[en] [en] BACKGROUND: Animal-associated microbial communities appear to be key factors in host physiology, ecology, evolution and its interactions with the surrounding environment. Teleost fish have received relatively little attention in the study of surface-associated microbiota. Besides the important role of microbiota in homeostasis and infection prevention, a few recent studies have shown that fish mucus microbiota may interact with and attract some specific parasitic species. However, our understanding of external microbial assemblages, in particular regarding the factors that determine their composition and potential interactions with parasites, is still limited. This is the objective of the present study that focuses on a well-known fish-parasite interaction, involving the Sparidae (Teleostei), and their specific monogenean ectoparasites of the Lamellodiscus genus. We characterized the skin and gill mucus bacterial communities using a 16S rRNA amplicon sequencing, tested how fish ecological traits and host evolutionary history are related to external microbiota, and assessed if some microbial taxa are related to some Lamellodiscus species.
RESULTS: Our results revealed significant differences between skin and gill microbiota in terms of diversity and structure, and that sparids establish and maintain tissue and species-specific bacterial communities despite continuous exposure to water. No phylosymbiosis pattern was detected for either gill or skin microbiota, suggesting that other host-related and environmental factors are a better regulator of host-microbiota interactions. Diversity and structure of external microbiota were explained by host traits: host species, diet and body part. Numerous correlations between the abundance of given bacterial genera and the abundance of given Lamellodiscus species have been found in gill mucus, including species-specific associations. We also found that the external microbiota of the only unparasitized sparid species in this study, Boops boops, harbored significantly more Fusobacteria and three genera, Shewenella, Cetobacterium and Vibrio, compared to the other sparid species, suggesting their potential involvement in preventing monogenean infection.
CONCLUSIONS: This study is the first to explore the diversity and structure of skin and gill microbiota from a wild fish family and present novel evidence on the links between gill microbiota and monogenean species in diversity and abundance, paving the way for further studies on understanding host-microbiota-parasite interactions.
Disciplines :
Microbiology
Author, co-author :
Scheifler, Mathilde ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs ; Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, Sorbonne Université - CNRS, 66650, Banyuls/Mer, France. mathilde.scheifler@gmail.com
Sanchez-Brosseau, Sophie; Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, Sorbonne Université - CNRS, 66650, Banyuls/Mer, France
Magnanou, Elodie; Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, Sorbonne Université - CNRS, 66650, Banyuls/Mer, France
Desdevises, Yves; Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, Sorbonne Université - CNRS, 66650, Banyuls/Mer, France
Language :
English
Title :
Diversity and structure of sparids external microbiota (Teleostei) and its link with monogenean ectoparasites.
Nelson J, Grande T, Mark W. Fishes of the world. 5th ed. Hoboken: Wiley; 2016. DOI: 10.1002/9781119174844
Bush A, Fernández J, Esch G, Seed J. Parasitism: the diversity and ecology of animal parasites. 1st ed. Cambridge: Cambridge University Press; 2001.
Lafferty K, Allesina S, Arim M, Briggs C, De Leo G, Dobson A, et al. Parasites in food webs: the ultimate missing links. Ecol Lett. 2008;11(6):533–46. DOI: 10.1111/j.1461-0248.2008.01174.x
Boutin S, Sauvage C, Bernatchez L, Audet C, Derome N. Inter individual variations of the fish skin microbiota: host genetics basis of mutualism? PLoS ONE. 2014;9(7): e102649. DOI: 10.1371/journal.pone.0102649
Llewellyn M, Boutin S, Hoseinifar S, Derome N. Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries. Front Microbiol. 2014;5:207. DOI: 10.3389/fmicb.2014.00207
Lescak E, Milligan-Myhre K. Teleosts as model organisms to understand host-microbe interactions. J Bacteriol. 2017;199(15):e00868-e916. DOI: 10.1128/JB.00868-16
Kirchman D, Cottrell M, Lovejoy C. The structure of bacterial communities in the western Arctic Ocean as revealed by pyrosequencing of 16S rRNA genes. Environ Microbiol. 2010;12(5):11321143. DOI: 10.1111/j.1462-2920.2010.02154.x
Caron D, Countway P, Jones A, Kim D, Schnetzer A. Marine protistan diversity. Ann Rev Mar Sci. 2012;4:467–93. DOI: 10.1146/annurev-marine-120709-142802
Esteban M. An overview of the immunological defenses in fish skin. ISRN Immunology. 2012;2012:1–29. DOI: 10.5402/2012/853470
McFall-Ngai M, Hadfield M, Bosch T, Carey H, Domazet-Lošo T, Douglas A, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA. 2013;110(9):32293236. DOI: 10.1073/pnas.1218525110
Archie E, Theis K. Animal behaviour meets microbial ecology. Anim Behav. 2011;82(3):425–36. DOI: 10.1016/j.anbehav.2011.05.029
