Low-diversity bacterial microbiota in Southern Ocean representatives of lanternfish genera Electrona, Protomyctophum and Gymnoscopelus (family Myctophidae)

English version

Autoři: Alison Gallet ^aff001; Philippe Koubbi ^aff002; Nelly Léger ^aff004; Mathilde Scheifler ^aff005; Magdalena Ruiz-Rodríguez ^aff005; Marcelino T. Suzuki ^aff006; Yves Desdevises ^aff005; Sébastien Duperron ^aff001
Působiště autorů: Muséum National d’Histoire Naturelle, CNRS, Molécules de Communication et Adaptation des Micro-organismes, MCAM, Muséum national d’Histoire naturelle, Paris, France ^aff001; IFREMER, Channel and North Sea Fisheries Research Unit, Boulogne-sur-Mer, France ^aff002; UFR 918 « Terre, Environnement, Biodiversité », Sorbonne Université, place Jussieu, Paris, France ^aff003; Sorbonne Université, Biologie des Organismes et Ecosystèmes Aquatiques BOREA, Paris, France ^aff004; Sorbonne Université, CNRS, Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, Banyuls/Mer, France ^aff005; Sorbonne Université, CNRS, Laboratoire de Biodiversité et Biotechnologies Microbiennes, LBBM Observatoire Océanologique, Banyuls/Mer, France ^aff006; Institut Universitaire de France, Paris, France ^aff007
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226159

Souhrn

Myctophids are among the most abundant mesopelagic teleost fishes worldwide. They are dominant in the Southern Ocean, an extreme environment where they are important both as consumers of zooplankton as well as food items for larger predators. Various studies have investigated myctophids diet, but no data is yet available regarding their associated microbiota, despite that the significance of bacterial communities to fish health and adaptation is increasingly acknowledged. In order to document microbiota in key fish groups from the Southern Ocean, the bacterial communities associated with the gut, fin, gills and light organs of members of six species within the three myctophid genera Electrona, Protomyctophum and Gymnoscopelus were characterized using a 16S rRNA-based metabarcoding approach. Gut communities display limited diversity of mostly fish-specific lineages likely involved in food processing. Fin and skin communities display diversity levels and compositions resembling more those found in surrounding seawater. Community compositions are similar between genera Electrona and Protomyctophum, that differ from those found in Gymnoscopelus and in water. Low abundances of potentially light-emitting bacteria in light organs support the hypothesis of host production of light. This first description of myctophid-associated microbiota, and among the first on fish from the Southern Ocean, emphasizes the need to extend microbiome research beyond economically-important species, and start addressing ecologically-relevant species.

Klíčová slova:

Bacteria – Fish – Gastrointestinal tract – Gills – Marine fish – Microbiome – Mollicutes – Antarctic Ocean

Zdroje

1. McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Loso T, Douglas AE, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A. 2013;110: 3229–3236. doi: 10.1073/pnas.1218525110 23391737

2. Llewellyn MS, Boutin S, Hoseinifar SH, Derome N. Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries. Front Microbiol. 2014;5. doi: 10.3389/fmicb.2014.00207 24917852

3. Egerton S, Culloty S, Whooley J, Stanton C, Ross RP. The Gut Microbiota of Marine Fish. Front Microbiol. 2018;9. doi: 10.3389/fmicb.2018.00873 29780377

4. Lescak EA, Milligan-Myhre KC. Teleosts as Model Organisms To Understand Host-Microbe Interactions. J Bacteriol. 2017;199. doi: 10.1128/JB.00868-16 28439034

5. Cherel Y, Fontaine C, Richard P, Labat J-P. Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean. Limnol Oceanogr. 2010;55: 324–332. doi: 10.4319/lo.2010.55.1.0324

6. Duhamel G, Hulley PA, Causse R, Koubbi P, Vacchi M, Pruvost P, et al. Biogeographic patterns of fish. Biogeographic atlas of the Southern Ocean. Cambridge, UK: De Broyer C., Koubbi P., Griffith H.J., Raymond B., Udekem d’Acoz C. et al (eds); 2014. pp. 328–362.

7. Saunders RA, Collins MA, Ward P, Stowasser G, Shreeve R, Tarling GA. Distribution, population structure and trophodynamics of Southern Ocean Gymnoscopelus (Myctophidae) in the Scotia Sea. Polar Biol. 2015;38: 287–308. doi: 10.1007/s00300-014-1584-9

8. Pakhomov EA, Perissinotto R, McQuaid CD. Prey composition and daily rations of myctophid fishes in the Southern Ocean. Mar Ecol Prog Ser. 1996;134: 1–14. doi: 10.3354/meps134001

9. Saunders RA, Collins MA, Ward P, Stowasser G, Hill SL, Shreeve R, et al. Predatory impact of the myctophid fish community on zooplankton in the Scotia Sea (Southern Ocean). Mar Ecol Prog Ser. 2015;541: 45–64. doi: 10.3354/meps11527

10. Eastman JT. The nature of the diversity of Antarctic fishes. Polar Biol. 2005;28: 93–107. doi: 10.1007/s00300-004-0667-4

11. Ward NL, Steven B, Penn K, Methe BA, Detrich WH. Characterization of the intestinal microbiota of two Antarctic notothenioid fish species. Extremophiles. 2009;13: 679–685. doi: 10.1007/s00792-009-0252-4 19472032

12. Song W, Li L, Huang H, Jiang K, Zhang F, Chen X, et al. The Gut Microbial Community of Antarctic Fish Detected by 16S rRNA Gene Sequence Analysis. In: BioMed Research International [Internet]. 2016 [cited 21 May 2019]. doi: 10.1155/2016/3241529 27957494

