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Structure of Manila Clam (Ruditapes philippinarum) Microbiota at the Organ Scale in Contrasting Sets of Individuals

  • Invertebrate Microbiology
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Abstract

Marine invertebrate microbiota has a key function in host physiology and health. To date, knowledge about bivalve microbiota is poorly documented except public health concerns. This study used a molecular approach to characterize the microbiota associated with the bivalve Manila clam (Ruditapes philippinarum) by determining (1) the difference among organs either or not under the influence of host habitat, (2) small-scale variability of microbiota, and (3) the experimental response of the Manila clam microbiota submitted to different lateral transmissions. These questions were investigated by sampling two groups of individuals living in contrasting habitats and carrying out a transplant experiment. Manila clam microbiota (i.e., bacterial community structure) was determined at organ-scale (gills, gut, and a pool of remaining tissues) by capillary electrophoresis DNA fingerprinting (CE fingerprinting). The Manila clam microbiota structure differed among organs indicating a selection of Manila clam microbiota at organ scale. Habitat strongly influenced gill and gut microbiota. In contrast, microbiota associated with remaining tissues was similar between group individuals suggesting that these communities are mostly autochthonous, i.e., Manila clam specific. Transplant experiment showed that improving living condition did not induce any change in microbiota associated with remaining tissues. In contrast, the reduction in individual habitat quality led to individuals in declining health as strongly suggested by the increase in phagocytosis activity and decrease in condition index together with the change in internal organ microbiota. This study provides a first description of the Manila clam holobiont which can withstand disturbance and respond opportunistically to improved environmental conditions.

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References

  1. Noda S, Iida T, Kitade O, Nakajima H, Kudo T, Ohkuma M (2005) Endosymbiotic Bacteroidales bacteria of the flagellated protist Pseudotrichonympha grassii in the gut of the termite Coptotermes formosanus. Appl Environ Microbiol 71:8811–8817

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  2. Kuo RC, Lin S (2013) Ectobiotic and endobiotic bacteria associated with Eutreptiella sp. isolated from long island sound. Protist 164:60–74

    Article  PubMed  Google Scholar 

  3. Gnanamanickam SS (2007) Plant-associated bacteria. Springer

  4. Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N (2010) The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ Microbiol 12:2885–2893

    Article  PubMed Central  PubMed  Google Scholar 

  5. McFall-Ngai MJ (2002) Unseen forces: the influence of bacteria on animal development. Dev Biol 242:1–14

    Article  PubMed  CAS  Google Scholar 

  6. Ruby E, Henderson B, McFall-Ngai M (2004) We get by with a little help from our (little) friends. Science 303:1305–1307

    Article  PubMed  CAS  Google Scholar 

  7. Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–35

    Article  PubMed  CAS  Google Scholar 

  8. Lafferty KD, Porter JW, Ford SE (2004) Are diseases increasing in the ocean? Annu Rev Ecol Evol Syst 35:31–54. doi:10.1146/annurev.ecolsys.35.021103.105704

    Article  Google Scholar 

  9. Plowright RK, Sokolow SH, Gorman ME, Daszak P, Foley JE (2008) Causal inference in disease ecology: investigating ecological drivers of disease emergence. Front Ecol Environ 6(8):420–429. doi:10.1890/070086

    Article  Google Scholar 

  10. Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nature Rev Microbiol 8:218–230

    Article  CAS  Google Scholar 

  11. Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  12. Zurel D, Benayahu Y, Or A, Kovacs A, Gophna U (2011) Composition and dynamics of the gill microbiota of an invasive indo-pacific oyster in the eastern Mediterranean Sea. Environ Microbiol 13:1467–1476

    Article  PubMed  Google Scholar 

  13. Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nature Rev Microbiol 6:725–740

    Article  CAS  Google Scholar 

  14. Tanaka R, Ootsubob M, SawabecT EY, Tajimac K (2004) Biodiversity and in situ abundance of gut microflora of abalone (Haliotis discus hannai) determined by culture-independent techniques. Aquaculture 241:453–463

