Debaryomyces hansenii and Rhodotorula mucilaginosa comprised the yeast core gut microbiota of wild and reared carnivorous salmonids, croaker and yellowtail

Environmental Microbiology

Volumn 16, Issue 9, 2014, Pages 2791-2803

  Raggi, Patricia ^a   Lopez, Paulina ^a   Diaz, Angélica ^a   Carrasco, Diana ^a   Silva, Alfonso ^b   Velez, Antonio ^c   Opazo, Rafael ^a   Magne, Fabien ^d,e   Navarrete, Paola A ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSIDAD CATÓLICA DEL NORTE   (Chile)

^c Fundacion Chile   (Chile)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DEBARYOMYCES HANSENII; RHODOTORULA MUCILAGINOSA; SALMONIDAE;

FUNGAL DNA;

ANIMAL; GENETICS; INTESTINE; ISOLATION AND PURIFICATION; MICROBIOLOGY; MICROFLORA; PERCIFORMES; RHODOTORULA; SALMONID; YEAST;

ANIMALS; DNA, FUNGAL; INTESTINES; MICROBIOTA; PERCIFORMES; RHODOTORULA; SALMONIDAE; YEASTS;

EID: 84906944032     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12397     Document Type: Article

References (74)

1. Andlid, T., Juarez, R.V., and Gustafsson, L. (1995) Yeast colonizing the intestine of rainbow-trout (Salmo-Gairdneri) and Turbot (Scophtalmus-Maximus). Microb Ecol 30: 321-334.
2. Andlid, T., Vazquez-Juarez, R., and Gustafsson, L. (1998) Yeasts isolated from the intestine of rainbow trout adhere to and grow in intestinal mucus. Mol Mar Biol Biotechnol 7: 115-126.
3. Aubin, J., Gatesoupe, F.J., Labbe, L., and Lebrun, L. (2005) Trial of probiotics to prevent the vertebral column compression syndrome in rainbow trout (Oncorhynchus mykiss Walbaum). Aquacult Res 36: 758-767.
4. Bass, D., Howe, A., Brown, N., Barton, H., Demidova, M., Michelle, H., etal. (2007) Yeast forms dominate fungal diversity in the deep oceans. Proc R Soc B 274: 3069-3077.
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. Bolumar, T., Sanz, Y., Aristoy, M.C., and Toldra, F. (2008) Purification and characterisation of proteases A and D from Debaryomyces hansenii. Int J Food Microbiol 124: 135-141.
7. Breuer, U., and Harms, H. (2006) Debaryomyces hansenii - an extremophilic yeast with biotechnological potential. Yeast 23: 415-437.
8. Bromuro, C., Torosantucci, A., Gomez, M.J., Urbani, F., and Cassone, A. (1994) Differential release of an immunodominant 65kDa mannoprotein antigen from yeast and mycelial forms of Candida albicans. J Med Vet Mycol 32: 447-459.
9. Bruce, J., and Morris, E.O. (1973) Psychrophilic yeasts isolated from marine fish. Antonie Van Leeuwenhoek 39: 331-339.
10. Buddington, R.K., Krogdahl, A., and Bakke-Mckellep, A.M. (1997) The intestines of carnivorous fish: structure and functions and the relations with diet. Acta Physiol Scand Suppl 638: 67-80.
11. Burgaud, G., Arzur, D., Durand, L., Cambon-Bonavita, M.A., and Barbier, G. (2010) Marine culturable yeasts in deep-sea hydrothermal vents: species richness and association with fauna. FEMS Microbiol Ecol 73: 121-133.
12. Chen, Y.S., Yanagida, F., and Chen, L.Y. (2009) Isolation of marine yeasts from coastal waters of northeastern Taiwan. Aquact Biol 8: 55-60.
13. Chi, Z.M., Chi, Z., Zhang, T., Liu, G.L., Li, J., and Wang, X.H. (2009) Production, characterization and gene cloning of the extracellular enzymes from the marine-derived yeasts and their potential applications. Biotechnol Adv 27: 236-255.
14. Cocolin, L., Bisson, L.F., and Mills, D.A. (2000) Direct profiling of the yeast dynamics in wine fermentations. FEMS Microbiol Lett 189: 81-87.
15. Delbès, C., Ali-Mandjee, L., and Montel, M.C. (2007) Monitoring bacterial communities in raw milk and cheese by culture-dependent and-independent 16S rRNA gene-based analyses. Appl Environ Microbiol 73: 1882-1891.
16. FAO (2012) The State of World Fisheries and Aquaculture. Rome, Italy: Food and Agriculture Organization of the United Nations.