13. Gutowska MA, Drazen JC, Robison BH. Digestive chitinolytic activity in marine fishes of Monterey Bay, California. Comp Biochem Physiol -Mol Integr Physiol. 2004;139: 351–358. doi: 10.1016/j.cbpb.2004.09.020 15556391

14. Widder EA. Bioluminescence in the Ocean: Origins of Biological, Chemical, and Ecological Diversity. Science. 2010;328: 704–708. doi: 10.1126/science.1174269 20448176

15. Deshmukh A. Control of bioluminescence in Myctophid fishes. IJMS Vol4607 July 2017. 2017; Available: http://nopr.niscair.res.in/handle/123456789/42233

16. Collins MA, Stowasser G, Fielding S, Shreeve R, Xavier JC, Venables HJ, et al. Latitudinal and bathymetric patterns in the distribution and abundance of mesopelagic fish in the Scotia Sea. Deep Sea Res Part II Top Stud Oceanogr. 2012;59–60: 189–198. doi: 10.1016/j.dsr2.2011.07.003

17. Hulley PA. Myctophidae. Grahamstown: J.L.B. Smith Institute of Ichthyology.; 1990.

18. Koubbi P, Moteki M, Duhamel G, Goarant A, Hulley P-A, O’Driscoll R, et al. Ecoregionalization of myctophid fish in the Indian sector of the Southern Ocean: Results from generalized dissimilarity models. Deep Sea Res Part II Top Stud Oceanogr. 2011;58: 170–180. doi: 10.1016/j.dsr2.2010.09.007

19. Toullec JY, Koubbi P. VT 155 / REPCCOAI Cruise, RV Marion Dufresne [Internet]. 2017. Available: https://doi.org/10.17600/17017100

20. 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: e1. doi: 10.1093/nar/gks808 22933715

21. Sinclair L, Osman OA, Bertilsson S, Eiler A. Microbial Community Composition and Diversity via 16S rRNA Gene Amplicons: Evaluating the Illumina Platform. PLOS ONE. 2015;10: e0116955. doi: 10.1371/journal.pone.0116955 25647581

22. Hall M, Beiko RG. 16S rRNA Gene Analysis with QIIME2. Methods Mol Biol Clifton NJ. 2018;1849: 113–129. doi: 10.1007/978-1-4939-8728-3_8 30298251

23. Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 2017;11: 2639. doi: 10.1038/ismej.2017.119 28731476

24. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007;35: 7188–7196. doi: 10.1093/nar/gkm864 17947321

25. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol. 2005;71: 8228–8235. doi: 10.1128/AEM.71.12.8228-8235.2005 16332807

26. Faith DP. Conservation evaluation and phylogenetic diversity. Biol Conserv. 1992;61: 1–10. doi: 10.1016/0006-3207(92)91201-3

27. Sedlacek I, Stankova E, Svec P. Composition of cultivable enteric bacteria from the intestine of Antarctic fish (family Nototheniidae). Czech J Anim Sci. 2016;61: 127–132. doi: 10.17221/8785-CJAS

28. Duperron S, Halary S, Habiballah M, Gallet A, Huet H, Duval C, et al. Response of Fish Gut Microbiota to Toxin-Containing Cyanobacterial Extracts: A Microcosm Study on the Medaka (Oryzias latipes). Environ Sci Technol Lett. 2019;6: 341–347. doi: 10.1021/acs.estlett.9b00297

29. Brown RM, Wiens GD, Salinas I. Analysis of the gut and gill microbiome of resistant and susceptible lines of rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 2019;86: 497–506. doi: 10.1016/j.fsi.2018.11.079 30513381

30. Lowrey L, Woodhams DC, 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: 6915–6925. doi: 10.1128/AEM.01826-15 26209676

31. 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 28555138

32. 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

33. 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: fiv061. doi: 10.1093/femsec/fiv061 26048284

34. Holben WE, Williams P, Gilbert MA, Saarinen M, Särkilahti LK, Apajalahti JHA. Phylogenetic analysis of intestinal microflora indicates a novel Mycoplasma phylotype in farmed and wild salmon. Microb Ecol. 2002;44: 175–185. doi: 10.1007/s00248-002-1011-6 12082453

35. Ciric M, Waite D, Draper J, Jones JB. Characterisation of gut microbiota of farmed Chinook salmon using metabarcoding. bioRxiv. 2018; 288761. doi: 10.1101/288761

36. Rimoldi S, Gini E, Iannini F, Gasco L, Terova G. The effect of dietary insect meal from Hermetia illucens prepupae on autochtonous gut microbiota of Rainbow trout (Oncorhynchus mykiss). Animals. 2019;9:143. doi: 10.3390/ani9040143 30987067

37. Dubilier N, Bergin C, Lott C. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol. 2008;6: 725–740. doi: 10.1038/nrmicro1992 18794911

38. Foran D. Evidence of luminous bacterial symbionts in the light organs of myctophid and stomiiform fishes. J Exp Zool. 1991;259: 1–8. doi: 10.1002/jez.1402590102 2072087

39. Haygood M, Edwards D, Mowlds G, Rosenblatt R. Bioluminescence of Myctophid and Stomiiform Fishes Is Not Due to Bacterial Luciferase. J Exp Zool. 1994;270: 225–231. doi: 10.1002/jez.1402700212

Low-diversity bacterial microbiota in Southern Ocean representatives of lanternfish genera Electrona, Protomyctophum and Gymnoscopelus (family Myctophidae)

Souhrn

Klíčová slova:

Zdroje

PLOS One

INSIGHTS from European Respiratory Congress

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií