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Candida utilis yeast as a functional protein source for Atlantic salmon (Salmo salar L.): Local intestinal tissue and plasma proteome responses


Autoři: Felipe Eduardo Reveco-Urzua aff001;  Mette Hofossæter aff002;  Mallikarjuna Rao Kovi aff003;  Liv Torunn Mydland aff001;  Ragnhild Ånestad aff001;  Randi Sørby aff002;  Charles McLean Press aff002;  Leidy Lagos aff001;  Margareth Øverland aff001
Působiště autorů: Department of Animal and Aquaculture Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Aas, Norway aff001;  Department of Basic Sciences and Aquatic Medicine, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, Oslo, Norway aff002;  Department of Plant Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Aas, Norway aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0218360

Souhrn

Microbial ingredients such as Candida utilis yeast are known to be functional protein sources with immunomodulating effects whereas soybean meal causes soybean meal-induced enteritis in the distal intestine of Atlantic salmon (Salmo salar L.). Inflammatory or immunomodulatory stimuli at the local level in the intestine may alter the plasma proteome profile of Atlantic salmon. These deviations can be helpful indicators for fish health and, therefore potential tools in the diagnosis of fish diseases. The present work aimed to identify local intestinal tissue responses and changes in plasma protein profiles of Atlantic salmon fed inactive dry Candida utilis yeast biomass, soybean meal, or combination of soybean meal based diet with various inclusion levels of Candida utilis. A fishmeal based diet was used as control diet. Inclusion of Candida utilis yeast to a fishmeal based diet did not alter the morphology, immune cell population or gene expression of the distal intestine. Lower levels of Candida utilis combined with soybean meal modulated immune cell populations in the distal intestine and reduced the severity of soybean meal-induced enteritis, while higher inclusion levels of Candida utilis were less effective. Changes in the plasma proteomic profile revealed differences between the diets but did not indicate any specific proteins that could be a marker for health or disease. The results suggest that Candida utilis does not alter intestinal morphology or induce major changes in plasma proteome, and thus could be a high-quality alternative protein source with potential functional properties in diets for Atlantic salmon.

Klíčová slova:

Diet – Fish – Gastrointestinal tract – Plasma proteins – Salmon – Soybean – Yeast – Surface-based morphometry


Zdroje

1. Lock ER, Arsiwalla T, Waagbø R. Insect larvae meal as an alternative source of nutrients in the diet of Atlantic salmon (Salmo salar) postsmolt. Aquaculture Nutrition. 2016;22(6):1202–13. doi: 10.1111/anu.12343

2. Sealey WM, Hardy RW, Barrows FT, Pan Q, Stone DAJ. Evaluation of 100% Fish Meal Substitution with Chicken Concentrate, Protein Poultry By-Product Blend, and Chicken and Egg Concentrate on Growth and Disease Resistance of Juvenile Rainbow Trout, Oncorhynchus mykiss. Journal of the World Aquaculture Society. 2011;42(1):46–55. doi: 10.1111/j.1749-7345.2010.00442.x

3. Naylor RL, Hardy RW, Bureau DP, Chiu A, Elliott M, Farrell AP, et al. Feeding aquaculture in an era of finite resources. Proceedings of the National Academy of Sciences. 2009;106(36):15103–10. doi: 10.1073/pnas.0905235106 19805247

4. Øverland M, Karlsson A, Mydland LT, Romarheim OH, Skrede A. Evaluation of Candida utilis, Kluyveromyces marxianus and Saccharomyces cerevisiae yeasts as protein sources in diets for Atlantic salmon (Salmo salar). Aquaculture. 2013;402–403:1–7. doi: 10.1016/j.aquaculture.2013.03.016

5. Ytrestøyl T, Aas TS, Åsgård T. Utilisation of feed resources in production of Atlantic salmon (Salmo salar) in Norway. Aquaculture. 2015;448:365–74. doi: 10.1016/j.aquaculture.2015.06.023

6. Gatlin DM, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, et al. Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquaculture Research. 2007;38(6):551–79. doi: 10.1111/j.1365-2109.2007.01704.x

7. Krogdahl Å, Michael P, Jim T, Ståle R, Marie BA. Important antinutrients in plant feedstuffs for aquaculture: an update on recent findings regarding responses in salmonids. Aquaculture Research. 2010;41(3):333–44. doi: 10.1111/j.1365-2109.2009.02426.x

8. Baeverfjord G, Krogdahl Å. Development and regression of soybean meal induced enteritis in Atlantic salmon, Salmo salar L., distal intestine: a comparison with the intestines of fasted fish. Journal of Fish Diseases. 1996;19(5):375–87. doi: 10.1046/j.1365-2761.1996.d01-92.x

9. van den Ingh TSGAM, Krogdahl Å, Olli JJ, Hendriks HGCJM, Koninkx JGJF. Effects of soybean-containing diets on the proximal and distal intestine in Atlantic salmon (Salmo salar): a morphological study. Aquaculture. 1991;94(4):297–305. doi: 10.1016/0044-8486(91)90174-6

10. Bjørgen H, Koppang EO, Gunnes G, Hordvik I, Moldal T, Kaldhusdal M, et al. Ectopic epithelial cell clusters in salmonid intestine are associated with inflammation. Journal of Fish Diseases. 2018;41(7):1031–40. doi: 10.1111/jfd.12780 29572978

11. Øverland M, Skrede A. Yeast derived from lignocellulosic biomass as a sustainable feed resource for use in aquaculture. Journal of the Science of Food and Agriculture. 2017;97(3):733–42. doi: 10.1002/jsfa.8007 27558451

12. Romarheim OH, Overland M, Mydland LT, Skrede A, Landsverk T. Bacteria grown on natural gas prevent soybean meal-induced enteritis in Atlantic salmon. J Nutr. 2011;141(1):124–30. doi: 10.3945/jn.110.128900 21106922.