Hellio C, Pons A, Beaupoil C, Bourgougnon N, Gal Y. Antibacterial, antifungal and cytotoxic activities of extracts from fish epidermis and epidermal mucus. Int J Antimicrob Agents. 2002;20(3):214–9. DOI: 10.1016/S0924-8579(02)00172-3
Naik S, Bouladoux N, Wilhelm C, Molloy M, Salcedo R, Kastenmuller W, et al. Compartmentalized control of skin immunity by resident commensals. Science. 2012;337(6098):1115–9. DOI: 10.1126/science.1225152
Boutin S, Bernatchez L, Audet C, Derôme N. Network analysis highlights complex interactions between pathogen, host and commensal microbiota. PLoS ONE. 2013;8(12): e84772. DOI: 10.1371/journal.pone.0084772
Lowrey L, Woodhams D, Tacchi L, Salinas I. Topographical mapping of the rainbow trout (Oncorhynchus mykiss) microbiome reveals a diverse bacterial community with antifungal properties in the skin. Appl Environ Microbiol. 2015;81(19):6915–25. DOI: 10.1128/AEM.01826-15
Kelly C, Salinas I. Under pressure: Interactions between commensal microbiota and the teleost immune system. Front Immunol. 2017;8:559. DOI: 10.3389/fimmu.2017.00559
Lokesh J, Kiron V. Transition from freshwater to seawater reshapes the skin-associated microbiota of Atlantic salmon. Sci Rep. 2016;6:19707. DOI: 10.1038/srep19707
Larsen A, Bullard S, Womble M, Arias C. 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. 2015;70(2):534–44. DOI: 10.1007/s00248-015-0578-7
Bierlich K, Miller C, DeForce E, Friedlaender A, Johnston D, Apprill A. Temporal and regional variability in the skin microbiome of humpback whales along the Western Antarctic Peninsula. Appl Environ Microbiol. 2018;84(5):e02574-e2617. DOI: 10.1128/AEM.02574-17
Ray L, Cai W, Willmon E, Arias C. Fish are not alone: characterization of the gut and skin microbiomes of Largemouth Bass (Micropterus salmoides), Bluegill (Lepomis macrochirus), and Spotted Gar (Lepisosteus oculatus). J Aquac Fish Sci. 2019;2(2):138–54.
Lambert S, Tragin M, Lozano J, Ghiglione J, Vaulot D, Bouget F, et al. Rhythmicity of coastal marine picoeukaryotes, bacteria and archaea despite irregular environmental perturbations. ISME J. 2019;13(2):388–401. DOI: 10.1038/s41396-018-0281-z
Chiarello M, Villéger S, Bouvier C, Bettarel Y, Bouvier T. 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. 2015;91(7):fiv061. DOI: 10.1093/femsec/fiv061
Chiarello M, Auguet J, Bettarel Y, Bouvier C, Claverie T, Graham N, et al. Skin microbiome of coral reef fish is highly variable and driven by host phylogeny and diet. Microbiome. 2018;6(1):147. DOI: 10.1186/s40168-018-0530-4
Reverter M, Sasal P, Tapissier-Bontemps N, Lecchini D, Suzuki M. Characterisation of the gill mucosal bacterial communities of four butterflyfish species: a reservoir of bacterial diversity in coral reef ecosystems. FEMS Microbiol Ecol. 2017;93(6):fix051. DOI: 10.1093/femsec/fix051
Brooks A, Kohl K, Brucker R, van Opstal E, Bordenstein S. Phylosymbiosis: Relationships and Functional Effects of Microbial Communities across Host Evolutionary History. PLoS Biol. 2016;14(11): e2000225. DOI: 10.1371/journal.pbio.2000225
Groussin M, Mazel F, Sanders J, Smillie C, Lavergne S, Thuiller W, et al. Unraveling the processes shaping mammalian gut microbiomes over evolutionary time. Nat Commun. 2017;8:14319. DOI: 10.1038/ncomms14319
Moran N, Sloan D. The hologenome concept: helpful or hollow? PLoS Biol. 2015;13(12): e1002311. DOI: 10.1371/journal.pbio.1002311
Legrand T, Catalano S, Wos-Oxley M, Stephens F, Landos M, Bansemer M, et al. The inner workings of the outer surface: skin and gill microbiota as indicators of changing gut health in Yellowtail Kingfish. Front Microbiol. 2018;8:2664. DOI: 10.3389/fmicb.2017.02664
Rosado D, Pérez-Losada M, Severino R, Cable J, Xavier R. Characterization of the skin and gill microbiomes of the farmed seabass (Dicentrarchus labrax) and seabream (Sparus aurata). Aquaculture. 2019;500:57–64. DOI: 10.1016/j.aquaculture.2018.09.063
Gomez D, Sunyer J, Salinas I. The mucosal immune system of fish: the evolution of tolerating commensals while fighting pathogens. Fish Shellfish Immunol. 2013;35(6):1729–39. DOI: 10.1016/j.fsi.2013.09.032
Rohde K. Marine parasitology. Victoria: Csiro Publishing; 2005. DOI: 10.1071/9780643093072
Sasal P, Trouvé S, Müller-Graf C, Morand S. Specificity and host predictability: a comparative analysis among monogenean parasites of fish. J Anim Ecol. 1999;68(3):437–44. DOI: 10.1046/j.1365-2656.1999.00313.x
Kearn G. Experiments on host-finding and host specificity in the monogenean skin parasite Entobdella soleae. Paraasitology. 1967;57(3):585–605. DOI: 10.1017/S0031182000072450
Buchmann K, Lindenstrøm T. Interactions between monogenean parasites and their fish hosts. Int J Parasitol. 2002;32(3):309–19. DOI: 10.1016/S0020-7519(01)00332-0
Kearn G. The effects of fish mucus on hatching in the monogenean parasite Entobdella soleae from the skin of the common sole, Solea solea. Parasitology. 1974;68(2):173–88. DOI: 10.1017/S0031182000045716
Buchmann K. Immune mechanisms in fish skin against monogeneans - A model. Folia Parasitol. 1999;46(1):1–9.
