Selection in the host structures the microbiota associated with developing cod larvae (Gadus morhua)

Environmental Microbiology

Volumn 17, Issue 10, 2015, Pages 3914-3924

  Bakke, Ingrid ^a   Coward, Eivind ^b   Andersen, Tom ^c   Vadstein, Olav ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; RNA 16S;

ACTINOBACTERIA; ANIMAL; ATLANTIC COD; BACTEROIDETES; CLASSIFICATION; DNA SEQUENCE; EMBRYOLOGY; FISH; GASTROINTESTINAL TRACT; GENETICS; INTESTINE FLORA; ISOLATION AND PURIFICATION; LARVA; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; PROTEOBACTERIA;

ACTINOBACTERIA; ANIMALS; BACTEROIDETES; BASE SEQUENCE; DNA, BACTERIAL; FISHES; GADUS MORHUA; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; LARVA; PROTEOBACTERIA; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 85027917273     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12888     Document Type: Article

References (60)

1. Anderson, M.J. (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32–46.
2. Attramadal, K.J.K., Truong, T.M.H., Bakke, I., Skjermo, J., Olsen, Y., and Vadstein, O. (2014) RAS and microbial maturation as tools for K-selection of microbial communities improve survival in cod larvae. Aquaculture 432: 483–490.
3. Austin, B. (2006) The bacterial microflora of fish, revised. Sci World J 6: 931–945.
4. Bakke, I., Skjermo, J., Tu Anh, V., and Vadstein, O. (2013) Live feed is not a major determinant of the microbiota associated with cod larvae (Gadus morhua). Environ Microbiol Rep 5: 537–548.
5. Bates, J.M., Mittge, E., Kuhlman, J., Baden, K.N., Cheesman, S.E., and Guillemin, K. (2006) Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev Biol 297: 374–386.
6. Bjornsdottir, R., Johannsdottir, J., Coe, J., Smaradottir, H., Agustsson, T., Sigurgisladottir, S., and Gudmundsdottir, B.K. (2009) Survival and quality of halibut larvae (Hippoglossus hippoglossus L.) in intensive farming: possible impact of the intestinal bacterial community. Aquaculture 286: 53–63.
7. Bray, J.R., and Curtis, J.T. (1957) An ordination of the upland forest communities of Southern Wisconsin. Ecol Monogr 27: 326–349.
8. Caporaso, J.G., Bittinger, K., Bushman, F.D., DeSantis, T.Z., Andersen, G.L., and Knight, R. (2010a) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26: 266–267.
9. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., et al. (2010b) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335–336.
10. Cheesman, S.E., and Guillemin, K. (2007) We know you are in there: conversing with the indigenous gut microbiota. Res Microbiol 158: 2–9.
11. Collado, L., and Jose Figueras, M. (2011) Taxonomy, epidemiology, and clinical relevance of the genus arcobacter. Clin Microbiol Rev 24: 174.
12. De Schryver, P., and Vadstein, O. (2014) Ecological theory as a foundation to control pathogenic invasion in aquaculture. Isme J 8: 2360–2368.
13. Delcroix, J., Gatesoupe, F.J., Desbruyères, E., Huelvan, C., Delliou, H.L., Le Gall, M.M., et al. (2014) The effects of dietary marine protein hydrolysates on the development of sea bass larvae, Dicentrarchus labrax, and associated microbiota. Aquac Nutr 21: 98–104.
14. DeSantis, T.Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E.L., Keller, K., et al. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72: 5069–5072.
15. Dethlefsen, L., Eckburg, P.B., Bik, E.M., and Relman, D.A. (2006) Assembly of the human intestinal microbiota. Trends Ecol Evol 21: 517–523.
16. Edgar, R.C. (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461.
17. Fraune, S., and Bosch, T.C.G. (2010) Why bacteria matter in animal development and evolution. Bioessays 32: 571–580.
18. Giatsis, C., Sipkema, D., Smidt, H., Verreth, J., and Verdegem, M. (2014) The colonization dynamics of the gut microbiota in Tilapia larvae. PLoS ONE 9: e103641.
