F., Takai, K., Nealson, K. H., & Horikoshi, K. (2004) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.03042-0 · Cited by 389 · see citing works
Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses
Tyson, G. W., & Banfield, J. F. (2007) · Environmental Microbiology · doi:10.1111/j.1462-2920.2007.01444.x · Cited by 326 · see citing works
Hydrogen is an energy source for hydrothermal vent symbioses
Petersen, J. M., Zielinski, F., Pape, T., Seifert, R., Moraru, C., Amann, R., Hourdez, S., Girguis, P. R., Wankel, S. D., Barbe, V., et al. (2011) · Nature · doi:10.1038/nature10325 · Cited by 323 · see citing works
Self-citation
Molecular Biology of Microbial Hydrogenases
Vignais, P. M., & Colbeau, A. (2004) · Current Issues in Molecular Biology · doi:10.21775/cimb.006.159 · Cited by 320 · see citing works
The bacterial cytochrome cbb3 oxidases
Pitcher, R. S., & Watmough, N. J. (2004) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2003.09.017 · Cited by 317 · see citing works
Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing -proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough
Inagaki, F. (2003) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.02682-0 · Cited by 271 · see citing works
Distribution, phylogenetic diversity and physiological characteristics of epsilon‐ Proteobacteria in a deep‐sea hydrothermal field
Nakagawa, S., Takai, K., Inagaki, F., Hirayama, H., Nunoura, T., Horikoshi, K., & Sako, Y. (2005) · Environmental Microbiology · doi:10.1111/j.1462-2920.2005.00856.x · Cited by 266 · see citing works
Genome of the Epsilonproteobacterial Chemolithoautotroph Sulfurimonas denitrificans
Sievert, S. M., Scott, K. M., Klotz, M. G., Chain, P., Hauser, L., Hemp, J., Hügler, M., Land, M., Lapidus, A. L., Larimer, F. W., et al. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01844-07 · Cited by 264 · see citing works
The Path of Carbon in Photosynthesis. XXI. The Cyclic Regenerationof Carbon Dioxide Acceptor
Bassham, J. A., USAEC, Benson, A., Kay, L., Harris, A., Wilson, A., & Calvin, M. (1953) · doi:10.2172/915417 · Cited by 256 · see citing works
Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas
Takai, K., Suzuki, M., Nakagawa, S., et al. (2006) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.64255-0 · Cited by 248 · see citing works
Deep-sea vent ε-proteobacterial genomes provide insights into emergence of pathogens
Nakagawa, S., Takaki, Y., Shimamura, S., Reysenbach, A., Takai, K., & Horikoshi, K. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700687104 · Cited by 246 · see citing works
Physiological Proteomics of the Uncultured Endosymbiont of Riftia pachyptila
Markert, S., Arndt, C., Felbeck, H., et al. (2007) · Science · doi:10.1126/science.1132913 · Cited by 227 · see citing works
Niche differentiation among sulfur-oxidizing bacterial populations in cave waters
Macalady, J. L., Dattagupta, S., Schaperdoth, I., et al. (2008) · The ISME Journal · doi:10.1038/ismej.2008.25 · Cited by 212 · see citing works
Enzymatic and Genetic Characterization of Carbon and Energy Metabolisms by Deep-Sea Hydrothermal Chemolithoautotrophic Isolates ofEpsilonproteobacteria
Takai, K., Campbell, B. J., Cary, S. C., Suzuki, M., Oida, H., Nunoura, T., Hirayama, H., Nakagawa, S., Suzuki, Y., Inagaki, F., et al. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.11.7310-7320.2005 · Cited by 201 · see citing works
Similarities and Differences in the Glycosylation Mechanisms in Prokaryotes and Eukaryotes
Dell, A., Galadari, A., Sastre, F., & Hitchen, P. G. (2010) · International Journal of Microbiology · doi:10.1155/2010/148178 · Cited by 190 · see citing works
Genome and physiology of a model Epsilonproteobacterium responsible for sulfide detoxification in marine oxygen depletion zones
Grote, J., Schott, T., Bruckner, C. G., Glöckner, F. O., Jost, G., Teeling, H., Labrenz, M., & Jürgens, K. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1111262109 · Cited by 170 · see citing works