Yoshinaga T, Nagakura T, Ogawa K, Fukuda Y, Wakabayashi H. Attachment-inducing capacity of fish skin epithelial extracts on oncomiracidia of Benedenia seriolae (Monogenea: Capsalidae). Int J Parasitol. 2002;32(3):381–4. DOI: 10.1016/S0020-7519(01)00339-3
Ohashi H, Umeda N, Hirazawa N, Ozaki Y, Miura C, Miura T. Purification and identification of a glycoprotein that induces the attachment of oncomiracidia of Neobenedenia girellae (Monogenea, Capsalidae). Int J Parasitol. 2007;37(13):1483–90. DOI: 10.1016/j.ijpara.2007.04.024
Wiegertjes G, Gert F. Host–parasite Interactions. 1st ed. London: Taylor & Francis; 2004. DOI: 10.4324/9780203487709
Reverter M, Sasal P, Banaigs B, Lecchini D, Lecellier G, Tapissier-Bontemps N. Fish mucus metabolome reveals fish life-history traits. Coral Reefs. 2017;36(2):463–75. DOI: 10.1007/s00338-017-1554-0
Reverter M, Sasal P, Suzuki M, Raviglione D, Inguimbert N, Pare A, et al. Insights into the natural defenses of a coral reef fish against gill ectoparasites: integrated metabolome and microbiome approach. Metabolites. 2020;10(6):227. DOI: 10.3390/metabo10060227
Llewellyn M, Leadbeater S, Garcia C, Sylvain F, Custodio M, Ang K, et al. Parasitism perturbs the mucosal microbiome of Atlantic Salmon. Sci Rep. 2017;7:43465. DOI: 10.1038/srep43465
Vasemägi A, Visse M, Kisand V. Effect of environmental factors and an emerging parasitic disease on gut microbiome of wild salmonid fish. mSphere. 2017;2(6): e00418-17. DOI: 10.1128/mSphere.00418-17
Afrin T, Murase K, Kounosu A, Hunt V, Bligh M, Maeda Y, et al. Sequential Changes in the Host Gut Microbiota during Infection with the Intestinal Parasitic Nematode Strongyloides venezuelensis. Front Cell Infect Microbiol. 2019;9:217. DOI: 10.3389/fcimb.2019.00217
Hennersdorf P, Kleinertz S, Theisen S, Abdul-Aziz M, Mrotzek G, Palm H, et al. Microbial Diversity and Parasitic Load in Tropical Fish of Different Environmental Conditions. PLoS ONE. 2016;11(3): e0151594. DOI: 10.1371/journal.pone.0151594
Fu P, Xiong F, Feng W, Zou H, Wu S, Li M, et al. Effect of intestinal tapeworms on the gut microbiota of the common carp, Cyprinus carpio. Parasit Vectors. 2019;12(1):252. DOI: 10.1186/s13071-019-3510-z
Gaulke C, Martins M, Watral V, Humphreys I, Spagnoli S, Kent M, et al. A longitudinal assessment of host-microbe-parasite interactions resolves the zebrafish gut microbiome’s link to Pseudocapillaria tomentosa infection and pathology. Microbiome. 2019;7(1):10. DOI: 10.1186/s40168-019-0622-9
Euzet L, Oliver G. Diplectanidae (Monogenea) des Téléostéens de la Méditerranée occidentale. III. Quelques Lamellodiscus Jonhston et Tiegs, 1922, parasites de poissons du genre Diplodus (Sparidae). Ann Parasitol Hum Comp. 1966;41(6):573–98. DOI: 10.1051/parasite/1966416573
Euzet L, Oliver G. Diplectanidae (Monogenea) de Téléostéens de la Méditerranée occidentale. IV. Quelques Lamellodiscus Jonhston et Tiegs, 1922, parasites de poissons du genre Pagellus Cuvier, 1829 (Sparidae). Ann Parasitol Hum Comp. 1967;42(4):407–25. DOI: 10.1051/parasite/1967424407
Oliver G. Recherches sur les Diplectanidae (Monogenea) parasites de Téléostéens du Golfe du Lion. II. Lamellodiscinae nov. sub. fam. Vie Milieu. 1969;10:43–72.
