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Host Species and Body Site Explain the Variation in the Microbiota Associated to Wild Sympatric Mediterranean Teleost Fishes

  • Host Microbe Interactions
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Abstract

Microorganisms are an important component in shaping the evolution of hosts and as such, the study of bacterial communities with molecular techniques is shedding light on the complexity of symbioses between bacteria and vertebrates. Teleost fish are a heterogeneous group that live in a wide variety of habitats, and thus a good model group to investigate symbiotic interactions and their influence on host biology and ecology. Here we describe the microbiota of thirteen teleostean species sharing the same environment in the Mediterranean Sea and compare bacterial communities among different species and body sites (external mucus, skin, gills, and intestine). Our results show that Proteobacteria is the dominant phylum present in fish and water. However, the prevalence of other bacterial taxa differs between fish and the surrounding water. Significant differences in bacterial diversity are observed among fish species and body sites, with higher diversity found in the external mucus. No effect of sampling time nor species individual was found. The identification of indicator bacterial taxa further supports that each body site harbors its own characteristic bacterial community. These results improve current knowledge and understanding of symbiotic relationships among bacteria and their fish hosts in the wild since the majority of previous studies focused on captive individuals.

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References

  1. Mcfall-Ngai M, Hadfield MG, Bosch TC et al (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. U. S. A. 110:3229–3236

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Ghanbari M, Kneifel W, Domig KJ (2015) A new view of the fish gut microbiome: advances from next-generation sequencing. Aquaculture 448:464–475

    CAS  Google Scholar 

  3. Kohl KD (2018) A microbial perspective on the grand challenges in comparative animal physiology. mSystems 3:e00146-17

    PubMed  PubMed Central  Google Scholar 

  4. Nelson JS, Grande TC, Mark WVH (2016) Fishes of the world5th edn. John Wiley & Sons, New York

    Google Scholar 

  5. Ciric M, Waite D, Draper J, Jones JB (2018) Characterisation of gut microbiota of farmed Chinook salmon using metabarcoding. BioRxiv:288761 https://www.biorxiv.org/content/early/2018/03/26/288761.full.pdf+html

  6. Barko PC, McMichael MA, Swanson KS, Williams DA (2018) The gastrointestinal microbiome: a review. J. Vet. Intern. Med. 32:9–25

    CAS  PubMed  Google Scholar 

  7. Rosado D, Pérez-Losada M, Severino R, Cable J, Xavier R (2018) Characterization of the skin and gill microbiomes of the farmed seabass (Dicentrarchus labrax) and seabream (Sparus aurata). Aquaculture 500:57–64. https://doi.org/10.1016/j.aquaculture.2018.09.063

    Article  CAS  Google Scholar 

  8. Tarnecki AM, Burgos FA, Ray CL, Arias CR (2017) Fish intestinal microbiome: diversity and symbiosis unraveled by metagenomics. J. Appl. Microbiol. https://doi.org/10.1111/jam.13415

  9. Reverter M, Sasal P, Tapissier-Bontemps N, Lecchini D, Suzuki M (2017) Characterisation of the gill mucosal bacterial communities of four butterflyfish species: a reservoir of bacterial diversity in coral reef ecosystems. FEMS Microbiol. Ecol. 93(6). https://doi.org/10.1093/femsec/fix051

  10. Llewellyn MS, Boutin S, Hoseinifar SH, Derome N (2014) Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries. Front. Microbiol. 5:207. https://doi.org/10.3389/fmicb.2014.00207/abstract

    Article  PubMed  PubMed Central  Google Scholar 

  11. Sullam KE, Essinger SD, Lozupone CA, O’Connor MP, Rosen GL, Knight R, Kilham SS, Russell JA (2012) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol. Ecol. 21:3363–3378

    PubMed  Google Scholar 

  12. Eichmiller JJ, Hamilton MJ, Staley C, Sadowsky MJ, Sorensen PW (2016) Environment shapes the fecal microbiome of invasive carp species. Microbiome 4:44

    PubMed  PubMed Central  Google Scholar 

  13. Li X, Ringø E, Hoseinifar SH, Lauzon HL, Birkbeck H, Yang D (2018) The adherence and colonization of microorganisms in fish gastrointestinal tract. Rev Aquacult. https://doi.org/10.1111/raq.12248