Self-citation
Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum
Hensen, D., Sperling, D., Trüper, H. G., Brune, D. C., & Dahl, C. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05408.x · Cited by 170 · see citing works
The High-Molecular-Weight Cytochrome c Cyc2 of Acidithiobacillus ferrooxidans Is an Outer Membrane Protein
Yarzábal, L. A., Brasseur, G., Ratouchniak, J., Lund, K., Lemesle-Meunier, D., DeMoss, J. A., & Bonnefoy, V. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.1.313-317.2002 · Cited by 168 · see citing works
Type II Protein Secretion in Pseudomonas aeruginosa : the Pseudopilus Is a Multifibrillar and Adhesive Structure
Durand, É., Bernadac, A., Ball, G., et al. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.9.2749-2758.2003 · Cited by 167 · see citing works
ADAPTATIONS TO SULFIDE BY HYDROTHERMAL VENT ANIMALS: SITES AND MECHANISMS OF DETOXIFICATION AND METABOLISM
Powell, M. A., & Somero, G. N. (1986) · Biological Bulletin · doi:10.2307/1541923 · Cited by 167 · see citing works
Abundance of Reverse Tricarboxylic Acid Cycle Genes in Free-Living Microorganisms at Deep-Sea Hydrothermal Vents
Campbell, B. J., & Cary, S. C. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.10.6282-6289.2004 · Cited by 163 · see citing works
The IS4 family of insertion sequences: evidence for a conserved transposase motif
Rezsöhazy, R., Hallet, B., Delcour, J., et al. (1993) · Molecular Microbiology · doi:10.1111/j.1365-2958.1993.tb01258.x · Cited by 157 · see citing works
Sulfur Metabolisms in Epsilon- and Gamma-Proteobacteria in Deep-Sea Hydrothermal Fields
Yamamoto, M., & Takai, K. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00192 · Cited by 151 · see citing works
Mariprofundus ferrooxydans PV-1 the First Genome of a Marine Fe(II) Oxidizing Zetaproteobacterium
Singer, E., Emerson, D., Webb, E. A., Barco, R. A., Kuenen, J. G., Nelson, W. C., Chan, C. S., Comolli, L. R., Ferriera, S., Johnson, J. H., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025386 · Cited by 147 · see citing works
Diversity, relative abundance and metabolic potential of bacterial endosymbionts in three Bathymodiolus mussel species from cold seeps in the Gulf of Mexico
Duperron, S., Sibuet, M., MacGregor, B. J., Kuypers, M. M. M., Fisher, C. R., & Dubilier, N. (2007) · Environmental Microbiology · doi:10.1111/j.1462-2920.2007.01259.x · Cited by 146 · see citing works
Self-citation
TWO NEW CARIDEAN SHRIMPS (BRESILIIDAE) FROM A HYDROTHERMAL FIELD ON THE MID-ATLANTIC RIDGE
Williams, A. B., & Rona, P. A. (1986) · Journal of Crustacean Biology · doi:10.1163/193724086x00299 · Cited by 140 · see citing works
Complete Genome Sequence of the Marine, Chemolithoautotrophic, Ammonia-Oxidizing Bacterium Nitrosococcus oceani ATCC 19707
Klotz, M. G., Arp, D. J., Chain, P., et al. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.00463-06 · Cited by 138 · see citing works
Ecosystem processes and interactions in a morass of diversity
Prosser, J. I. (2012) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2012.01435.x · Cited by 134 · see citing works
Comparative genomic analysis of carbon and nitrogen assimilation mechanisms in three indigenous bioleaching bacteria: predictions and validations
Levicán, G. J., Ugalde, J. A., Ehrenfeld, N., Maass, A., & Parada, P. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-581 · Cited by 131 · see citing works
Two New Caridean Shrimps (Bresiliidae) from a Hydrothermal Field on the Mid-Atlantic Ridge
Williams, A. B., & Rona, P. A. (1986) · Journal of Crustacean Biology · doi:10.2307/1548184 · Cited by 129 · see citing works
Electron transport chains and bioenergetics of respiratory nitrogen metabolism in Wolinella succinogenes and other Epsilonproteobacteria
Kern, M., & Simon, J. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2008.12.010 · Cited by 128 · see citing works