    Article  Google Scholar 

  15. Beleneva N, Zhukova V (2009) Seasonal dynamics of cell numbers and biodiversity of marine heterotrophic bacteria inhabiting invertebrates and water ecosystems of the peter the great Bay, Sea of Japan. Microbiology 78:369–375

    Article  CAS  Google Scholar 

  16. Dame RF (1996) Ecology of marine bivalves: an ecosystem approach, CRC Marine Science, CRC press, p. 254

  17. Pruzzo C, Gallo G, Canesi L (2005) Persistence of vibrios in marine bivalves: the role of interactions with haemolymph components. Environ Microbiol 7:761–772

    Article  PubMed  Google Scholar 

  18. Antunes F, Hinzmann M, Lopes-Lima M, Machado J, da Costa PM (2010) Association between environmental microbiota and indigenous bacteria found in hemolymph, extrapallial fluid and mucus of Anodonta cygnea (Linnaeus, 1758). Microb Ecol 60:304–309

    Article  PubMed  Google Scholar 

  19. Rosenberg E, Koren O, Reshef L, Efrony R, Rosenberg LZ (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 355:349–360

    Google Scholar 

  20. Webster NS, Blackall LL (2009) What do we really know about sponge-microbial symbioses? The ISME J 3:1–3

    Article  CAS  Google Scholar 

  21. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10

    Article  Google Scholar 

  22. Hansson L, Agis M, Maier C, Weinbauer MG (2009) Community composition of bacteria associated with cold-water coral Madrepora oculata: within and between colony variability. Mar Ecol Prog Ser 397:89–102

    Article  CAS  Google Scholar 

  23. Porporato EMD, Lo Giudice A, Michaud L, De Domenico E, Spanò N (2013) Diversity and antibacterial activity of the bacterial communities associated with Two Mediterranean Sea pens, Pennatula phosphorea and Pteroeides spinosum (Anthozoa: Octocorallia). Microb Ecol 66:701–714

    Article  PubMed  CAS  Google Scholar 

  24. Frias-Lopez J, Zerkle AL, Bonheyo GT, Fouke BW (2002) Partitioning of bacterial communities between seawater and healthy, black band diseased and dead coral surfaces. Appl Environ Microbiol 68:2214–2228

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  25. Cárdenas CA, Bell JJ, Davy SK, Hoggard M, Taylor MW (2014) Influence of environmental variation on symbiotic bacterial communities of two temperate sponges. FEMS Microbiol Ecol. doi:10.1111/1574-6941.12317

    PubMed  Google Scholar 

  26. Neulinger SC, Gartner A, Jarnegren J, Ludvigsen M, Lochte K, Dullo WC (2009) Tissue-associated “candidatus Mycoplasma corallicola” and filamentous bacteria on the cold-water coral Lophelia pertusa (Scleractinia). Appl Environ Microbiol 75:1437–1444

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  27. Sweet MJ, Croquer A, Bythell JC (2011) Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30:39–52

    Article  Google Scholar 

  28. Fan L, Liu M, Simister R, Webster NS, Thomas T (2013) Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress. The ISME J 7:991–1002

    Article  CAS  Google Scholar 

  29. Olson JB, Thacker RW, Gochfeld DJ (2014) Molecular community profiling reveals impacts of time, space, and disease status on the bacterial community associated with the Caribbean sponge Aplysina cauliformis. FEMS Microbiol Ecol 87:268–79. doi:10.1111/1574-6941.12222

    Article  PubMed  CAS  Google Scholar 

  30. Klaus JS, Frias-Lopez J, Bonheyo GT, Heikoop JM, Fouke BW (2005) Bacterial communities inhabiting the healthy tissues of two Caribbean reef corals: interspecific and spatial variation. Coral Reefs 24:129–137