17. Gadanho, M., and Sampaio, J.P. (2005) Occurrence and diversity of yeasts in the Mid-Atlantic ridge hydrothermal fields near the Azores Archipelago. Microb Ecol 50: 408-417.
18. Gao, L.M., Chi, Z.M., Sheng, J., Wang, L., Li, J., and Gong, F. (2007) Inulinase-producing marine yeasts: evaluation of their diversity and inulin hydrolysis by their crude enzymes. Microb Ecol 54: 722-729.
19. Garcia-Gonzalez, A., Lotz, M., and Ochoa, J.L. (2009) Anti-inflammatory activity of superoxide dismutase obtained from Debaryomyces hansenii on type II collagen induced arthritis in rats. Rev Invest Clin 61: 212-220.
20. Gatesoupe, F.J. (2007) Live yeasts in the gut: natural occurrence, dietary introduction, and their effects on fish health and development. Aquaculture 267: 20-30.
21. Guzmán-Villanueva, L., Tovar-Ramírez, D., and Civera-Cerecedo, R. (2007) Effect of wild and ornithine decarboxylase deficient Debaryomyces hansenii, on Paralabrax maculatofasciatus larvae development. In Caribbean and Latin American Aquaculture. Latin American and Caribbean Chapter (ed.). San Juan, Puerto Rico: World Aquaculture Society, p. 53.
22. Hovda, M.B., Lunestad, B.T., Fontanillas, R., and Rosnes, J.T. (2007) Molecular characterisation of the intestinal microbiota of farmed Atlantic salmon (Salmo salar L.). Aquaculture 272: 581-588.
23. Kandasamy, K., Alikunhi, N., and Subramanian, M. (2012) Yeasts in marine and estuarine environments. J Yeast Fungal Res 3: 74-82.
24. Kanther, M., and Rawls, J.F. (2010) Host-microbe interactions in the developing zebrafish. Curr Opin Immunol 22: 10-19.
25. Kibenge, F.S., Godoy, M.G., Wang, Y., Kibenge, M.J., Gherardelli, V., Mansilla, S., etal. (2009) Infectious salmon anaemia virus (ISAV) isolated from the ISA disease outbreaks in Chile diverged from ISAV isolates from Norway around 1996 and was disseminated around 2005, based on surface glycoprotein gene sequences. Virol J 6: 88.
26. Kohlmeyer, J., and Kohlmeyer, E. (1979) Marine Mycology. The Higher Fungi. New York, NY, USA: Academic Press.
27. Kutty, S.N., and Philip, R. (2008) Marine yeasts - a review. Yeast 25: 465-483.
28. Kutty, S.N., Philip, R., and Damodaran, R. (2013) Marine yeasts in the slope sediments of Arabian sea and bay of Bengal. Eur J Exp Biol 3: 311-327.
29. Laconi, S., and Pompei, R. (2007) Study and characterization of intestinal yeasts of mullet (Mugil spp.) for potential probiotic use. J Food Agric Environ 5: 475-480.
30. Lazarus, C., and Koburger, J. (1974) Identification of yeasts from the Suwannee river Florida estuary. Appl Microbiol 27: 1108-1111.
31. Liu, M., Clemons, K.V., Bigos, M., Medovarska, I., Brummer, E., and Stevens, D.A. (2011) Immune responses induced by heat killed Saccharomyces cerevisiae: a vaccine against fungal infection. Vaccine 29: 1745-1753.
32. Maccaferri, S., Klinder, A., Brigidi, P., Cavina, P., and Costabile, A. (2012) Potential probiotic Kluyveromyces marxianus B0399 modulates the immune response in Caco-2 cells and peripheral blood mononuclear cells and impacts the human gut microbiota in an in vitro colonic model system. Appl Environ Microbiol 78: 956-964.
33. Meena, D.K., Das, P., Kumar, S., Mandal, S.C., Prusty, A.K., Singh, S.K., etal. (2013) Beta-glucan: an ideal immunostimulant in aquaculture (a review). Fish Physiol Biochem 39: 431-457.
34. Muyzer, G., Dewaal, E.C., and Uitterlinden, A.G. (1993) Profiling of complex microbial-populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction-amplified genes-coding for 16S ribosomal-RNA. Appl Environ Microbiol 59: 695-700.
35. Nagahama, T., Hamamoto, M., Nakase, T., and Horikoshi, K. (2001) Rhodotorula lamellibrachii sp nov., a new yeast species from a tubeworm collected at the deep-sea floor in Sagami Bay and its phylogenetic analysis. Antonie Van Leeuwenhoek 80: 317-323.