Oliver G. Lamellodiscus obeliae n. sp. une nouvelle espèce de Diplectanidae (Monogenea, Monopisthocotylea) parasite de Pagellus centrodontus (Delaroche, 1809) (Pisces, Sparidae). Z F Parasitenkunde. 1973;41:103–8. DOI: 10.1007/BF00328754
Oliver G. Nouveaux aspects du parasitisme des Diplectanidae Bychowsky, 1957 (Monogenea, Monopisthocotylea) chez les Téléostéens Perciformes des côtes de France. Comptes Rendus de l’Académie des Sciences, Paris. 1974;279(10):803–5.
Oliver G. Les Diplectanidae Bychowsky, 1957 (Monogenea, Monopisthocotylea, Dactylogyridea), Systématique, Biologie, Ontogénie, Écologie, essai de phylogenèse. Thèse d’État: Université des Sciences et Techniques du Languedoc, Montpellier; 1987.
San FD. Microhabitat des Monogènes Dactylogyroidea parasites branchiaux de Téléostéens Mugilidae et Sparidae. Thèse d’Etat: Université des Sciences et Techniques du Languedoc, Montpellier; 1978.
Euzet L. Diplectanidae (Monogenea) parasites de poissons des Iles Kerkennah (Tunisie). Arch Inst Pasteur Tunis. 1984;61:463–74.
Euzet L, Combes C, Caro C. A check list of Monogenea of Mediterranean fish. In: Second international symposium on Monogenea, Montpellier/Sète (France). 1993.
Neifar L. Contribution à l'étude de la biodiversité des monogènes parasites de poissons du secteur nord-est de la Tunisie. Mémoire de Diplôme d'Etudes Approfondies. Université de Tunis. 1995.
Desdevises Y. The phylogenetic position of Furnestinia echeneis (Monogenea, Diplectanidae) based on molecular data: A case of morphological adaptation? Int J Parasitol. 2001;31(2):205–8. DOI: 10.1016/S0020-7519(00)00163-6
Amine F, Euzet L, Kechemir-Issad N. Description de deux nouvelles espèces de Lamellodiscus Johnston & Tiegs, 1922 (Monogenea: Diplectanidae) du groupe morphologique ‘ignoratus’, parasites de Diplodus sargus et D. vulgaris (Teleostei: Sparidae). Syst Parasitol. 2006;64(1):37–45. DOI: 10.1007/s11230-005-9016-4
Amine F, Euzet L, Kechemir-Issad N. Lamellodiscus theroni sp. Nov. (Monogenea, Diplectanidae), a gill parasite from Diplodus puntazzo (Teleostei, Sparidae) from the Mediterranean Sea. Acta Parasitol. 2007;52(4):305–9. DOI: 10.2478/s11686-007-0052-x
Boudaya L, Neifar L, Euzet L. Diplectanid parasites of Lithognathus mormyrus (L.) (Teleostei: Sparidae) from the Mediterranean Sea, with the description of Lamellodiscus flagellatus n. sp. (Monogenea: Diplectanidae). Syst Parasitol. 2009;74(2):149–59. DOI: 10.1007/s11230-009-9213-7
Justine J, Briand M. Three new species, Lamellodiscus tubulicornis n. sp., L. magnicornis n. sp. and L. parvicornis n. sp. (Monogenea: Diplectanidae) from Gymnocranius spp. (Lethrinidae: Monotaxinae) off New Caledonia, with the proposal of the new morphological group “tubulicornis” within Lamellodiscus Johnston & Tiegs, 1922. Syst Parasitol. 2010;75(3):159–79. DOI: 10.1007/s11230-009-9224-4
Chiba S, Iwatsuki Y, Yoshino T, Hanzawa N. Comprehensive phylogeny of the family Sparidae (Perciformes: Teleostei) inferred from mitochondrial gene analyses. Genes Genet Syst. 2009;84(2):153–70. DOI: 10.1266/ggs.84.153
Ruiz-Rodríguez M, Scheifler M, Sanchez-Brosseau S, Magnanou E, West N, Suzuki M, et al. Host species and body site explain the variation in the microbiota associated to wild sympatric mediterranean teleost fishes. Microb Ecol. 2020;80:212–22. DOI: 10.1007/s00248-020-01484-y
Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013;41(1): e1. DOI: 10.1093/nar/gks808
Sinclair L, Osman O, Bertilsson S, Eiler A. Microbial community composition and diversity via 16S rRNA gene amplicons: evaluating the illumina platform. PLoS ONE. 2015;10(2): e0116955. DOI: 10.1371/journal.pone.0116955
Caporaso J, Kuczynski J, Stombaugh J, Bittinger K, Bushman F, Costello E, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6. DOI: 10.1038/nmeth.f.303
Callahan B, McMurdie P, Holmes S. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 2017;11:2639–43. DOI: 10.1038/ismej.2017.119
Hall M, Beiko R. 16S rRNA Gene Analysis with QIIME2. Methods Mol Biol. 2018;1849:113–29. DOI: 10.1007/978-1-4939-8728-3_8
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013;41(Database Issue):D590–6.