    Article  Google Scholar 

  31. Littman RA, Willis BL, Pfeffer C, Bourne DG (2009) Diversities of coral-associated bacteria differ with location, but not species, for three acroporid corals on the Great Barrier Reef. FEMS Microbiol Ecol 68:152–163

    Article  PubMed  CAS  Google Scholar 

  32. Rodriguez-Lanetty M, Granados-Cifuentes C, Barberan A, Bellantuono A, Bastidas C (2013) Ecological inferences from a deep screening of the complex bacterial consortia associated with the coral, porites astreoides. Mol Ecol 22:4349–62. doi:10.1111/mec.12392

    Article  PubMed  CAS  Google Scholar 

  33. Karlińska-Batres K, Wörheide G (2013) Phylogenetic diversity and community structure of the symbionts associated with the coralline sponge Astrosclera willeyana of the great barrier reef. Microb Ecol 65:740–752

    Article  PubMed  Google Scholar 

  34. Pita L, López-Legentil S, Erwin PM (2013) Biogeography and host fidelity of bacterial communities in Ircinia spp. From the Bahamas. Microb Ecol 66:437–447

    Article  PubMed  CAS  Google Scholar 

  35. Schöttner S, Hoffmann F, Wild C, Rapp HT, Boetius A, Ramette A (2009) Inter- and intra-habitat bacterial diversity associated with cold-water corals. ISME J 3:756–759

    Article  PubMed  Google Scholar 

  36. Cleary DFR, Becking LE, de Voogd NJ, Pires ACC, Polonia ARM, Egas C, Gomes NMC (2013) Habitat- and host-related variation in sponge bacterial symbiont communities in Indonesian waters. FEMS Microbiol Ecol 85:465–482

    Article  PubMed  CAS  Google Scholar 

  37. Charlotte E, Kvennefors E, Sampayo E, Ridgway T, Barnes AC, Hoegh-Guldberg O (2010) Bacterial communities of two ubiquitous great barrier reef corals reveals both site- and species-specificity of common bacterial associates. PLoS ONE 5(4), e10401

    Article  Google Scholar 

  38. FAO (2007) The state of world fisheries and aquaculture, Fisheries and Aquaculture Department, Food and Agriculture. Organization of the United Nations, Rome

  39. Caill-Milly, N, Bobinet, J, Lissardy, M, Morandeau, G, Sanchez, F (2008) Campagne d'évaluation du stock de palourdes du bassin d'Arcachon. Année 2008. In: IFREMER. pp. 1–67

  40. Caill-Milly N, de Casamajor, MN, Lissardy M, Sanchez F, Morandeau G (2003) Evaluation du stock de palourdes du bassin d'Arcachon—Campagne 2003. In: IFREMER. pp. 1–44

  41. Caill-Milly N, Duclercq B, Morandeau G (2006) Campagne d'évaluation du stock de palourdes du bassin d'Arcachon. In: IFREMER. pp. 1–51

  42. Lassalle G, de Montaudouin X, Soudant P, Paillard C (2007) Parasite co-infection of two sympatric bivalves, the Manila clam (Ruditapes philippinarum) and the cockle (Cerastoderma edule) along a latitudinal gradient. Aquat Living Resour 20:33–42

    Article  Google Scholar 

  43. Dang C, de Montaudouin X, Gonzalez P, Mesmer-Dudons N, Caill-Milly N (2008) Brown Muscle Disease (BMD), an emergent pathology affecting Manila clam Ruditapes philippinarum in Arcachon Bay (SW France). Dis Aquat Org 80:219–228

    Article  PubMed  CAS  Google Scholar 

  44. Dang C, de Montaudouin X, Gam M, Paroissin C, Caill-Milly N (2010) The Manila clam population in Arcachon Bay (SW France): can it be kept sustainable? J Sea Res 63:108–118