  14. Stagaman K, Burns AR, Guillemin K, Bohannan BJM (2017) The role of adaptive immunity as an ecological filter on the gut microbiota in zebrafish. ISME J 11:1630–1639

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Wong S, Rawls JF (2012) Intestinal microbiota composition in fishes is influenced by host ecology and environment. Mol. Ecol. 21:3100–3102

    PubMed  PubMed Central  Google Scholar 

  16. Nayak SK (2010) Role of gastrointestinal microbiota in fish. Aquac. Res. 41:1553–1573

    Google Scholar 

  17. Xing M, Hou Z, Yuan J, Liu Y, Qu Y, Liu B (2013) Taxonomic and functional metagenomic profiling of gastrointestinal tract microbiome of the farmed adult turbot (Scophthalmus maximus). FEMS Microbiol. Ecol. 86:432–443

    CAS  PubMed  Google Scholar 

  18. Li T, Long M, Gatesoupe FJ, Zhang Q, Li A, Gong X (2015) Comparative analysis of the intestinal bacterial communities in different species of carp by pyrosequencing. Microb. Ecol. 69:25–36

    CAS  PubMed  Google Scholar 

  19. Ellis AE (2001) Innate host defense mechanisms of fish against. Dev. Comp. Immunol. 25:827–839

    CAS  PubMed  Google Scholar 

  20. Chen CY, Chen PC, Weng FCH, Shaw GTW, Wang D (2017) Habitat and indigenous gut microbes contribute to the plasticity of gut microbiome in oriental river prawn during rapid environmental change. PLoS One 12:e0181427

    PubMed  PubMed Central  Google Scholar 

  21. Esteban MA (2012) An overview of the immunological defenses in fish skin. ISRN Immunol 853470:1–29. https://doi.org/10.5402/2012/853470

    Article  Google Scholar 

  22. Legrand TPRA, Catalano SR, Wos-Oxley ML, Stephens F, Landos M, Bansemer MS, Stone DAJ, Qin JG, Oxley APA (2018) The inner workings of the outer surface: skin and gill microbiota as indicators of changing gut health in yellowtail kingfish. Front. Microbiol. 8:2664. https://doi.org/10.3389/fmicb.2017.02664

    Article  PubMed  PubMed Central  Google Scholar 

  23. Marshall WS, Bellamy D (2010) The 50 year evolution of in vitro systems to reveal salt transport functions of teleost fish gills. Comp Biochem Physiol A Mol Integr Physiol 155:275–280. https://doi.org/10.1016/j.cbpa.2009.11.016

    Article  CAS  PubMed  Google Scholar 

  24. Peatman E, Lange M, Zhao H, Beck BH (2015) Physiology and immunology of mucosal barriers in catfish (Ictalurus spp.). Tissue barriers 3:e1068907. https://doi.org/10.1080/21688370.2015.1068907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Derome N, Gauthier J, Boutin S, Llewellyn M (2016) Bacterial opportunistic pathogens of fish. In: Hurst CJ (ed) The Rasputin effect: when commensals and symbionts become parasitic. Springer International Publishing, Cham, pp 81–108

    Google Scholar 

  26. Boutin S, Audet C, Derome N (2013) Probiotic treatment by indigenous bacteria decreases mortality without disturbing the natural microbiota of Salvelinus fontinalis. Canadian J Microbiol 59:662–670

    CAS  Google Scholar 

  27. Ye L, Amberg J, Chapman D, Gaikowski M, Liu WT (2014) Fish gut microbiota analysis differentiates physiology and behavior of invasive Asian carp and indigenous American fish. ISME J 8:541–551

    CAS  PubMed  Google Scholar 

  28. Chiarello M, Villéger S, Bouvier C, Bettarel Y, Bouvier T (2015) High diversity of skin-associated bacterial communities of marine fishes is promoted by their high variability among body parts, individuals and species. FEMS Microbiol Ecol 91:fiv061

    PubMed  Google Scholar 

  29. Sullam KE, Rubin BE, Dalton CM, Kilham SS, Flecker AS, Russell JA (2015) Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies. ISME J 9:1508–1522. https://doi.org/10.1038/ismej.2014.1231

    Article  PubMed  PubMed Central  Google Scholar 

  30. McGeoch MA, Chown SL (1998) Scaling up the value of bioindicators. Trend Ecol Evol 13:46–47

    CAS  Google Scholar 

  31. Legendre P, Legendre L (2012) Numerical ecology, 3rdEnglish edn. Elsevier Science BV, Amsterdam

  32. Chiba SN, Iwatsuki Y, Yoshino T, Hanzawa N (2009) Comprehensive phylogeny of the family Sparidae (Perciformes: Teleostei) inferred from mitochondrial gene analyses. Genes Genet Syst 84:153–170