19. Gilbert, M.J., Kik, M., Timmerman, A.J., Severs, T.T., Kusters, J.G., Duim, B., and Wagenaar, J.A. (2014) Occurrence, diversity, and host association of intestinal campylobacter, arcobacter, and helicobacter in reptiles. PLoS ONE 9: e101599.
20. Hammer, Ø., Harper, D.A.T., and Ryan, P.D. (2001) PAST: paleontological Statistics software package for education and data analysis. Palaeontol Electron 4: 9.
21. Hansen, G.H., and Olafsen, J.A. (1999) Bacterial interactions in early life stages of marine cold water fish. Microb Ecol 38: 1–26.
22. Ingerslev, H.C., Jorgensen, L.v.G., Strube, M.L., Larsen, N., Dalsgaard, I., Boye, M., and Madsen, L. (2014) The development of the gut microbiota in rainbow trout (Oncorhynchus mykiss) is affected by first feeding and diet type. Aquaculture 424: 24–34.
23. Jensen, S., Ovreas, L., Bergh, Ø., and Torsvik, V. (2004) Phylogenetic analysis of bacterial communities associated with larvae of the Atlantic halibut propose succession from a uniform normal flora. Syst Appl Microbiol 27: 728–736.
24. Jose Figueras, M., Levican, A., Collado, L., Isabel Inza, M., and Yustes, C. (2011) Arcobacter ellisii sp nov., isolated from mussels. Syst Appl Microbiol 34: 414–418.
25. Kanther, M., and Rawls, J.F. (2010) Host–microbe interactions in the developing zebrafish. Curr Opin Immunol 22: 10–19.
26. Kjørsvik, E., Vandermeeren, T., Kryvi, H., Arnfinnson, J., and Kvenseth, P.G. (1991) Early development of the digestive tract of cod larvae, Gadus morhua, during start-feeding and starvation. J Fish Biol 38: 1–15.
27. Kjørsvik, E., Pittman, K., and Pavlov, D. (2004) Chapter 6: from fertilisation to the end of metamorphosis – functional development. In Culture of Cold-Water Marine Fish. Moksness, E., Kjørsvik, E., and Olsen, Y. (eds). Oxford, UK: Blackwell Publishing, pp. 204–278.
28. Koenig, J.E., Spor, A., Scalfone, N., Fricker, A.D., Stombaugh, J., Knight, R., Angenent, L.T., and Ley, R.E. (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA 108: 4578–4585.
29. Korsnes, K., Nicolaisen, O., Skar, C.K., Nerland, A.H., and Bergh, O. (2006) Bacteria in the gut of juvenile cod Gadus morhua fed live feed enriched with four different commercial diets. Ices J Mar Sci 63: 296–301.
30. Ley, R.E., Peterson, D.A., and Gordon, J.I. (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124: 837–848.
31. Li, X., Yu, Y., Feng, W., Yan, Q., and Gong, Y. (2012) Host species as a strong determinant of the intestinal microbiota of fish larvae. J Microbiol 50: 29–37.
32. Llewellyn, M.S., Boutin, S., Hoseinifar, S.H., and Derome, N. (2014) Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries. Front Microbiol 5: 1–17.
33. McIntosh, D., Ji, B., Forward, B.S., Puvanendran, V., Boyce, D., and Ritchie, R. (2008) Culture-independent characterization of the bacterial populations associated with cod (Gadus morhua L.) and live feed at an experimental hatchery facility using denaturing gradient gel electrophoresis. Aquaculture 275: 42–50.
34. Mantel, N. (1967) Detection of disease clustering and a generalized regression approach. Cancer Res 27: 209–220.
35. Nayak, S.K. (2010a) Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29: 2–14.
36. Nayak, S.K. (2010b) Role of gastrointestinal microbiota in fish. Aquac Res 41: 1553–1573.
37. Palmer, C., Bik, E.M., DiGiulio, D.B., Relman, D.A., and Brown, P.O. ((2007) Development of the human infant intestinal microbiota. PLoS Biol 5: 1556–1573.
38. Pantoja-Feliciano, I.G., Clemente, J.C., Costello, E.K., Perez, M.E., Blaser, M.J., Knight, R., and Dominguez-Bello, M.G. (2013) Biphasic assembly of the murine intestinal microbiota during early development. Isme J 7: 1112–1115.
39. Raup, D.M., and Crick, R.E. (1979) Measurement of faunal similarity in paleontology. J Paleontol 53: 1213–1227.