36. Nagahama, T., Hamamoto, M., Nakase, T., and Horikoshi, K. (2003) Rhodotorula benthica sp nov and Rhodotorula calyptogenae sp nov., novel yeast species from animals collected from the deep-sea floor, and Rhodotorula lysiniphila sp nov., which is related phylogenetically. Int J Sys Evol Microbiol 53: 897-903.
37. Nagahama, T., Hamamoto, M., and Horikoshi, K. (2006) Rhodotorula pacifica sp nov., a novel yeast species from sediment collected on the deep-sea floor of the north-west Pacific Ocean. Int J Sys Evol Microbiol 56: 295-299.
38. Navarrete, P., Espejo, R.T., and Romero, J. (2009) Molecular analysis of microbiota along the digestive tract of juvenile Atlantic salmon (Salmo salar L.). Microb Ecol 57: 550-561.
39. Navarrete, P., Magne, F., Araneda, C., Fuentes, P., Barros, L., Opazo, R., etal. (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. doi:10.1371/journal.pone.0031335.
40. Nei, M., and Li, W.H. (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76: 5269-5273.
41. Peu, P., Brugere, H., Pourcher, A., Kerouredan, M., Godon, J., Delgenes, J., and Dabert, P. (2006) Dynamics of a pig slurry microbial community during anaerobic storage and management. Appl Environ Microbiol 72: 3578-3585.
42. Pietrella, D., Lupo, P., Rachini, A., Sandini, S., Ciervo, A., Perito, S., etal. (2008) A Candida albicans mannoprotein deprived of its mannan moiety is efficiently taken up and processed by human dendritic cells and induces T-cell activation without stimulating proinflammatory cytokine production. Infect Immun 76: 4359-4367.
43. 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.
44. 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.
45. Rawls, J.F., Mahowald, M.A., Goodman, A.L., Trent, C.M., and Gordon, J.I. (2007) In vivo imaging and genetic analysis link bacterial motility and symbiosis in the zebrafish gut. Proc Natl Acad Sci USA 104: 7622-7627.
46. Reyes-Becerril, M., Tovar-Ramirez, D., Ascencio-Valle, F., Civera-Cerecedo, R., Gracia-Lopez, V., and Barbosa-Solomieu, V. (2008) Effects of dietary live yeast Debaryomyces hansenii on the immune and antioxidant system in juvenile leopard grouper Mycteroperca rosacea exposed to stress. Aquacult 280: 39-44.
47. Reyes-Becerril, M., Ángeles Esteban, M.A., Tovar-Ramírez, D., and Ascencio-Valle, F. (2011) Polyamine determination in different strains of the yeast Debaryomyces hansenii by high pressure liquid chromatography. Food Chem 127: 1862-1865.
48. Roeselers, G., Mittge, E.K., Stephens, W.Z., Parichy, D.M., Cavanaugh, C.M., Guillemin, K., and Rawls, J.F. (2011) Evidence for a core gut microbiota in the zebrafish. ISME J 5: 1595-1608.
49. 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.
50. Roth, F., Ahean, D., Fell, J.W., Meyers, S., and Meyer, S. (1962) Ecology and taxonomy of yeasts isolated from various marine substrates. Limnol Oceanogr 7: 178-185.
51. Segal-Kischinevzky, C., Rodarte-Murguia, B., Valdes-Lopez, V., Mendoza-Hernandez, G., Gonzalez, A., and Alba-Lois, L. (2011) The euryhaline yeast Debaryomyces hansenii has two catalase genes encoding enzymes with differential activity profile. Curr Microbiol 62: 933-943.
52. Semova, I., Carten, J.D., Stombaugh, J., Mackey, L.C., Knight, R., Farber, S.A., and Rawls, J.F. (2012) Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish. Cell Host Microbe 12: 277-288.
53. Shade, A., and Handelsman, J. (2012) Beyond the Venn diagram: the hunt for a core microbiome. Environ Microbiol 14: 4-12.
54. Sullam, K.E., Essinger, S.D., Lozupone, C.A., O'Connor, M.P., Rosen, G.L., Knight, R., etal. (2012) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol Ecol 21: 3363-3378.
55. Takac, S., and Sengel, B.S. (2010) Extracellular lipolytic enzyme activity of a newly isolated Debaryomyces hansenii. Prep Biochem Biotechnol 40: 28-37.
56. Tap, J., Mondot, S., Levenez, F., Pelletier, E., Caron, C., Furet, J.P., etal. (2009) Towards the human intestinal microbiota phylogenetic core. Environ Microbiol 11: 2574-2584.