Nitratiruptor tergarcus gen. nov., sp. nov. and Nitratifractor salsuginis gen. nov., sp. nov., nitrate-reducing chemolithoautotrophs of the ε-Proteobacteria isolated from a deep-sea hydrothermal system in the Mid-Okinawa Trough
Nakagawa, S., Takai, K., Inagaki, F., Horikoshi, K., & Sako, Y. (2005) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.63480-0 · Cited by 124 · see citing works
Unexpected co‐occurrence of six bacterial symbionts in the gills of the cold seep mussel Idas sp. (Bivalvia: Mytilidae)
Duperron, S., Halary, S., Lorion, J., Sibuet, M., & Gaill, F. (2007) · Environmental Microbiology · doi:10.1111/j.1462-2920.2007.01465.x · Cited by 123 · see citing works
Analysis of the Pseudoalteromonas tunicata Genome Reveals Properties of a Surface-Associated Life Style in the Marine Environment
Thomas, T., Evans, F. F., Schleheck, D., Mai‐Prochnow, A., Burke, C., Penesyan, A., Dalisay, D. S., Stelzer‐Braid, S., Saunders, N. F. W., Johnson, J. H., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003252 · Cited by 123 · see citing works
Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata
Ponsard, J., Cambon-Bonavita, M.-A., Zbinden, M., Lepoint, G., Joassin, A., Corbari, L., Shillito, B., Durand, L., Cueff-Gauchard, V., & Compère, P. (2013) · The ISME Journal · doi:10.1038/ismej.2012.87 · Cited by 110 · see citing works
Novel Chemoautotrophic Endosymbiosis between a Member of the Epsilonproteobacteria and the Hydrothermal-Vent Gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean
Suzuki, Y., Sasaki, T., Suzuki, M., Nogi, Y., Miwa, T., Takai, K., Nealson, K. H., & Horikoshi, K. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.9.5440-5450.2005 · Cited by 110 · see citing works
Trophic ecology of massive shrimp aggregations at a Mid‐Atlantic Ridge hydrothermal vent site
Polz, M. F., Robinson, J. J., Cavanaugh, C. M., & Dover, C. L. V. (1998) · Limnology and Oceanography · doi:10.4319/lo.1998.43.7.1631 · Cited by 109 · see citing works
Dual symbiosis of the vent shrimp Rimicaris exoculata with filamentous gamma‐ and epsilonproteobacteria at four Mid‐Atlantic Ridge hydrothermal vent fields
Petersen, J. M., Ramette, A., Lott, C., Cambon‐Bonavita, M., Zbinden, M., & Dubilier, N. (2010) · Environmental Microbiology · doi:10.1111/j.1462-2920.2009.02129.x · Cited by 107 · see citing works
Self-citation
Heat-shock response and temperature resistance in the deep-sea vent shrimp Rimicaris exoculata
Ravaux, J., Gaill, F., Bris, N. L., Sarradin, P., Jollivet, D., & Shillito, B. (2003) · Journal of Experimental Biology · doi:10.1242/jeb.00419 · Cited by 106 · see citing works
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
Self-citation
Microbial diversity associated with the hydrothermal shrimpRimicaris exoculatagut and occurrence of a resident microbial community
Durand, L., Zbinden, M., Cueff-Gauchard, V., Duperron, S., Roussel, E. G., Shillito, B., & Cambon-Bonavita, M.-A. (2010) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2009.00806.x · Cited by 100 · see citing works
Self-citation
Peptidoglycan induces loss of a nuclear peptidoglycan recognition protein during host tissue development in a beneficial animal-bacterial symbiosis
Troll, J. V., Adin, D. M., Wier, A. M., Paquette, N., Silverman, N. S., Goldman, W. E., Stadermann, F. J., Stabb, E. V., & McFall‐Ngai, M. (2009) · Cellular Microbiology · doi:10.1111/j.1462-5822.2009.01315.x · Cited by 97 · see citing works
Abundance of Zetaproteobacteria within crustal fluids in back‐arc hydrothermal fields of the Southern Mariana Trough
Kato, S., Yanagawa, K., Sunamura, M., et al. (2009) · Environmental Microbiology · doi:10.1111/j.1462-2920.2009.02031.x · Cited by 95 · see citing works
Distribution of bacteria and associated minerals in the gill chamber of the vent shrimp Rimicaris exoculata and related biogeochemical processes.