    CAS  PubMed  Google Scholar 

  33. Louisi P (2015) Europe and Mediterranean marine fish identification guide. Eugen Ulmer, Paris

    Google Scholar 

  34. Pallaoro A, Dulcic S, Matic–Skoko M, Kraljevic M, Jardas I (2008) Biology of the salema Sarpa salpa (L. 1758) (Pisces, Sparidae) from the middle eastern Adriatic. J. Appl. Ichthyol. 24:276–281

    Google Scholar 

  35. Savage DC (1977) Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol. 31:107–133

    CAS  PubMed  Google Scholar 

  36. Vaahtovuo J, Toivanen P, Eerola E (2001) Study of murine fecal microflora by cellular fatty acids analysis; effect of age and mouse strain. A Van Leeuw 80:35–42

    CAS  Google Scholar 

  37. Parada AE, Needham DM, Fuhrman JA (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18:1403–1414

    CAS  PubMed  Google Scholar 

  38. Suzuki M, Giovannoni SJ (1996) Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl environ Microbiol 62:625

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    CAS  PubMed  Google Scholar 

  40. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a Chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Env Microbiol 72:5069–5072

    CAS  Google Scholar 

  42. R Core Team (2018) The R project for statistical computing. https://www.r-project.org

  43. Oksanen J, Blanchet FG, Friendly M et al (2018) Vegan: community ecology package. R package version 2:5–2 https://CRAN.R-project.org/package=vegan

    Google Scholar 

  44. Sokal RR, Rohlf FJ (2015) Biometry. The principles and practice of statistics in biological research4th edn. W.H. Freeman and Company, New York

    Google Scholar 

  45. Statsoft Inc (2005) STATISTICA (data analysis software system), version 7.1

  46. McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. Plos one 8:e61217

    CAS  PubMed  PubMed Central  Google Scholar 

  47. De Cáceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574

    PubMed  Google Scholar 

  48. De Cáceres M, Legendre P, Moretti M (2010) Improving indicator species analysis by combining groups of sites. Oikos 119:1674–1684

    Google Scholar 

  49. Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67:345–366

    Google Scholar 

  50. Crespo BG, Pommier T, Fernández-Gómez B, Pedrós-Alio P (2013) Taxonomic composition of the particle-attached and free-living bacterial assemblages in the Northwest Mediterranean Sea analyzed by pyrosequencing of the 16S rRNA. Microbiol Open 2:541–552

    CAS  Google Scholar 

  51. Semova I, Carten JD, Stombaugh J, Mackey LC, Knight R, Farber SA, Rawls JF (2012) Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish. Cell Host Microbe 12:277–288

    CAS  PubMed  Google Scholar 

  52. Navarrete P, Magne F, Araneda C, Fuentes P, Barros L, Opazo R, Espejo R, Romero J (2012) PCR-TTGE analysis of 16S rRNA from rainbow trout (Oncorhynchus mykiss) gut microbiota reveals host-specific communities of active bacteria. PLoS One 7:e31335

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Franchini P, Fruciano C, Frickey T, Jones JC, Meyer A (2014) The gut microbial community of Midas cichlid fish in repeatedly evolved limnetic–benthic species pairs. PLoS One 9:e95027

    PubMed  PubMed Central  Google Scholar 

  54. Larsen AM, Bullard SA, Womble M, Arias CR (2015) Community structure of skin microbiome of gulf killifish, Fundulus grandis, is driven by seasonality and not exposure to oiled sediments in a Louisiana salt marsh. Microb. Ecol. 70:534–544

    CAS  PubMed  Google Scholar 

  55. Schmidt VT, Smith KF, Melvin DW, Amaral-Zettler LA (2015) Community assembly of a euryhaline fish microbiome during salinity acclimation. Mol. Ecol. 24:2537–2550

    PubMed  Google Scholar 

  56. Smith CJ, Danilowicz BS, Meijer WG (2007) Characterization of the bacterial community associated with the surface and mucus layer of whiting (Merlangius merlangus). FEMS Microbiol. Ecol. 62:90–97

