Investigation of bacterial communities within the digestive organs of the hydrothermal vent shrimp Rimicaris exoculata provide insights into holobiont geographic clustering.
Open accessAbstract
Prokaryotic communities forming symbiotic relationships with the vent shrimp, Rimicaris exoculata, are well studied components of hydrothermal ecosystems at the Mid-Atlantic Ridge (MAR). Despite the tight link between host and symbiont, the observed lack of spatial genetic structure seen in R. exoculata contrasts with the geographic differentiation detected in specific bacterial ectosymbionts. The geographic clustering of bacterial lineages within a seemingly panmictic host suggests either the presence of finer scale restriction to gene flow not yet detected in the host, horizontal transmission (environmental selection) of its endosymbionts as a consequence of unique vent geochemistry, or vertically transmitted endosymbionts that exhibit genetic differentiation. To identify which hypothesis best fits, we tested whether bacterial assemblages exhibit differentiation across sites or host populations by performing a 16S rRNA metabarcoding survey on R. exoculata digestive prokaryote samples (n = 31) taken from three geochemically distinct vents across MAR: Rainbow, Trans-Atlantic Geotraverse (TAG) and Logatchev. Analysis of communities across two organs (digestive tract, stomach), three molt colors (white, red, black) and three life stages (eggs, juveniles, adults) also provided insights into symbiont transmission mode. Examining both whole communities and operational taxonomic units (OTUs) confirmed the presence of three main epibionts: Epsilonproteobacteria, Mollicutes and Deferribacteres. With these findings, we identified a clear pattern of geographic segregation by vent in OTUs assigned to Epsilonproteobacteria. Additionally, we detected evidence for differentiation among all communities associated to vents and life stages. Overall, results suggest a combination of environmental selection and vertical inheritance of some of the symbiotic lineages.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Our metabarcoding results provide a second report of Entomoplasmatales on the eggs of R. exoculata with a different sequencing technique: Illumina MiSeq versus 454 Pyrosequencing used in Cowart et al. (2017).
“Despite their very low abundance, our metabarcoding results provide a second report of this group on the eggs of R. exoculata with a different sequencing technique: Illumina MiSeq versus 454 Pyrosequencing used in 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 Cowart et al. (2017)
The Materials and methods section says Cowart et al. used 454 pyrosequencing on R. exoculata samples that included eggs. The Discussion (‘Bacterial communities over the life cycle’; no page given) reports very few Mollicutes in eggs, but our copy does not identify the egg-associated bacteria specifically as Entomoplasmatales. Thus the cited paper supports the sequencing comparison and a broader bacterial-group finding, not the claimed prior report of Entomoplasmatales on eggs. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.22.4673 · Cited by 64,617 · see citing works
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
Kumar, S., Stecher, G., & Tamura, K. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw054 · Cited by 43,923 · see citing works
QIIME allows analysis of high-throughput community sequencing data
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., et al. (2010) · Nature Methods · doi:10.1038/nmeth.f.303 · Cited by 34,887 · see citing works
Search and clustering orders of magnitude faster than BLAST
Edgar, R. C. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq461 · Cited by 20,617 · see citing works
PAST: PALEONTOLOGICAL STATISTICAL SOFTWARE PACKAGE FOR EDUCATION AND DATA ANALYSIS
Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001) · Palaeontologia Electronica · Cited by 17,871 · see citing works
Median-joining networks for inferring intraspecific phylogenies
Bandelt, H. J., Forster, P., & Rohl, A. (1999) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026036 · Cited by 11,742 · see citing works
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB
DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., Huber, T., Dalevi, D., Hu, P., & Andersen, G. L. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.03006-05 · Cited by 10,891 · see citing works
Pruesse, E., Quast, C., Knittel, K., Fuchs, B. M., Ludwig, W., Peplies, J., & Glöckner, F. O. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm864 · Cited by 6,682 · see citing works
Nonparametric estimation of the number of classes in a population
Chao, A. (1984) · Scandinavian Journal of Statistics · Cited by 4,263 · see citing works
PyNAST: a flexible tool for aligning sequences to a template alignment