Zbinden, M., Le Bris, N., Gaill, F., & Compère, P. (2004) · Marine Ecology Progress Series · doi:10.3354/meps284237 · Cited by 95 · see citing works
Hydrogenimonas thermophila gen. nov., sp. nov., a novel thermophilic, hydrogen-oxidizing chemolithoautotroph within the ε-Proteobacteria, isolated from a black smoker in a Central Indian Ridge hydrothermal field
Takai, K., Nealson, K. H., & Horikoshi, K. (2004) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.02787-0 · Cited by 95 · see citing works
Sulfur Oxidation at Deep-Sea Hydrothermal Vents
Sievert, S. M., Hügler, M., Taylor, C. D., & Wirsen, C. O. (2007) · Springer eBooks · doi:10.1007/978-3-540-72682-1_19 · Cited by 93 · see citing works
New insigths on the metabolic diversity among the epibiotic microbial communitiy of the hydrothermal shrimp Rimicaris exoculata.
Zbinden, M., Shillito, B., Le Bris, N., de Villardi de Montlaur, C., Roussel, E., Guyot, F., Gaill, F., & Cambon-Bonavita, M.-A. (2008) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2008.03.009 · Cited by 89 · see citing works
Multi-step Assembly Pathway of the cbb3-type Cytochrome c Oxidase Complex
Kulajta, C., Thumfart, J. O., Haid, S., Daldal, F., & Koch, H. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.11.039 · Cited by 88 · see citing works
Acquisition of epibiotic bacteria along the life cycle of the hydrothermal shrimp Rimicaris exoculata
Guri, M., Durand, L., Cueff-Gauchard, V., Zbinden, M., Crassous, P., Shillito, B., & Cambon-Bonavita, M.-A. (2012) · The ISME Journal · doi:10.1038/ismej.2011.133 · Cited by 87 · see citing works
Self-citation
Biofilm : mise en place et organisation d’une communauté bactérienne
Filloux, A., & Vallet-Gély, I. (2003) · médecine/sciences · doi:10.1051/medsci/200319177 · Cited by 83 · see citing works
Microbial Enzymes Involved in Carbon Dioxide Fixation.
Atomi, H. (2002) · Journal of Bioscience and Bioengineering · doi:10.1016/s1389-1723(02)80186-4 · Cited by 82 · see citing works
Molecular characterization of inorganic sulfur‐compound metabolism in the deep‐sea epsilonproteobacterium Sulfurovum sp. NBC37‐1
Yamamoto, M., Nakagawa, S., Shimamura, S., et al. (2010) · Environmental Microbiology · doi:10.1111/j.1462-2920.2010.02155.x · Cited by 81 · see citing works
Electron transport to periplasmic nitrate reductase (NapA) of Wolinella succinogenes is independent of a NapC protein
Simon, J., Sänger, M., Schuster, S. C., & Groß, R. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03544.x · Cited by 81 · see citing works
Pathways of carbon and energy metabolism of the epibiotic community associated with the deep-sea hydrothermal vent shrimp Rimicaris exoculata.