Yilmaz P, Parfrey L, Yarza P, Gerken J, Pruesse E, Quast C, et al. The SILVA and “all-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res. 2014;42(Database issue):D643–8. DOI: 10.1093/nar/gkt1209
Mirarab S, Nguyen N, Warnow T. SEPP: SATé-enabled phylogenetic placement. In: Pacific symposium on biocomputing, 2012, pp 247–58.
Janssen S, McDonald D, Gonzalez A, Navas-Molina J, Jiang L, Xu Z, et al. Phylogenetic placement of exact amplicon sequences improves associations with clinical information. mSystems. 2018;3(3): e0002118. DOI: 10.1128/mSystems.00021-18
McMurdie P, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8(4): e61217. DOI: 10.1371/journal.pone.0061217
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett W, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):R60. DOI: 10.1186/gb-2011-12-6-r60
Allegrucci G, Caccone A, Sbordoni V. Cytochrome b sequence divergence in the European sea bass (Dicentrarchus labrax) and phylogenetic relationships among some Perciformes species. J Zoolog Syst Evol Res. 1999;37(3):149–56.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–9. DOI: 10.1093/molbev/msy096
Darriba D, Taboada G, Doallo R, Posada D. jModelTest 2: more models, new heuristics and highperformance computing. Nat Methods. 2012;9(8):772. DOI: 10.1038/nmeth.2109
Nguyen L, Schmidt H, von Haeseler A, Minh B. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–74. DOI: 10.1093/molbev/msu300
Oksanen F, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, et al. Vegan: Community Ecology Package. R package version 2.5-6. 2019. https://CRAN.R-project.org/package=vegan.
Paradis E, Schliep K. Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019;35(3):526–8. DOI: 10.1093/bioinformatics/bty633
Larsen A, Tao Z, Bullard S, Arias C. Diversity of the skin microbiota of fishes: evidence for host species specificity. FEMS Microbiol Ecol. 2013;85(3):483–94. DOI: 10.1111/1574-6941.12136
Llewellyn M, McGinnity P, Dionne M, Letourneau J, Thonier F, Carvalho G, et al. The biogeography of the atlantic salmon (Salmo salar) gut microbiome. ISME J. 2016;10(5):1280–4. DOI: 10.1038/ismej.2015.189
Reinhart E, Korry B, Rowan-Nash A, Belenky P. Defining the distinct skin and gut microbiomes of the Northern Pike (Esox lucius). Front Microbiol. 2019;10:2118. DOI: 10.3389/fmicb.2019.02118
Gallet A, Koubbi P, Léger N, Scheifler M, Ruiz-Rodriguez M, Suzuki M, et al. Low-diversity bacterial microbiota in Southern Ocean representatives of lanternfish genera Electrona, Protomyctophum and Gymnoscopelus (family Myctophidae). PLoS ONE. 2019;12: e0226159. DOI: 10.1371/journal.pone.0226159
Rosado D, Pérez-Losada M, Pereira A, Severino R, Xavier R. Effects of aging on the skin and gill microbiota of farmed seabass and seabream. Anim Microbiome. 2021;3:10. DOI: 10.1186/s42523-020-00072-2
Dodd E, Pierc M, Lee J, Poretsky R. Influences of claywater and greenwater on the skin microbiome of cultured larval sablefish (Anoplopoma fimbria). Anim Microbiome. 2020;2:27. DOI: 10.1186/s42523-020-00045-5
Guivier E, Pech N, Chappaz R, Gilles A. Microbiota associated with the skin, gills, and gut of the fish Parachondrostoma toxostoma from the Rhône basin. Freshw Biol. 2020;65(3):446–59. DOI: 10.1111/fwb.13437
Pratte Z, Besson M, Hollman R, Stewarta F. The gills of reef fish support a distinct microbiome influenced by host-specific factors. Appl Environ Microbiol. 2018;84(9):e00063-e118. DOI: 10.1128/AEM.00063-18
Tort L, Balasch J, Mackenzie S. Fish immune system. A crossroads between innate and adaptive responses. Immunologia. 2003;22(3):277–86.