    Article  Google Scholar 

  45. Meisterhans G, Raymond N, Lebreton S, Salin F, Bourasseau L, de Montaudouin X, Garabetian F, Jude-Lemeilleur F (2011) Dynamics of bacterial bommunities in bockles (Cerastoderma edule) with respect to trematode parasite (Bucephalus minimus) infestation. Microb Ecol 62:620–631

    Article  PubMed  Google Scholar 

  46. SOMLIT, The French coastal monitoring network (Service d’Observation en Milieu LITtoral; INSU/CNRS; http://somlit.epoc.u-bordeaux1.fr

  47. Dang C, Sauriau PG, Savoye N, Caill-Milly N, Martinez P, Millaret C, Haure J, de Montaudouin X (2009) Determination of diet in Manila clams by spatial analysis of stable isotopes. Mar Ecol Prog Ser 387:167–177

    Article  Google Scholar 

  48. Walne PR, Mann R (1975) Growth and biochemical composition Ostrea edulis and Crassostrea gigas. In: H Barnes (ed) Proc. 9th European Marine Biology Symposium. Oban. Aberdeen University Press, Aberdeen, pp. 587–607

  49. Delaporte M, Soudant P, Moal J, Lambert C, Quéré C, Miner P, Choquet G, Paillard C, Samain JF (2003) Effect of a mono-specific algal diet on immune functions in two bivalve species—Crassostrea gigas and Ruditapes philippinarum. J Exp Biol 206:3053–3064

    Article  PubMed  CAS  Google Scholar 

  50. Kennedy P, Kennedy H, Papadimitriou S (2005) The effect of acidification on the determination of organic carbon, total nitrogen and their stable isotopic composition in algae and marine sediment. Rap Com Mass Spectrom 19:1063–1068

    Article  CAS  Google Scholar 

  51. Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322

    PubMed Central  PubMed  CAS  Google Scholar 

  52. Normand P, Ponsonnet C, Nesme X, Neyra M, Simonet P (1996) ITS analysis of prokaryotes. In: Akkermans DL, van Elsas JD, de Bruijn FJ (eds) Molecular microbial ecology manual. Kluwer Academic Publishers, Netherlands, pp 1–12

    Google Scholar 

  53. Osborne CA, Rees GN, Bernstein Y, Janssen PH (2006) New threshold and confidence estimates for terminal restriction fragment length polymorphism analysis of complex bacterial communities. Appl Environ Microbiol 72:1270–8

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  54. Ramette A (2009) Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities. Appl Environ Microbiol 75:2495–2505

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  55. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edition. PRIMER-E: Plymouth

  56. Kropf S, Heuer H, Grüning M, Smalla K (2004) Significance test for comparing complex microbial community fingerprints using pairwise similarity measures. J Microbiol Methods 57:187–195

    Article  PubMed  CAS  Google Scholar 

  57. Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62:142–160

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  58. Siegel S, Castellan NJ (1988) Non parametric statistics for the behavioral sciences, 2nd edn. Mc Graw-Hill, New York

    Google Scholar 

  59. Humphreys J, Caldow RWG, McGrorty S, West A.D, Jensen AC (2007). Population dynamics of naturalised Manila clams Ruditapes philippinarum in British coastal waters. Mar. Biol. 151: 2255–2270. In: Marine Biology. Springer: Berlin. ISSN 0025–3162

  60. Ren Y, Xu B, Guo Y, Yang M, Yang J (2008) Growth, mortality and reproduction of the transplanted Manila clam (Ruditapes philippinarum, Adams & Reeve 1850) in Jiaozhou Bay. Aqua Res 39:1759–1768

    Article  Google Scholar 

  61. Marie B, Trinkler N, Zanella-Cléon I, Guichard N, Becchi M, Paillard C, Marin F (2011) Proteomic identification of novel proteins from the calcifying shell matrix of the Manila clam Venerupis philippinarum. Mar Biotechnol 13:955–962