Caporaso, J. G., Bittinger, K. L., Bushman, F. D., DeSantis, T. Z., Andersen, G. L., & Knight, R. D. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp636 · Cited by 3,374 · see citing works
Multivariate analyses in microbial ecology
Ramette, A. (2007) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2007.00375.x · Cited by 1,928 · see citing works
Wang, Y., & Qian, P. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007401 · Cited by 1,270 · see citing works
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
Defining operational taxonomic units using DNA barcode data
Blaxter, M., Mann, J., Chapman, T. W., Thomas, F., Whitton, C., Floyd, R., & Abebe, E. (2005) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2005.1725 · Cited by 885 · see citing works
Douville, É., Charlou, J., Oelkers, É. H., Bienvenu, P., Colon, C. F. J., Donval, J., Fouquet, Y., Prieur, D., & Appriou, P. (2002) · Chemical Geology · doi:10.1016/s0009-2541(01)00351-5 · Cited by 701 · see citing works
Emerson, D., & Moyer, C. L. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.6.3085-3093.2002 · Cited by 447 · see citing works
Childress, J. J., & Fisher, C. R. (2000) · Time to knit · doi:10.1016/0967-0653(93)91450-q · Cited by 402 · see citing works
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
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
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
Loudon, A. H., Woodhams, D. C., Parfrey, L. W., Archer, H. M., Knight, R. D., McKenzie, V. J., & Harris, R. N. (2013) · The ISME Journal · doi:10.1038/ismej.2013.200 · Cited by 306 · see citing works
Desbruyères, D., Biscoito, M., Caprais, J., Colaço, A., Comtet, T., Crassous, P., Fouquet, Y., Khripounoff, A., Bris, N. L., Olu, K., et al. (2001) · Deep Sea Research Part I Oceanographic Research Papers · doi:10.1016/s0967-0637(00)00083-2 · Cited by 302 · see citing works
Tivey, M. K., Humphris, S. E., Thompson, G., Hannington, M. D., & Rona, P. A. (1995) · Journal of Geophysical Research: Solid Earth · doi:10.1029/95jb00610 · Cited by 268 · see citing works
Rozas, J., & Rozas, R. (1995) · Computer applications in the biosciences · doi:10.1093/bioinformatics/11.6.621 · Cited by 248 · see citing works
Mira, Á., & Moran, N. A. (2002) · Microbial Ecology · doi:10.1007/s00248-002-0012-9 · Cited by 244 · see citing works
Severmann, S., Johnson, C. M., Beard, B. L., German, C. R., Edmonds, H. N., Chiba, H., & Green, D. R. H. (2004) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2004.06.001 · Cited by 221 · see citing works
Dominance of one bacterial phylotype at a Mid-Atlantic Ridge hydrothermal vent site.
Polz, M. F., & Cavanaugh, C. M. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.16.7232 · Cited by 217 · see citing works
Fouquet, Y., Cambon, P., Etoubleau, J., Charlou, J. L., Ondréas, H., Barriga, F. J. A. S., Cherkashov, G., Semkova, T., Poroshina, I., Bohn, M., et al. (2010) · Geophysical Monograph Series · doi:10.1029/2008gm000746 · Cited by 216 · see citing works
Parasites: proxies for host genealogy and ecology?
Nieberding, C. M., & Olivieri, I. (2006) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2006.11.012 · Cited by 215 · see citing works
Flores, G. E., Campbell, J. H., Kirshtein, J. D., Meneghin, J., Podar, M., Steinberg, J. I., Seewald, J. S., Tivey, M. K., Voytek, M. A., Yang, Z. K., et al. (2011) · Environmental Microbiology · doi:10.1111/j.1462-2920.2011.02463.x · Cited by 209 · see citing works
Charlou, J. L., Donval, J. P., Konn, C., Ondréas, H., Fouquet, Y., Jean‐Baptiste, P., & Fourré, É. (2010) · Geophysical monograph · doi:10.1029/2008gm000752 · Cited by 196 · see citing works
Influence of sea-floor spreading on the global hydrothermal vent fauna
Tunnicliffe, V., & Fowler, C. M. R. (1996) · Nature · doi:10.1038/379531a0 · Cited by 170 · see citing works
Feeding biology of the shrimp Rimicaris exoculata at hydrothermal vents on the Mid-Atlantic Ridge
Dover, C. L. V., Fry, B., Grassle, J. F., Humphris, S. E., & Rona, P. A. (1988) · Marine Biology · doi:10.1007/bf00391196 · Cited by 160 · 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:10.1163/193724086x00299 · Cited by 140 · 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
The organic complexation of dissolved iron along the U.S. GEOTRACES (GA03) North Atlantic Section
Buck, K. N., Sohst, B. M., & Sedwick, P. N. (2015) · Deep Sea Research Part II Topical Studies in Oceanography · doi:10.1016/j.dsr2.2014.11.016 · Cited by 119 · see citing works
Thompson, G., Mottl, M. J., & Rona, P. A. (1985) · Chemical Geology · doi:10.1016/0009-2541(85)90159-7 · Cited by 114 · see citing works
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
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-citationBougault, H., Charlou, J., Fouquet, Y., Needham, H. D., Vaslet, N., Appriou, P., Jean‐Baptiste, P., Rona, P. A., Dmitriev, L. V., & Silantiev, S. (1993) · Journal of Geophysical Research Atmospheres · doi:10.1029/93jb00508 · Cited by 104 · see citing works