Ip Y, Chew F. Ammonia production, excretion, toxicity, and defense in fish: a review. Front Physiol. 2010;1(1):134.
Salinas I. The mucosal immune system of teleost fish. Biology. 2015;4(3):525–39. DOI: 10.3390/biology4030525
Cabillon N, Lazado C. Mucosal barrier functions of fish under changing environmental conditions. Fishes. 2019;4(1):2. DOI: 10.3390/fishes4010002
Randall D, Wright P. Ammonia distribution and excretion in fish. Fish Physiol Biochem. 1987;3(3):107–20. DOI: 10.1007/BF02180412
Bordas M, Balebona M, Rodriguez-Maroto J, Borrego J, Moriñigo M. Chemotaxis of pathogenic Vibrio strains towards mucus surfaces of gilt- head sea bream (Sparus aurata L.). Appl Environ Microbiol. 1998;64(4):1573–5. DOI: 10.1128/AEM.64.4.1573-1575.1998
Larsen M, Larsen J, Olsen J. Chemotaxis of Vibrio anguillarum to fish mucus: role of the origin of the fish mucus, the fish species and the serogroup of the pathogen. FEMS Microbiol Ecol. 2001;38(1):77–80. DOI: 10.1111/j.1574-6941.2001.tb00884.x
Ochman H, Worobey M, Kuo C, Ndjango J, Peeters M, Hahn B, et al. Evolutionary Relationships of Wild Hominids Recapitulated by Gut Microbial Communities. PLoS Biol. 2010;8(11): e1000546. DOI: 10.1371/journal.pbio.1000546
Kropáčková L, Těšický M, Albrecht T, Kubovčiak J, Čížková D, Tomášek O, et al. Codiversification of gastrointestinal microbiota and phylogeny in passerines is not explained by ecological divergence. Mol Ecol. 2017;26(19):5292–304. DOI: 10.1111/mec.14144
Ross A, Müller K, Scott Weese J, Neufeld J. Comprehensive skin microbiome analysis reveals the uniqueness of human skin and evidence for phylosymbiosis within the class Mammalia. Proc Natl Acad Sci USA. 2018;115(25):E5786–95. DOI: 10.1073/pnas.1801302115
Hovda M, Lunestad B, Fontanillas R, Rosnes J. Molecular characterisation of the intestinal microbiota of farmed Atlantic salmon (Salmo salar L.). Aquaculture. 2007;272(1–4):581–8. DOI: 10.1016/j.aquaculture.2007.08.045
Zarkasi K, Abell G, Taylor R, Neuman C, Hatje E, Tamplin M, et al. Pyrosequencing-based characterization of gastrointestinal bacteria of Atlantic salmon (Salmo salar L.) within a commercial mariculture system. J Appl Microbiol. 2014;117(1):18–27. DOI: 10.1111/jam.12514
Neuman C, Hatje E, Zarkasi K, Smullen R, Bowman J, Katouli M. The effect of diet and environmental temperature on the faecal microbiota of farmed Tasmanian Atlantic Salmon (Salmo salar L.). Aquac Res. 2016;47(2):660–72. DOI: 10.1111/are.12522
Zhang M, Sun Y, Liu Y, Qiao F, Chen L, Liu W, et al. Response of gut microbiota to salinity change in two euryhaline aquatic animals with reverse salinity preference. Aquaculture. 2016;454:72–80. DOI: 10.1016/j.aquaculture.2015.12.014
Dehler C, Secombes C, Martin S. Environmental and physiological factors shape the gut microbiota of Atlantic salmon parr (Salmo salar L.). Aquaculture. 2017;467:149–57. DOI: 10.1016/j.aquaculture.2016.07.017
Hagi T, Tanaka D, Iwamura Y, Hoshino T. Diversity and seasonal changes in lactic acid bacteria in the intestinal tract of cultured freshwater fish. Aquaculture. 2004;234(1–4):335–46. DOI: 10.1016/j.aquaculture.2004.01.018
Dulski T, Kozłowski K, Ciesielski S. Habitat and seasonality shape the structure of tench (Tinca tinca L.) gut microbiome. Sci Rep. 2020;10(1):4460. DOI: 10.1038/s41598-020-61351-1
Chiarello M, Paz-Vinas I, Veyssière C, Santoul F, Loot G, Ferriol J, et al. Environmental conditions and neutral processes shape the skin microbiome of European catfish (Silurus glanis) populations of Southwestern France. Environ Microbiol Rep. 2019;11(4):605–14. DOI: 10.1111/1758-2229.12774
Minich J, Petrus S, Michael J, Michael T, Knight R, Allen E. Temporal, environmental, and biological drivers of the mucosal microbiome in a wild marine fish, Scomber japonicus. mSphere. 2020;5(3):e00401-e420. DOI: 10.1128/mSphere.00401-20