Hügler, M., Petersen, J. M., Dubilier, N., Imhoff, J. F., & Sievert, S. M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016018 · Cited by 80 · see citing works
First hsp70 from two hydrothermal vent shrimps, Mirocaris fortunata and Rimicaris exoculata: Characterization and sequence analysis
Ravaux, J., Toullec, J., Léger, N., et al. (2006) · Gene · doi:10.1016/j.gene.2006.09.001 · Cited by 72 · see citing works
Unusual fatty acid composition of storage lipids in the bresilioid shrimp Rimicaris exoculata couples the photic zone with MAR hydrothermal vent sites
Pond, D., Gebruk, A. V., Southward, E., Southward, A., Fallick, A. E., Bell, M., & Sargent, J. (2000) · Marine Ecology Progress Series · doi:10.3354/meps198171 · Cited by 68 · see citing works
Bacterial symbionts and mineral deposits in the branchial chamber of the hydrothermal vent shrimp Rimicaris exoculata: relationship to moult cycle
Corbari, L., Zbinden, M., Cambon-Bonavita, M., Gaill, F., & Compère, P. (2008) · Aquatic Biology · doi:10.3354/ab00024 · Cited by 67 · see citing works
Iron oxide deposits associated with the ectosymbiotic bacteria in the hydrothermal vent shrimp Rimicaris exoculata
Corbari, L., Cambon‐Bonavita, M., Long, G. J., Grandjean, F., Zbinden, M., Gaill, F., & Compère, P. (2008) · Biogeosciences · doi:10.5194/bg-5-1295-2008 · Cited by 65 · see citing works
Self-citation
Taxonomic and Functional Metagenomic Profiling of the Microbial Community in the Anoxic Sediment of a Sub-saline Shallow Lake (Laguna de Carrizo, Central Spain)
Ferrer, M., Guazzaroni, M., Richter, M., et al. (2011) · Microbial Ecology · doi:10.1007/s00248-011-9903-y · Cited by 64 · see citing works
Shell biofilm‐associated nitrous oxide production in marine molluscs: processes, precursors and relative importance
Heisterkamp, I., Schramm, A., Larsen, L. H., Svenningsen, N. B., Lavik, G., de Beer, D., & Stief, P. (2012) · Environmental Microbiology · doi:10.1111/j.1462-2920.2012.02823.x · Cited by 63 · see citing works
JCoast – A biologist-centric software tool for data mining and comparison of prokaryotic (meta)genomes
Richter, M., Lombardot, T., Kostadinov, I., Kottmann, R., Duhaime, M. B., Peplies, J., & Glöckner, F. O. (2008) · BMC Bioinformatics · doi:10.1186/1471-2105-9-177 · Cited by 59 · see citing works
Self-citation
Interactions of Deep-Sea Vent Invertebrates with Their Environment: The Case of Rimicaris exoculata
Schmidt, C., Bris, N. L., & Gaill, F. (2008) · Journal of Shellfish Research · doi:10.2983/0730-8000(2008)27[79:iodviw]2.0.co;2 · Cited by 58 · see citing works
Unveiling microbial life in the new deep‐sea hypersaline Lake Thetis . Part II: a metagenomic study
Ferrer, M., Werner, J., Chernikova, T. N., Bargiela, R., Fernández, L., Cono, V. L., Waldmann, J., Teeling, H., Golyshina, O. V., Glöckner, F. O., et al. (2011) · Environmental Microbiology · doi:10.1111/j.1462-2920.2011.02634.x · Cited by 55 · see citing works
Self-citation
The Nitrogen Cycle: Denitrification and its Relationship to N2 Fixation
van Spanning, R. J. M., Delgado, M. J., & Richardson, D. J. (2005) · Springer eBooks · doi:10.1007/1-4020-3544-6_13 · Cited by 44 · see citing works
Bacterial symbionts of B athymodiolus mussels and E scarpia tubeworms from C hapopote, an asphalt seep in the southern G ulf of M exico
Raggi, L., Schubotz, F., Hinrichs, K., et al. (2012) · Environmental Microbiology · doi:10.1111/1462-2920.12051 · Cited by 42 · see citing works
