The culturable intestinal microbiota of triploid and diploid juvenile Atlantic salmon (Salmo salar) - a comparison of composition and drug resistance

BMC Veterinary Research

Volumn 7, Issue , 2011, Pages

  Cantas, Leon ^a,b   Fraser, Thomas W K ^a   Fjelldal, Per Gunnar ^c   Mayer, Ian ^a   Sørum, Henning ^a  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b Norwegian Food Safety Authority   (Norway)

^c INSTITUTE OF MARINE RESEARCH   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS (BACTERIUM); BACTERIA (MICROORGANISMS); CARNOBACTERIUM; PECTOBACTERIUM CAROTOVORUM; PSEUDOMONAS; PSYCHROBACTER; SALMO SALAR; VIBRIO;

ANTIINFECTIVE AGENT;

ANIMAL; ANIMAL FOOD; ANTIBIOTIC RESISTANCE; ARTICLE; ATLANTIC SALMON; BACTERIUM; CLASSIFICATION; DRUG EFFECT; GASTROINTESTINAL TRACT; GENETICS; ISOLATION AND PURIFICATION; METAGENOME; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY;

ANIMAL FEED; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; DRUG RESISTANCE, BACTERIAL; GASTROINTESTINAL TRACT; METAGENOME; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; SALMO SALAR; WATER MICROBIOLOGY;

EID: 81155124441     PISSN: None     EISSN: 17466148     Source Type: Journal    
DOI: 10.1186/1746-6148-7-71     Document Type: Article

References (71)