Schmidt V, Smith K, Melvin D, Amaral-Zettler L. Community assembly of a euryhaline fish microbiome during salinity acclimation. Mol Ecol. 2015;24(10):2537–50. DOI: 10.1111/mec.13177
Sylvain F, Cheaib B, Llewellyn M, Gabriel Correia T, Barros Fagundes D, Luis Val A, et al. pH drop impacts differentially skin and gut microbiota of the Amazonian fish tambaqui (Colossoma macropomum). Sci Rep. 2016;6(1):32032. DOI: 10.1038/srep32032
Alonso-Sáez L, Balagué V, Sà E, Sánchez O, González J, Pinhassi J, et al. Seasonality in bacterial diversity in north-west Mediterranean coastal waters: Assessment through clone libraries, fingerprinting and FISH. FEMS Microbiol Ecol. 2007;60(1):98–112. DOI: 10.1111/j.1574-6941.2006.00276.x
Cram J, Chow C, Sachdeva R, Needham D, Parada A, Steele J, et al. Seasonal and interannual variability of the marine bacterioplankton community throughout the water column over ten years. ISME J. 2015;9(3):563–80. DOI: 10.1038/ismej.2014.153
Escalas A, Auguet JC, Avouac A, Seguin R, Gradel A, Borrossi L, et al. Ecological specialization within a carnivorous fish family is supported by a herbivorous microbiome shaped by a combination of gut traits and specific diet. Front Mar Sci. 2021;8:91. DOI: 10.3389/fmars.2021.622883
Navarrete P, Magne F, Araneda C, Fuentes P, Barros L, Opazo R, et al. PCR-TTGE analysis of 16S rRNA from rainbow trout (Oncorhynchus mykiss) gut microbiota reveals host-specific communities of active bacteria. PLoS ONE. 2012;7(2): e31335. DOI: 10.1371/journal.pone.0031335
Sullam K, Essinger S, Lozupone C, O’Connor M, Rosen G, Knight R, et al. Environmental and ecological factors that shape the gut bacterial communities of fish: A meta-analysis. Mol Ecol. 2012;21(13):3363–78. DOI: 10.1111/j.1365-294X.2012.05552.x
Ringø E, Zhou Z, Vecino J, Wadsworth S, Romero J, Krogdahl A, et al. Effect of dietary components on the gut microbiota of aquatic animals. A never-ending story? Aquac Nutr. 2016;22(2):219–82. DOI: 10.1111/anu.12346
Wang A, Ran C, Ringø E, Zhou Z. Progress in fish gastrointestinal microbiota research. Rev Aquac. 2018;10(3):626–40. DOI: 10.1111/raq.12191
Landeira-Dabarca A, Sieiro C, Álvarez M. Change in food ingestion induces rapid shifts in the diversity of microbiota associated with cutaneous mucus of Atlantic salmon Salmo salar. J Fish Biol. 2013;82(3):893–906. DOI: 10.1111/jfb.12025
Butt R, Volkoff H. Gut Microbiota and Energy Homeostasis in Fish. Front Endocrinol. 2019;24(10):9. DOI: 10.3389/fendo.2019.00009
López Nadal A, Ikeda-Ohtsubo W, Sipkema D, Peggs D, McGurk C, Forlenza M, et al. Feed, microbiota, and gut immunity: using the zebrafish model to understand fish health. Front Immunol. 2020;5(11):114. DOI: 10.3389/fimmu.2020.00114
Shephard K. Functions for fish mucus. Rev Fish Biol Fish. 1994;4:401–29. DOI: 10.1007/BF00042888
Caruso G, Denaro M, Caruso R, Mancari F, Genovese L, Maricchiolo G. Response to short term starvation of growth, haematological, biochemical and non-specific immune parameters in European sea bass (Dicentrarchus labrax) and blackspot sea bream (Pagellus bogaraveo). Mar Environ Res. 2011;72(1–2):46–52. DOI: 10.1016/j.marenvres.2011.04.005
Lindenstrøm T, Secombes C, Buchmann K. Expression of immune response genes in rainbow trout skin induced by Gyrodactylus derjavini infections. Vet Immunol Immunopathol. 2004;97(34):137–48. DOI: 10.1016/j.vetimm.2003.08.016
Easy R, Ross N. Changes in Atlantic salmon (Salmo salar) epidermal mucus protein composition profiles following infection with sea lice (Lepeophtheirus salmonis). Comp Biochem Physiol Part D Genomics Proteomics. 2009;4(3):159–67. DOI: 10.1016/j.cbd.2009.02.001
Grøntvedt R, Espelid S. Immunoglobulin producing cells in the spotted wolffish (Anarhichas minor Olafsen): Localization in adults and during juvenile development. Dev Comp Immunol. 2003;27(6–7):569–78. DOI: 10.1016/S0145-305X(03)00028-4