    Article  PubMed  CAS  Google Scholar 

  62. Dang C, de Montaudouin X (2009) Brown muscle disease and Manila clam Ruditapes philippinarum dynamics in Arcachon Bay. France J Shellfish Res 28:355–362

    Article  Google Scholar 

  63. Dang C, de Montaudouin X, Gonzalez P, Mesmer-Dudons N, Caill-Milly N (2008) Description of a new pathology affecting the adductor muscle of manila clam (Ruditapes philippinarum) in Arcachon Bay (SW France). J Shellfish Res 27:1000–1001

    Google Scholar 

  64. Ray SM (1966) A review of the culture method of detecting Dermocystidium marinum with suggested modifications and precautions. Proc Nat Shell Assoc 54:55–69

    Google Scholar 

  65. Dang C, de Montaudouin X, Caill-Milly N, Trumbiç E (2010) Spatio-temporal patterns of perkinsosis in the Manila clam Ruditapes philippinarum from Arcachon Bay (SW France). Dis Aqua Org 91:151–159

    Article  Google Scholar 

  66. Prieur D, Mevel G, Nicolas J, Plusquellec A, Vigneulle M (1990) Interactions between bivalve molluscs and bacteria in the marine environment. Oceanogra Mar Biol 28:277–352

    Google Scholar 

  67. Meziti A, Ramette A, Mente E, Kormas KA (2010) Temporal shifts of the Norway lobster (Nephrops norvegicus) gut bacterial communities. FEMS Microbiol Ecol 74:472–484

    Article  PubMed  CAS  Google Scholar 

  68. Canesi L, Gallo G, Gavioli M, Pruzzo C (2002) Bacteria-hemocyte interactions and phagocytosis in marine bivalves. Microsc Res Tech 57:469–476

    Article  PubMed  Google Scholar 

  69. Ellis RP, Parry H, Spicer JI, Hutchinson TH, Pipe RK, Widdicombe S (2011) Immunological function in marine invertebrates: responses to environmental perturbation. Fish Shellfish Immunol 30:1209–1222

    Article  PubMed  CAS  Google Scholar 

  70. Romero J, García-Varela M, Laclette JP, Espejo RT (2002) Bacterial 16S rRNA gene analysis revealed that bacteria related to Arcobacter spp. constitute an abundant and common component of the oyster microbiota (Tiostrea chilensis). Microb Ecol 44:365–371

    Article  PubMed  CAS  Google Scholar 

  71. Auby I, Bost CA, Budzinski H, Dalloyau S, Desternes A, Belles A, Trut G, Plus M, Pere C, Couzi L, Feigne C, Steinmetz J (2011) Régression des herbiers de zostères dans le Bassin d’Arcachon: état des lieux et recherche des causes. http://archimer.ifremer.fr/doc/00054/16507/

  72. Le Treut Y (1986) La palourde. Anatomie - Biologie - Elevage - Pêche - Consommation - Inspection sanitaire. Thèse de Doctorat, Ecole Nationale Vétérinaire de Nantes. pp. 161

  73. Harris JM (1993) The presence, nature, and role of gut microflora in aquatic invertebrates: a synthesis. Microb Ecol 25:195–231

    Article  PubMed  CAS  Google Scholar 

  74. Gros O, Gaill F (2007) Extracellular bacterial association in gills of “wood mussels”. Cah Biol Mar 48:103–109

    Google Scholar 

  75. Distel DL, DeLong EF, Waterbury JB (1991) Phylogenetic characterization and in situ localization of the bacterial symbiont of shipworms (Teredinidae: Bivalvia) by using 16S rRNA sequence analysis and oligodeoxynucleotide probe hybridization. Appl Environ Microbiol 57:2376–2382

    PubMed Central  PubMed  CAS  Google Scholar 

  76. Gros O, Darrasse A, Durand P, Frenkiel L, Moueza M (1996) Environmental transmission of a sulfur-oxidizing bacterial gill endosymbiont in the tropical lucinid bivalve Codakia orbicularis. Appl Environ Microbiol 62:2324–2330