1. Piferrer F, Beaumont A, Falguiere JC, Flajshans M, Haffray P, Colombo L. Polyploid fish and shellfish: production, biology and applications to aquaculture for performance improvement and genetic containment. Aquaculture 2009, 293:125-156.
2. McGinnity P, Prodohl P, Ferguson K, Hynes R, O'Maoileidigh N, Baker N, Cotter D, O'Hea B, Cooke D, Rogan G, Taggart J, Cross T. Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proceedings of the Royal Society of London Series B-Biological Sciences 2003, 270:2443-2450.
3. Taranger GL, Carillo M, Schulz RW, Fontaine P, Zanuy S, Felip A, Weltzien FA, Dufour S, Karlsen O, Norberg B, Andersson E, Hausen T. Control of pubert in farmed fish. General and Cpmperative Endoctinology 2010, 165:483-515.
4. Powell MD, Jones MA, Lijalad M. Effects of skeletal deformities on swimming performance and recovery from exhaustive exercise in triploid Atlantic salmon. Diseases of Aquatic Organisms 2009, 85:59-66.
5. Benfey TJ. Use of sterile triploid Atlantic salmon (Salmo salar L.) for aquaculture in New Brunswick, Canada. ICES Journal of Marine Science 2001, 58:525-529.
6. Small SA, Benfey TJ. Cell-size in triploid salmon. Journal of Experimental Zoology 1987, 241:339-342.
7. Aliah RS, Yamaoka K, Inada Y, Taniguchi N. Effects of triploidy on tissue structure of some organs in ayu. Nippon Suisan Gakkaishi 1990, 56:569-575.
8. Benfey TJ, Dye HM, Solar II, Donaldson EM. The growth and reproductive endocrinology of adult triploid Pacific salmonids. Fish Physiology and Biochemistry 1989, 6:113-120.
9. Bernier NJ, Brauner CJ, Heath JW, Randall DJ. Oxygen and carbon dioxide transport during sustained exercise in diploid and triploid chinook salmon (Oncorhynchus tshawytscha). Canadian Journal of Fisheries and Aquatic Sciences 2004, 61:1797-1805.
10. Atkins ME, Benfey TJ. Effect of acclimation temperature on routine metabolic rate in triploid salmonids. Comparative Biochemistry and Physiology A-Molecular & Integrative Physiology 2008, 149:157-161.
11. Fjelldal PG, Lock EJ, Hansen T, Wargelius A, El-Mowafi A, Ørnsrud R. Extra dietary phosphorous prevents vertebral deformities in triploid Atlantic salmon (Salmo salar L.) smolts. Oral presentation at the Interdisciplinary Approach in Fish Skeletal Biology Second Meeting, 26-28 April, 2011, Tavira, Portugal
12. Myers JM, Hershberger WK. Early growth and survival of heat-shocked and tetraploid-derived triploid rainbow-trout (Oncorhynchus-mykiss). Aquaculture 1991, 96:97-107.
13. Blanc JM, Chourrout D, Krieg F. Evaluation of juvenile rainbow trout survival and growth in half-sib families from diploid and tetraploid sires. Aquaculture 1987, 65:215-220.
14. Ojolick EJ, Cusack R, Benfey TJ, Kerr SR. Survival and growth of all-female diploid and triploid rainbow-trout (Oncorhynchus-mykiss) reared at chronic high-temperature. Aquaculture 1995, 131:177-187.
15. Ozerov MY, Lumme J, Pakk P, Rintamaki P, Zietara MS, Barskaya Y, Lebedeva D, Saadre E, Gross R, Primmer CR, Vasemagi A. High Gyrodactylus salaris infection rate in triploid Atlantic salmon Salmo salar. Diseases of Aquatic Organisms 2010, 91:129-136.
16. Galbreath PF, Adams ND, Sherrill LW, Martin TH. Thermal tolerance of diploid versus triploid rainbow trout and brook trout assessed by time to chronic lethal maximum. Environmental Biology of Fishes 2006, 75:183-193.
17. Benfey TJ, McCabe LE, Pepin P. Critical thermal maxima of diploid and triploid brook charr, Salvelinus fontinalis. Environmental Biology of Fishes 1997, 49:259-264.
18. Benfey TJ, Biron M. Acute stress response in triploid rainbow trout (Oncorhynchus mykiss) and brook trout (Salvelinus fontinalis). Aquaculture 2000, 184:167-176.
19. Budino B, Cal RM, Piazzon MC, Lamas J. The activity of several components of the innate immune system in diploid and triploid turbot. Comparative Biochemistry and Physiology A-Molecular & Integrative Physiology 2006, 145:108-113.
20. Ringø E, Strøm E, Tabachek JA. Intestinal microflora of salmonids: a review. Aquaculture Research 1995, 26:773-789.
21. Sissons JW. Potential of probiotic organisms to prevent diarrhea and promote digestion in farm-animals - a review. Journal of the Science of Food and Agriculture 1989, 49:1-13.
22. Rawls JF, Samuel BS, Gordon JI. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:4596-4601. 10.1073/pnas.0400706101, 384792, 15070763.
23. Nayak SK. Role of gastrointestinal microbiota in fish. Aquaculture Research 2010, 41:1553-1573.
24. Olsen RE, Sundell K, Mayhew TM, Myklebust R, Ringo E. Acute stress alters intestinal function of rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture 2005, 250:480-495.