57. Torok, V.A., Allison, G.E., Percy, N.J., Ophel-Keller, K., and Hughes, R.J. (2011) Influence of antimicrobial feed additives on broiler commensal posthatch gut microbiota development and performance. Appl Environ Microbiol 77: 3380-3390.
58. Tovar, D., Zambonino, J., Cahu, C., Gatesoupe, F.J., Vazquez-Juarez, R., and Lesel, R. (2002) Effect of live yeast incorporation in compound diet on digestive enzyme activity in sea bass (Dicentrarchus labrax) larvae. Aquaculture 204: 113-123.
59. Tschop, M.H., Hugenholtz, P., and Karp, C.L. (2009) Getting to the core of the gut microbiome. Nat Biotechnol 27: 344-346.
60. Turnbaugh, P.J., and Gordon, J.I. (2009) The core gut microbiome, energy balance and obesity. J Physiol 587: 4153-4158.
61. van Uden, N., and Branco, C. (1963) Distribution and population densities of yeast species in Pacific water, air, animals and kelp off southern California. Limnol Oceanogr 8: 323-329.
62. Vázquez-Juárez, R., Andlid, T., and Gustafsson, L. (1994) Cell surface hydrophobicity and its relation to adhesion of yeasts isolated from fish gut. Colloids Surf B Biointerfaces 2: 199-209.
63. Van de Peer, Y., and De Wachter, R. (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10: 569-570.
64. Vazquez-Juarez, R., Andlid, T., and Gustafsson, L. (1997) Adhesion of yeast isolated from fish gut to crude intestinal mucus of rainbow trout, Salmo gairdneri. Mol Mar Biol Biotechnol 6: 64-71.
65. Viana, P.A., de Rezende, S.T., Marques, V.M., Trevizano, L.M., Passos, F.M.L., Oliveira, M.G.A., etal. (2006) Extracellular alpha-galactosidase from Debaryomyces hansenii UFV-1 and its use in the hydrolysis of raffinose oligosaccharides. J Agric Food Chem 54: 2385-2391.
66. Viana, P.A., de Rezende, S.T., Falkoski, D.L., Leite, T.D., Jose, I.C., Moreira, M.A., and Guimaraes, V.M. (2007) Hydrolysis of oligosaccharides in soybean products by Debaryomyces hansenii UFV-1 alpha-galactosidases. Food Chem 103: 331-337.
67. Viana, P.A., de Rezende, S.T., Passos, F.M.L., Oliveira, J.S., Teixeira, K.N., Santos, A.M.C., etal. (2009) Debaryomyces hansenii UFV-1 intracellular alpha-galactosidase characterization and comparative studies with the extracellular enzyme. J Agric Food Chem 57: 2515-2522.
68. Viana, P.A., de Rezende, S.T., Passos, F.M.L., Machado, S.G., Maitan, G.P., Coelho, V.T.D., and Guimaraes, V.M. (2011a) Alpha-galactosidases production by Debaryomyces hansenii UFV-1. Food Sci Biotechnol 20: 601-606.
69. Viana, P.A., de Rezende, S.T., Alves, A.D., Manfrini, R.M., Alves, R.J., Bemquerer, M.P., etal. (2011b) Activity of Debaryomyces hansenii UFV-1 alpha-galactosidases against alpha-D-galactopyranoside derivatives. Carbohydrate Res 346: 602-605.
70. Wache, Y., Auffray, F., Gatesoupe, F.J., Zambonino, J., Gayet, V., Labbe, L., and Quentel, C. (2006) Cross effects of the strain of dietary Saccharomyces cerevisiae and rearing conditions on the onset of intestinal microbiota and digestive enzymes in rainbow trout, Onchorhynchus mykiss, fry. Aquaculture 258: 470-478.
71. Wong, S., and Rawls, J.F. (2012) Intestinal microbiota composition in fishes is influenced by host ecology and environment. Mol Ecol 21: 3100-3102.
72. Wong, S., Waldrop, T., Summerfelt, S., Davidson, J., Barrows, F., Kenney, P.B., etal. (2013) Aquacultured rainbow trout (Oncorhynchus mykiss) possess a large core intestinal microbiota that is resistant to variation in diet and rearing density. Appl Environ Microbiol 79: 4974-4984.
73. Zaura, E., Keijser, B.J., Huse, S.M., and Crielaard, W. (2009) Defining the healthy 'core microbiome' of oral microbial communities. BMC Microbiol 9: 259.
74. Zoetendal, E., Collier, C., and Koike, S. (2004) Molecular ecological analysis of the gastrointestinal microbiota: a review. J Nutr 134: 465-472.