Regulation of dsr genes encoding proteins responsible for the oxidation of stored sulfur in Allochromatium vinosum
Grimm, F., Dobler, N., & Dahl, C. (2009) · Microbiology · doi:10.1099/mic.0.034645-0 · Cited by 38 · see citing works
Regulation of Hydrogenase Gene Expression
Vignais, P. M. (2008) · Advances in photosynthesis and respiration · doi:10.1007/978-1-4020-8815-5_37 · Cited by 35 · see citing works
Lithoheterotrophic growth and electron transfer chain components of the filamentous gliding bacteriumLeucothrix mucorDSM 2157 during oxidation of sulfur compounds
Grabovich, M. Y., Muntyan, M. S., Lebedeva, V. Y., Ustiyan, V. S., & Дубинина, Г. А. (1999) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1999.tb13772.x · Cited by 25 · see citing works
Biotic and abiotic controls on iron oxyhydroxide formation in the gill chamber of the hydrothermal vent shrimp Rimicaris exoculata
Schmidt, C., Corbari, L., Gaill, F., & Bris, N. L. (2009) · Geobiology · doi:10.1111/j.1472-4669.2009.00209.x · Cited by 18 · see citing works
High production of H-2 and CH4 and abiotic hydrocarbons in ultramafic-hosted hydrothermal systems on the Mid-Atlantic Ridge
Charlou, J., Donval, J., Konn, C., et al. (2010) · Institutional Archive of Ifremer (French Research Institute for Exploitation of the Sea) · doi:10.1016/j.gca.2010.04.028 · Cited by 3 · see citing works

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Research works printed but not linked: 2

Peretó J.G., Velasco A.M., Becerra A. and Lazcano A. (1999). Comparative biochemistry of CO 2 fixation and the evolution of autotrophy. Int Microbiol 2(1): 3-10.
Takai K., Inagaki F., Nakagawa S., Hirayama H., Nunoura T., Sako Y. et al. (2003). Isolation and phylogenetic diversity of members of previously uncultivated Epsilon-Proteobacteria in deep-sea hydrothermal fields. FEMS Microbiology Letters 218: 167-174.

Sorted by citations

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Stokke, R., Dahle, H., Roalkvam, I., Wissuwa, J., Daae, F. L., Tooming‐Klunderud, A., Thorseth, I. H., Pedersen, R. B., & Steen, I. H. (2015) · Environmental Microbiology · doi:10.1111/1462-2920.12970 · Cited by 63 · see citing works
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Methou, P., Hernández-Ávila, I., Aube, J., Cueff-Gauchard, V., Gayet, N., Amand, L., Shillito, B., Pradillon, F., & Cambon-Bonavita, M.-A. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00808 · Cited by 30 · see citing works
Self-citation
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Le Bloa, S., Boidin-Wichlacz, C., Cueff-Gauchard, V., Rosa, R. D., Cuvillier-Hot, V., Durand, L., Methou, P., Pradillon, F., Cambon-Bonavita, M.-A., & Tasiemski, A. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01511 · Cited by 30 · see citing works
Self-citation
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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Cowart, D. A., Durand, L., Cambon-Bonavita, M.-A., & Arnaud-Haond, S. (2017) · PLoS ONE · doi:10.1371/journal.pone.0172543 · Cited by 17 · see citing works
Self-citation
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Le Bloa, S., Durand, L., Cueff- Gauchard, V., Le Bars, J., Taupin, L., Marteau, C., Bazire, A., & Cambon-Bonavita, M.-A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0174338 · Cited by 12 · see citing works