25. Sun Y, Yang H, Ling Z, Chang J, Ye J. Gut microbiota of fast and slow growing grouper Epinephelus coioides. African Journal of Microbiology Research 2009, 3:713-720.
26. Egidius E. Vibriosis - Pathogenicity and pathology - a review. Aquaculture 1987, 67:15-28.
27. Bakke-McKellep AM, Penn MH, Salas PM, Refstie S, Sperstad S, Landsverk T, Ringo E, Krogdahl A. Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). British Journal of Nutrition 2007, 97:699-713. 10.1017/S0007114507381397, 17349083.
28. Joborn A, Olsson JC, Westerdahl A, Conway PL, Kjelleberg S. Colonization in the fish intestinal tract and production of inhibitory substances in intestinal mucus and faecal extracts by Carnobacterium sp. strain K1. Journal of Fish Diseases 1997, 20:383-392.
29. Robertson PAW, O'Dowd C, Burrells C, Williams P, Austin B. Use of Carnobacterium sp as a probiotic for Atlantic salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss, Walbaum). Aquaculture 2000, 185:235-243.
30. Merrifield DL, Dimitroglou A, Foey A, Davies SJ, Baker RTM, Bogwald J, Castex M, Ringo E. The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture 2010, 302:1-18.
31. Cabello FC. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environmental Microbiology 2006, 8:1137-1144. 10.1111/j.1462-2920.2006.01054.x, 16817922.
32. Barton MD. Antibiotic use in animal feed and its impact on human health. Nutrition Research Reviews 2000, 13:279-299. 10.1079/095442200108729106, 19087443.
33. Sørum H. Antimicrobial drug resistance in fish pathogens. ASM Pres 2006, 213-237.
34. Kruse H, Sørum H. Transfer of multiple-drug resistance plasmids between bacteria of diverse origins in natural microenvironments. Applied and Environmental Microbiology 1994, 60:4015-4021. 201930, 11865872.
35. Rhodes G, Huys G, Swings J, McGann P, Hiney M, Smith P, Pickup RW. Distribution of oxytetracycline resistance plasmids between aeromonads in hospital and aquaculture environments: Implication of Tn1721 in dissemination of the tetracycline resistance determinant Tet A. Applied and Environmental Microbiology 2000, 66:3883-3890. 10.1128/AEM.66.9.3883-3890.2000, 92234, 10966404.
36. Björklund H, Rabergh CMI, Bylund G. Residues of oxolinic acid and oxytetracycline in fish and sediments from fish farms. Aquaculture 1991, 97:85-96.
37. McPhearson RM, Depaola A, Zywno SR, Motes ML, Guarino AM. Antibiotic-resistance in Gram-negative bacteria from cultured catfish and aquaculture ponds. Aquaculture 1991, 99:203-211.
38. Miranda CD, Zemelman R. Antibiotic resistant bacteria in fish from the Concepcion Bay, Chile. Marine Pollution Bulletin 2001, 42:1096-1102. 10.1016/S0025-326X(01)00093-5, 11763221.
39. Tamminen M, Karkman A, Lohmus A, Muziasari WI, Takasu H, Wada S, Suzuki S, Virta M. Tetracycline resistance genes persist at aquaculture farms in the absence of selection pressure. Environmental Sciene and Technology 2011, 45:386-391.
40. Benfey TJ, Sutterlin AM. Triploidy induced by heat-shock and hydrostatic-pressure in landlocked Atlantic salmon (Salmo-salar L). Aquaculture 1984, 36:359-367.
41. Benfey TJ, Sutterlin AM, Thompson RJ. Use of erythrocyte measurements to identify triploid salmonids. Canadian Journal of Fisheries and Aquatic Sciences 1984, 41:980-984.
42. Hovda MB, Lunestad BT, Fontanillas R, Rosnes JT. Molecular characterisation of the intestinal microbiota of farmed Atlantic salmon (Salmo salar L.). Aquaculture 2007, 272:581-588.
43. Hucker GJ, Conn HJ. Methods of Gram staining. NY State Agr Exp Sta Tech Bull 1923, No. 93.
44. Devereux J, Haeberli P, Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 1984, 12:387-395. 10.1093/nar/12.1Part1.387, 321012, 6546423.
45. Bosshard PP, Zbinden R, Abels S, Böddinghaus B, Altwegg M, Böttger EC. 16S rRNA gene sequencing versus the API 20 NE system and the VITEK 2 ID-GNB card for identification of nonfermenting Gram-negative bacteria in the clinical laboratory. Journal of Clinical Microbiology 2006, 44:1359-1366. 10.1128/JCM.44.4.1359-1366.2006, 1448638, 16597863.
46. Huber I, Spanggaard B, Rossen KF, Nielsen T, Gram L. Phylogenetic analysis and in situ identification of the intestinal microbial community of rainbow trout (Oncorhynchus mykiss, Walbaum). Journal of Applied Microbiology 2004, 96:117-132. 10.1046/j.1365-2672.2003.02109.x, 14678165.
47. Spanggaard B, Huber I, Nielsen J, Nielsen T, Appel KF, Gram L. The microflora of rainbow trout intestine: a comparison of traditional and molecular identification. Aquaculture 2000, 182:1-15.
48. Strøm E. Melkesyrebakterier i fisketarm. Isolasjon, karakterisering og egenskaper. M.Sci Thesis, The Norwegian College of Fishery Science 88 1988,
49. Ringø E. The effect of chromic oxide (Cr2O3) on aerobic bacterial-populations associated with the intestinal epithelial mucosa of Arctic charr, Salvelinus-alpinus (L). Canadian Journal of Microbiology 1993, 39:1169-1173.