40. Rawls, J.F., Samuel, B.S., and Gordon, J.I. (2004) Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc Natl Acad Sci USA 101: 4596–4601.
41. Rawls, J.F., Mahowald, M.A., Ley, R.E., and Gordon, J.I. (2006) Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 127: 423–433.
42. Reeder, J., and Knight, R. (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7: 668–669.
43. Reitan, K.I., Natvik, C.M., and Vadstein, O. (1998) Drinking rate, uptake of bacteria and microalgae in turbot larvae. J Fish Biol 53: 1145–1154.
44. Robinson, C.J., Bohannan, B.J.M., and Young, V.B. (2010) From structure to function: the ecology of host-associated microbial communities. Microbiol Mol Biol Rev 74: 453.
45. Romero, J., and Navarrete, P. (2006) 16S rDNA-based analysis of dominant bacterial populations associated with early life stages of coho salmon (Oncorhynchus kisutch). Microb Ecol 51: 422–430.
46. Romero, J., Garcia-Varela, M., Laclette, J.P., and Espejo, R.T. (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.
47. Skjermo, J., and Vadstein, O. (1999) Techniques for microbial control in the intensive rearing of marine larvae. Aquaculture 177: 333–343.
48. Star, B., Haverkamp, T.H.A., Jentoft, S., and Jakobsen, K.S. (2013) Next generation sequencing shows high variation of the intestinal microbial species composition in Atlantic cod caught at a single location. BMC Microbiol 13: 248.
49. Sullam, K.E., Essinger, S.D., Lozupone, C.A., O′Connor, M.P., Rosen, G.L., Knight, R., Kilham, S.S., and Russell, J.A. (2012) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol Ecol 21: 3363–3378.
50. Sun, Y.X., Yang, H.L., Ling, Z.C., and Ye, J.D. (2013) Microbial communities associated with early stages of intensively reared orange-spotted grouper (Epinephelus coioides). Aquac Res 46: 131–140. doi:10.1111/are.12167.
51. Tinh, N.T.N., Dierckens, K., Sorgeloos, P., and Bossier, P. (2008) A review of the functionality of probiotics in the larviculture food chain. Mar Biotechnol 10: 1–12.
52. Vadstein, O. (2000) Strategies for avoiding bacterial infections: beat them or join them. ASM News 66: 446–447.
53. Vadstein, O., Oie, G., Olsen, Y., Salvesen, I., Skjermo, J., and Skjakbraek, G. (1993) A strategy to obtain microbial control during larval development of marine fish. In Fish Farm Technology. Reinertsen, R., Dahle, L. A., Jørgensen, L., and Tvinnereim, K. (eds). Rotterdam: A.A. Balkema, pp. 69–75.
54. Vadstein, O., Bergh, O., Gatesoupe, F.-J., Galindo-Villegas, J., Mulero, V., Picchietti, S., et al. (2013) Microbiology and immunology of fish larvae. Rev Aquac 5: S1–S25.
55. Verner-Jeffreys, D.W., Shields, R.J., Bricknell, I.R., and Birkbeck, T.H. (2003) Changes in the gut-associated microflora during the development of Atlantic halibut (Hippoglossus hippoglossus L.) larvae in three British hatcheries. Aquaculture 219: 21–42.
56. Vik, U., Logares, R., Blaalid, R., Halvorsen, R., Carlsen, T., Bakke, I., et al. (2013) Different bacterial communities in ectomycorrhizae and surrounding soil. Sci Rep 3: 3471.
57. Wang, Q., Garrity, G.M., Tiedje, J.M., and Cole, J.R. (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261–5267.
58. Wold, P.A., Hoehne-Reitan, K., Cahu, C.L., Infante, J.Z., Rainuzzo, J., and Kjorsvik, E. (2007) Phospholipids vs. neutral lipids: effects on digestive enzymes in Atlantic cod (Gadus morhua) larvae. Aquaculture 272: 502–513.
59. Wold, P.A., Hoehne-Reitan, K., Rainuzzo, J., and Kjorsvik, E. (2008) Allometric growth and functional development of the gut in developing cod Gadus morhua L. larvae. J Fish Biol 72: 1637–1658.
60. Yan, Q.Y., van der Gast, C.J., and Yu, Y.H. (2012) Bacterial community assembly and turnover within the intestines of developing zebrafish. PLoS ONE 7: e30603.