Pawluk R, Uren Webster T, Cable J, de Leaniz C, Consuegra S. Immune-related transcriptional responses to parasitic infection in a naturally inbred fish: Roles of genotype and individual variation. Genome Biol Evol. 2018;10(1):319–27. DOI: 10.1093/gbe/evx274
Franzenburg S, Walter J, Künzel S, Wang J, Baines J, Bosch T, et al. Distinct antimicrobial peptide expression determines host species-specific bacterial associations. Proc Natl Acad Sci USA. 2013;110(39):E3730–8. DOI: 10.1073/pnas.1304960110
Org E, Parks B, Joo J, Emert B, Schwartzman W, Kang E, et al. Genetic and environmental control of host-gut microbiota interactions. Genome Res. 2015;25(10):1558–69. DOI: 10.1101/gr.194118.115
Chaston J, Dobson A, Newell P, Douglas A. Host genetic control of the microbiota mediates the Drosophila nutritional phenotype. Appl Environ Microbiol. 2016;82(2):671–9. DOI: 10.1128/AEM.03301-15
Bautista-Garfias C, Ixta-Rodriguez O, MartÍnez-Gomez F, Lopez M, Aguilar-Figueroa B. Effect of viable or dead Lactobacillus casei organisms administered orally to mice on resistance against Trichinella spiralis infection. Parasite. 2001;8(2 Suppl):S226–8. DOI: 10.1051/parasite/200108s2226
Hayes K, Bancroft A, Goldrick M, Portsmouth C, Roberts I, Grencis R. Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science. 2010;328(5984):13911394. DOI: 10.1126/science.1187703
Reverter M, Tapissier-Bontemps N, Lecchini D, Banaigs B, Sasal P. Biological and ecological roles of external fish mucus: a review. Fishes. 2018;3(4):41. DOI: 10.3390/fishes3040041
von Engelhardt W, Bartels J, Kirschberger S, Düttingdorf H, Busche R. Role of short-chain fatty acids in the hind gut. Veterinary Q. 1998;20(Suppl 3):S52–9. DOI: 10.1080/01652176.1998.9694970
Andoh A, Bamba T, Sasaki M. Physiological and anti-inflammatory roles of dietary fiber and butyrate in intestinal functions. J Parenter Enter Nutr. 1999;23(5 Suppl):S70–3. DOI: 10.1177/014860719902300518
Hess S, Wenger A, Ainsworth T, Rummer J. Exposure of clownfish larvae to suspended sediment levels found on the Great Barrier Reef: Impacts on gill structure and microbiome. Sci Rep. 2015;5(1):10561. DOI: 10.1038/srep10561
Sugita H, Shibuya K, Shimooka H, Deguchi Y. Antibacterial abilities of intestinal bacteria in freshwater cultured fish. Aquaculture. 1996;145(1–4):195–203. DOI: 10.1016/S0044-8486(96)01319-1
Tsuchiya C, Sakata T, Sugita H. Novel ecological niche of Cetobacterium somerae, an anaerobic bacterium in the intestinal tracts of freshwater fish. Lett Appl Microbiol. 2008;46(1):43–8.
Ito K, Okabe S, Asakawa M, Bessho K, Taniyama S, Shida Y, et al. Detection of tetrodotoxin (TTX) from two copepods infecting the grass puffer Takifugu niphobles: TTX attracting the parasites? Toxicon. 2006;48(6):620–6. DOI: 10.1016/j.toxicon.2006.06.020
Midha A, Janek K, Niewienda A, Henklein P, Guenther S, Serra D, et al. The intestinal roundworm Ascaris suum releases antimicrobial factors which interfere with bacterial growth and biofilm formation. Front Cell Infect Microbiol. 2018;8:271. DOI: 10.3389/fcimb.2018.00271
Maeda Y, Palomares-Rius J, Hino A, Afrin T, Mondal S, Nakatake A, et al. Secretome analysis of Strongyloides venezuelensis parasitic stages reveals that soluble and insoluble proteins are involved in its parasitism. Parasit Vectors. 2019;12(1):21. DOI: 10.1186/s13071-018-3266-x
Cotton S, Donnelly S, Robinson M, Dalton J, Thivierge K. Defense peptides secreted by helminth pathogens: antimicrobial and/or immunomodulator molecules? Front Immunol. 2012;3:269. DOI: 10.3389/fimmu.2012.00269
Cooper D, Eleftherianos I. Parasitic nematode immunomodulatory strategies: recent advances and perspectives. Pathogens. 2016;5(3):58. DOI: 10.3390/pathogens5030058
Hahn M, Dheilly N. Experimental models to study the role of microbes in host–parasite interactions. Front Microbiol. 2016;23(7):1300.
Dheilly N, Martínez Martínez J, Rosario K, Brindley P, Fichorova R, et al. Parasite microbiome project: Grand challenges. PLOS Pathog. 2019;15(10): e1008028. DOI: 10.1371/journal.ppat.1008028