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-citationDurand, 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-citationZbinden, M., Le Bris, N., Gaill, F., & Compère, P. (2004) · Marine Ecology Progress Series · doi:10.3354/meps284237 · Cited by 95 · see citing works
Teixeira, S., Cambon‐Bonavita, M., Serrão, E. Á., Desbruyères, D., & Arnaud‐Haond, S. (2010) · Journal of Biogeography · doi:10.1111/j.1365-2699.2010.02408.x · Cited by 92 · see citing works
Self-citationZbinden, 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
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-citationJan, C., Petersen, J. M., Werner, J., Teeling, H., Huang, S., Glöckner, F. O., Golyshina, O. V., Dubilier, N., Golyshin, P. N., Jebbar, M., et al. (2014) · Environmental Microbiology · doi:10.1111/1462-2920.12406 · Cited by 83 · see citing works
Self-citationMiroshnichenko, M. L., Slobodkin, A. I., Kostrikina, N. A., L’Haridon, S., Nercessian, O., Spring, S., Stackebrandt, E. S., Bonch-Osmolovskaya, E. A., & Jeanthon, C. (2003) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.02673-0 · Cited by 82 · see citing works
Teixeira, S., Serrão, E. Á., & Arnaud‐Haond, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038521 · Cited by 82 · see citing works
Self-citationHügler, 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
Aires, T., Serrão, E. Á., Kendrick, G. A., Duarte, C. M., & Arnaud‐Haond, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068429 · Cited by 70 · see citing works
Self-citationCorbari, L., Zbinden, M., Cambon-Bonavita, M., Gaill, F., & Compère, P. (2008) · Aquatic Biology · doi:10.3354/ab00024 · Cited by 67 · see citing works
Gloter, A., Zbinden, M., Guyot, F., Gaill, F., & Colliex, C. (2004) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2004.03.040 · Cited by 61 · see citing works
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
Slobodkina, G. B., Kolganova, T. V., Chernyh, N. A., et al. (2009) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.006767-0 · Cited by 45 · see citing works
Phylum BIX. Deferribacteres phy. nov.
Garrity, G. M., Holt, J. M., Huber, H., STETTER, K. O., Greene, A. C., Patel, B. K. C., Caccavo, F., Allison, M. J., MacGregor, B. J., & Stahl, D. A. (2001) · Springer eBooks · doi:10.1007/978-0-387-21609-6_26 · Cited by 34 · see citing works
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
Self-citationKaspari, M. E., Stevenson, B. S., Shik, J. Z., & Kerekes, J. F. (2010) · Ecology · doi:10.1890/09-2089.1 · Cited by 27 · see citing works
Fluid and gas fluxes from the Logatchev hydrothermal vent area
Schmale, O., Walter, M., von Deimling, J. S., Sültenfuß, J., Walker, S. L., Rehder, G., & Keir, R. S. (2012) · Geochemistry Geophysics Geosystems · doi:10.1029/2012gc004158 · Cited by 12 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [1]Childress J, Fisher C. The biology of hydrothermal vent animals: physiology, biochemistry, and autotrophic symbioses. Oceanography and marine biology: an annual review. 1992; 30: 337– 441.
- [52]Garrity G, Holt J, Huber H, Stetter K, Greene A, Patel B, et al. Deferribacteres phy. nov.. In: Springer, editor. Bergey’s Manual of Systematic Bacteriology New York2001. p. 465–71.
Cited by
Sorted by citations
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
- Authors
- Cowart, D. A., Durand, L., Cambon-Bonavita, M.-A., & Arnaud-Haond, S.
- Affiliations
- Ifremer (FR)
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2017-03-15
- Volume
- 12
- Issue
- 3
- Pages
- e0172543
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC5351989
- OpenAlex
- W2603935660
- Cited by
- 17
- References
- 59
- Citations by year
- 2025: 1 · 2024: 1 · 2023: 2 · 2022: 5 · 2021: 2 · 2020: 2 · 2019: 2 · 2018: 2
- FWCI
- 1.24
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Institutional Archive of Ifremer (French Research Institute for Exploitation of the Sea) (submittedVersion, other-oa)
- HAL (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- European Union (FP7, Hermione project)
- Ifremer
- 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 › Agricultural and Biological Sciences › Insect Science › Insect symbiosis and bacterial influences
- Keywords
- Rimicaris exoculata, hydrothermal vent shrimp, holobiont, symbiotic bacteria, geographic clustering, endosymbionts, epibionts, Epsilonproteobacteria, Mollicutes, Deferribacteres, symbiont transmission, vertical transmission, horizontal transmission, life stages, gastrointestinal tract, Mid-Atlantic Ridge, TAG hydrothermal field, Logatchev hydrothermal field, Rainbow hydrothermal field, 16S rRNA metabarcoding
- MeSH terms
- Animals, Crustacea, Geography, Gastrointestinal Tract
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