50. Malison JA, Procarione LS, Held JA, Kayes TB, Amundson CH. The influence of triploidy and heat and hydrostatic-pressure shocks on the growth and reproductive development of juvenile yellow perch (Perca-flavescens). Aquaculture 1993, 116:121-133.
51. Johnson RM, Shrimpton JM, Heath JW, Heath DD. Family, induction methodology and interaction effects on the performance of diploid and triploid chinook salmon (Oncorhynchus tshawytscha). Aquaculture 2004, 234:123-142.
52. Navarrete P, Espejo RT, Romero J. Molecular analysis of microbiota along the digestive tract of juvenile Atlantic salmon (Salmo salar L.). Microbial Ecology 2009, 57:550-561. 10.1007/s00248-008-9448-x, 18797955.
53. Ringø E, Sperstad S, Kraugerud OF, Krogdahl A. Use of 16S rRNA gene sequencing analysis to characterize culturable intestinal bacteria in Atlantic salmon (Salmo salar) fed diets with cellulose or non-starch polysaccharides from soy. Aquaculture Research 2008, 39:1087-1100.
54. Kim DH, Brunt J, Austin B. Microbial diversity of intestinal contents and mucus in rainbow trout (Oncorhynchus mykiss). J Appl Microbiol 2007, 102:1654-1664. 10.1111/j.1365-2672.2006.03185.x, 17578431.
55. Nikolopoulou D, Moutou KA, Fountoulaki E, Venou B, Adamidou S, Alexis T. Patterns of gastric evacuation, digesta chatacretistics and pH changes along the gastrointestinal tract of gilthead sea bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L.): a comparative study. Comp Biochem Fisiol 2010, 4:406-414.
56. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nature Reviews Immunology 2009, 9:313-323. 10.1038/nri2515, 19343057.
57. Garner SR, Madison BN, Bernier NJ, Neff BD. Juvenile growth and aggression in diploid and triploid chinook salmon Oncorhynchus tshawytscha (Walbaum). Journal of Fish Biology 2008, 73:169-185.
58. Peruzzi S, Varsamos S, Chatain B, Fauvel C, Menu B, Falguiere JC, Severe A, Flik G. Haematological and physiological characteristics of diploid and triploid sea bass, Dicentrarchus labrax L. Aquaculture 2005, 244:359-367.
59. Aaltonen TM, Jokinen EI, Lappivaara J, Markkula SE, Salo HM, Leppanen H, Lammi R. Effects of primary- and secondary-treated bleached kraft mill effluents on the immune system and physiological parameters of roach. Aquatic Toxicology 2000, 51:55-67. 10.1016/S0166-445X(00)00101-6, 10998499.
60. Pickering AD, Pottinger TG. Stress responses and disease resistance in salmonid fish - effects of chronic elevation of plasma-cortisol. Fish Physiology and Biochemistry 1989, 7:253-258.
61. Pickering AD, Pottinger TG, Carragher J, Sumpter JP. The effects of acute and chronic stress on the levels of reproductive hormones in the plasma of mature male brown trout, Salmo-trutta-l. General and Comparative Endocrinology 1987, 68:249-259. 10.1016/0016-6480(87)90036-0, 2828150.
62. Biron M, Benfey TJ. Cortisol, glucose and hematocrit changes during acute stress, cohort sampling, and the diel cycle in diploid and triploid brook trout (Salvelinus-fontinalis Mitchill). Fish Physiology and Biochemistry 1994, 13:153-160.
63. Sadler J, Pankhurst NW, Pankhurst PM, King H. Physiological stress responses to confinement in diploid and triploid Atlantic salmon. Journal of Fish Biology 2000, 56:506-518.
64. Beyea MM, Benfey TJ, Kieffer JD. Hematology and stress physiology of juvenile diploid and triploid shortnose sturgeon (Acipenser brevirostrum). Fish Physiology and Biochemistry 2005, 31:303-313.
65. Leggatt RA, Scheer KW, Afonso LOB, Iwama GK. Triploid and diploid rainbow trout do not differ in their stress response to transportation. North American Journal of Aquaculture 2006, 68:1-8.
66. Moriarty DJW. Control of luminous Vibrio species in penaeid aquaculture ponds. Aquaculture 1998, 164:351-358.
67. Chelossi E, Vezzulli L, Milano A, Branzoni M, Fabiano M, Riccardi G, Banat IM. Antibiotic resistance of benthic bacteria in fish-farm and control sediments of the Western Mediterranean. Aquaculture 2003, 219:83-97.
68. Miranda CD, Zemelman R. Bacterial resistance to oxytetracycline in Chilean salmon farming. Aquaculture 2002, 212:31-47.
69. Schmidt AS, Bruun MS, Dalsgaard I, Pedersen K, Larsen JL. Occurrence of antimicrobial resistance in fish-pathogenic and environmental bacteria associated with four Danish rainbow trout farms. Applied and Environmental Microbiology 2000, 66:4908-4915. 10.1128/AEM.66.11.4908-4915.2000, 92398, 11055942.
70. Hawkey PM, Jones AM. The changing epidemiology of resistance. Journal of Antimicrobial Chemotherapy 2009, 64:3-10.
71. Licht TR, Wilcks A. Conjugative gene transfer in the gastrointestinal environment. Adv Appl Microbiol 2006, 58:77-95.