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Robinson, N. J., Lazo-Wasem, E. M., Butler, B. O., et al. (2019) · PLoS ONE · doi:10.1371/journal.pone.0218838 · Cited by 11 · see citing works
Epibiont molluscs on neogastropod shells from sandy bottoms, Pacific coast of Mexico
Olabarría, C. (2000) · Journal of the Marine Biological Association of the United Kingdom · doi:10.1017/s0025315499001861 · Cited by 21 · see citing works
Suctorians (Ciliophora: Suctoria) as epibionts of decapods of families Cambaridae and Pseudothelphusidae
Ramírez-Ballesteros, M., & Mayén‐Estrada, R. (2019) · Zootaxa · doi:10.11646/zootaxa.4648.2.11 · Cited by 1 · see citing works
Reproductive patterns of decapod crustaceans from hydrothermal vents
Dover, C. L. V., Williams, A. B., & Berg, C. J. (1985) · Bulletin of the Biological Society of Washington · Cited by 60 · see citing works
New record of Epistylis hentscheli (Ciliophora, Peritrichia) as an epibiont of Procambarus (Austrocambarus) sp. (Crustacea, Decapoda) in Chiapas, Mexico
Ramírez-Ballesteros, M., Fernández‐Leborans, G., & Mayén‐Estrada, R. (2018) · ZooKeys · doi:10.3897/zookeys.782.26417 · Cited by 5 · see citing works

Authors: Jan, C., Petersen, J. M., Werner, J., Teeling, H., Huang, S., Glöckner, F. O., Golyshina, O. V., Dubilier, N., Golyshin, P. N., Jebbar, M., & Cambon‐Bonavita, M.
Affiliations: Université de Bretagne Occidentale (FR)
Max Planck Institute for Marine Microbiology (DE)
Constructor University (DE)
Bangor University (GB)
Centre National de la Recherche Scientifique (FR)
Ifremer (FR)
Corresponding author: Cambon‐Bonavita, Marie‐Anne
ORCID: Petersen, Jillian M.
Werner, Johannes
Teeling, Hanno
Huang, Sixing
Glöckner, Frank Oliver
Golyshina, Olga V.
Dubilier, Nicole
Golyshin, Peter N.
Jebbar, Mohamed
Cambon‐Bonavita, Marie‐Anne
Venue: Environmental Microbiology
Publisher: Wiley
Published: 2014-03-04
Volume: 16
Issue: 9
Pages: 2723-2738
ISSN: 1462-2912 (ISSN-L)
1462-2920
DOI: 10.1111/1462-2920.12406
OpenAlex: W1813176225
Cited by: 83
References: 99
Citations by year: 2026: 1 · 2025: 1 · 2024: 3 · 2023: 3 · 2022: 11 · 2021: 21 · 2020: 8 · 2019: 6 · 2018: 10 · 2017: 8 · 2016: 5 · 2015: 4 · 2014: 2
FWCI: 5.49
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Environmental Microbiology (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Institutional Archive of Ifremer (French Research Institute for Exploitation of the Sea) (submittedVersion)
Max Planck Digital Library (submittedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion)
Funders: european MAMBA project (FP7-KBBE-2008-226977)
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 › Engineering › Biomedical Engineering › Metal Extraction and Bioleaching
Keywords: Rimicaris exoculata, deep-sea shrimp, Zetaproteobacteria, hydrothermal vent shrimp, Epsilonproteobacteria, Gammaproteobacteria, reductive tricarboxylic acid cycle, Calvin cycle, ammonium production, bacterial metagenomics
MeSH terms: Animals, DNA, Bacterial, Gills, Photosynthesis, RNA, Ribosomal, 16S, Symbiosis, In Situ Hybridization, Fluorescence, Sequence Analysis, DNA, Gammaproteobacteria, Epsilonproteobacteria, Decapoda, Chemoautotrophic Growth, Metagenomics, Carbon Cycle, Hydrothermal Vents

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The gill chamber epibiosis of deep‐sea shrimp R imicaris exoculata : an in‐depth metagenomic investigation and discovery of Z etaproteobacteria

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