    PubMed Central  PubMed  CAS  Google Scholar 

  77. Halary S, Riou V, Gaill F, Boudier T, Duperron S (2008) 3D FISH for the quantification of methane- and sulphur-oxidizing endosymbionts in bacteriocytes of the hydrothermal vent mussel Bathymodiolus azoricus. ISME J 2:284–92. doi:10.1038/ismej.2008.3

    Article  PubMed  CAS  Google Scholar 

  78. De Montaudouin X, Paul-Pont I, Lambert C, Gonzalez P, Raymond N, Jude F, Legeay A, Baudrimont M, Dang C, Le Grand F, Le Goïc N, Bourasseau L, Paillard C (2010) Bivalve population health: multistress to identify hot spots. Mar Pol Bull 60:1307–1318

    Article  Google Scholar 

  79. Paul-Pont I, Gonzalez P, Baudrimont M, Jude F, Raymond N, Bourrasseau L, Le Goïc N, Haynes F, Legeay A, Paillard C, de Montaudouin X (2010) Interactive effects of metal contamination and pathogenic organisms on the marine bivalve Cerastoderma edule. Mar Pol Bull 60:515–525

    Article  CAS  Google Scholar 

  80. Reid HI, Soudant P, Lambert C, Paillard C, Birkbeck TH (2003) Salinity effects on immune parameters of Ruditapes philippinarum challenged with Vibrio tapetis. Dis Aquat Org 56:249–258

    Article  PubMed  CAS  Google Scholar 

  81. Hégaret H, da Silva PM, Wikfors GH, Lambert C, De Bettignies T, Shumway SE, Soudant P (2007) Hemocyte response of Manila clams, Ruditapes philippinarum, with varying parasite, Perkinsus olseni, severity to toxic-algal exposures. Aquat Toxicol 84:469–479

    Article  PubMed  Google Scholar 

  82. Yu JH, Song JH, Choi MC, Park SW (2009) Effects of water temperature change on immune function in surf clams, Mactra veneriformis (Bivalvia: Mactridae). J Invertebrate Pathol 102:30–35

    Article  CAS  Google Scholar 

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Acknowledgments

This project is part of the REPAMEP project funding by LITEAU 3 (nL11-6778), a program of the French Ministry for Environment. The authors thank the shellfish industry CODIMER (Gujan-Mestras, 33-France) for having placed water bath used in the depuration process at our disposal. We thank the crew of R/V Planula IV (INSU) Francis Prince and Laurent Letort for help with clam sampling, and Andrea Niemi (Fisheries and Oceans Canada) for having improved the English.

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Authors and Affiliations

  1. Université de Bordeaux, UMR 5805 EPOC, F-33120, Arcachon, France

    Guillaume Meisterhans, Natalie Raymond, Emilie Girault, Line Bourrasseau, Xavier de Montaudouin, Frédéric Garabetian & Florence Jude-Lemeilleur

  2. CNRS, UMR 5805 EPOC, F-33120, Arcachon, France

    Guillaume Meisterhans, Natalie Raymond, Emilie Girault, Line Bourrasseau, Xavier de Montaudouin, Frédéric Garabetian & Florence Jude-Lemeilleur

  3. Freshwater Institute, Fisheries and Oceans Canada, Winnipeg, MB, R3T 2N6, Canada

    Guillaume Meisterhans

  4. LEMAR UMR 6539, Unité Mixte UBO/CNRS/IFREMER/IRD, IUEM, Place Nicolas Copernic, F-29280, Plouzané, France

    Christophe Lambert

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  1. Guillaume Meisterhans
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Meisterhans, G., Raymond, N., Girault, E. et al. Structure of Manila Clam (Ruditapes philippinarum) Microbiota at the Organ Scale in Contrasting Sets of Individuals. Microb Ecol 71, 194–206 (2016). https://doi.org/10.1007/s00248-015-0662-z

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