    CAS  PubMed  Google Scholar 

  57. Larsen A, Tao Z, Bullard SA, Arias CR (2013) Diversity of the skin microbiota of fishes: evidence for host species specificity. FEMS Microbiol. Ecol. 85:483–494

    CAS  PubMed  Google Scholar 

  58. Qin C, Huang K, Xu H (2002) Isolation and characterization of a novel polysaccharide from the mucus of the loach, Misgurnus anguillicaudatus. Carbohydr. Polym. 49:367–371

    CAS  Google Scholar 

  59. Zhang C, Huang KX (2005) Characteristic immunostimulation by MAP, a polysaccharide isolated from the mucus of the loach, Misgurnus anguillicaudatus. Carbohydr. Polym. 59:75–82

    CAS  Google Scholar 

  60. Lowrey L, Woodhams DC, Tacchi L, Salinas I (2015) Topographical mapping of the rainbow trout (Oncorhynchus mykiss) microbiome reveals a diverse bacterial community with antifungal properties in the skin. Appl Env Microbiol 81:6915–6925

    CAS  Google Scholar 

  61. Gómez GD, Balcázar JL (2018) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol. Med. Microbiol. 52:145–154 http://www.ncbi.nlm.nih.gov/pubmed/18081845

    Google Scholar 

  62. Gallet A, Koubbi P, Léger N, Scheifler M, Ruiz-Rodríguez M, Suzuki MT, Desdevises Y, Duperron S (2019) Low-diversity bacterial microbiota in Southern Ocean representatives of lanternfish genera Electrona, Protomyctophum and Gymnoscopelus (family Myctophidae). PLoS One 14(12):e0226159. https://doi.org/10.1371/journal.pone.0226159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM, Guillemin K, Rawls JF (2011) Evidence for a core gut microbiota in the zebrafish. ISME J 5:1595–1608 http://www.ncbi.nlm.nih.gov/pubmed/21472014

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Tremaroli V, Backhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489:242–249. https://doi.org/10.1038/nature11552

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Fish sampling was performed by the “Service des Moyens à la Mer (FR3724) de l’Observatoire Océanologique de Banyuls/Mer (OOB)”. We are grateful to the BIO2MAR platform (http://bio2mar.obs-banyuls.fr) for providing technical help and support and access to instrumentation.

Funding

This work was funded by Sorbonne Université, programme Emergence 2016 (project SU-16-R-EMR-22-MICROFISH), which included a post-doctoral contract for MRR.

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Authors and Affiliations

  1. Biologie Intégrative des Organismes Marins, BIOM, Sorbonne Université, CNRS, Observatoire Océanologique de Banyuls-sur-Mer. Avenue Pierre Fabre., F-66650, Banyuls/Mer, France

    M. Ruiz-Rodríguez, M. Scheifler, S. Sanchez-Brosseau, E. Magnanou & Y. Desdevises

  2. FR3724, Sorbonne Université, CNRS, Observatoire Océanologique de Banyuls-sur-Mer. Avenue Pierre Fabre., F-66650, Banyuls/Mer, France

    N. West & M. Suzuki

  3. Molécules de Communication et Adaptation des Micro-organismes, MCAM, Muséum National d’Histoire Naturelle, CNRS, 12 rue Buffon, Paris, France

    S. Duperron

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  1. M. Ruiz-Rodríguez
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  2. M. Scheifler
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  3. S. Sanchez-Brosseau
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  4. E. Magnanou
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  5. N. West
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  6. M. Suzuki
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  7. S. Duperron
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  8. Y. Desdevises
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Correspondence to M. Ruiz-Rodríguez.

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Ethical Statement

All applicable international, national, and/or institutional guidelines for the use of animals were followed. The Observatoire Océanologique de Banyuls sur Mer holds the authorization from the “Direction interrégionale de la Mer Méditerrannée” for fishing and handling wild Mediterranean teleosts. Wild fish were caught (see above for details) by competent persons on the research vessel “Nereis II” and in accordance with the European Union Regulations concerning the protection and welfare of experimental animals (European directive 91/492/CCE).

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Ruiz-Rodríguez, M., Scheifler, M., Sanchez-Brosseau, S. et al. Host Species and Body Site Explain the Variation in the Microbiota Associated to Wild Sympatric Mediterranean Teleost Fishes. Microb Ecol 80, 212–222 (2020). https://doi.org/10.1007/s00248-020-01484-y

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