13. Grammes F, Reveco FE, Romarheim OH, Landsverk T, Mydland LT, Overland M. Candida utilis and Chlorella vulgaris counteract intestinal inflammation in Atlantic salmon (Salmo salar L.). PLoS One. 2013;8(12):e83213. doi: 10.1371/journal.pone.0083213 24386162.

14. Romarheim OH, Landsverk T, Mydland LT, Skrede A, Øverland M. Cell wall fractions from Methylococcus capsulatus prevent soybean meal-induced enteritis in Atlantic salmon (Salmo salar). Aquaculture. 2013;402–403:13–8. doi: 10.1016/j.aquaculture.2013.03.011

15. Romarheim OH, Hetland DL, Skrede A, Overland M, Mydland LT, Landsverk T. Prevention of soya-induced enteritis in Atlantic salmon (Salmo salar) by bacteria grown on natural gas is dose dependent and related to epithelial MHC II reactivity and CD8alpha+ intraepithelial lymphocytes. Br J Nutr. 2013;109(6):1062–70. doi: 10.1017/S0007114512002899 22813713.

16. Dimitroglou A, Reynolds P, Ravnoy B, Johnsen F. The Effect of Mannan Oligosaccharide Supplementation on Atlantic Salmon Smolts (Salmo salar L.) Fed Diets with High Levels of Plant Proteins. Journal of Aquaculture Research & Development. 2011;s1. doi: 10.4172/2155-9546.S1-011

17. Zhu F, Du B, Xu B. A critical review on production and industrial applications of beta-glucans. Food Hydrocolloids. 2016;52:275–88. doi: 10.1016/j.foodhyd.2015.07.003

18. Viennois E, Zhao Y, Merlin D. Biomarkers of Inflammatory Bowel Disease: From Classical Laboratory Tools to Personalized Medicine. Inflammatory bowel diseases. 2015;21(10):2467–74. doi: 10.1097/MIB.0000000000000444 25985250.

19. Gruys E, Toussaint MJM, Niewold TA, Koopmans SJ. Acute phase reaction and acute phase proteins. Journal of Zhejiang University Science B. 2005;6(11):1045–56. Epub 2005/10/28. 16252337.

20. NRC. Nutrient requirements of fish and shrimp. Animal Nutrition Series. 2011.

21. Boardman T, Warner C, Ramirez-Gomez F, Matrisciano J, Bromage E. Characterization of an anti-rainbow trout (Oncorhynchus mykiss) CD3epsilon monoclonal antibody. Vet Immunol Immunopathol. 2012;145(1–2):511–5. Epub 2011/12/23. doi: 10.1016/j.vetimm.2011.11.017 22188783.

22. Hetland DL, Jorgensen SM, Skjodt K, Dale OB, Falk K, Xu C, et al. In situ localisation of major histocompatibility complex class I and class II and CD8 positive cells in infectious salmon anaemia virus (ISAV)-infected Atlantic salmon. Fish Shellfish Immunol. 2010;28(1):30–9. Epub 2009/09/22. doi: 10.1016/j.fsi.2009.09.011 19766193.

23. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nature Methods. 2012;9:671. doi: 10.1038/nmeth.2089 22930834

24. Kortner TM, Valen EC, Kortner H, Marjara IS, Krogdahl Å, Bakke AM. Candidate reference genes for quantitative real-time PCR (qPCR) assays during development of a diet-related enteropathy in Atlantic salmon (Salmo salar L.) and the potential pitfalls of uncritical use of normalization software tools. Aquaculture. 2011;318(3–4):355–63. doi: 10.1016/j.aquaculture.2011.05.038

25. Pfaffl MW. Quantification strategies in real-time polymerase chain reaction. Quantitative real-time PCR Appl Microbiol. 2012:53–62.

26. Lagos L, Tandberg J, Kashulin-Bekkelund A, Colquhoun DJ, Sørum H, Winther-Larsen HC. Isolation and Characterization of Serum Extracellular Vesicles (EVs) from Atlantic Salmon Infected with Piscirickettsia Salmonis. Proteomes. 2017;5(4):34.

27. Vizcaíno JA, Csordas A, Del-Toro N, Dianes JA, Griss J, Lavidas I, et al. 2016 update of the PRIDE database and its related tools. Nucleic acids research. 2015;44(D1):D447–D56. doi: 10.1093/nar/gkv1145 26527722

28. Chong J, Xia J. MetaboAnalystR: an R package for flexible and reproducible analysis of metabolomics data. Bioinformatics. 2018;34(24):4313–4. doi: 10.1093/bioinformatics/bty528 29955821

29. van den Berg RA, Hoefsloot HC, Westerhuis JA, Smilde AK, van der Werf MJ. Centering, scaling, and transformations: improving the biological information content of metabolomics data. BMC genomics. 2006;7(1):142.

30. Arndt D, Xia J, Liu Y, Zhou Y, Guo AC, Cruz JA, et al. METAGENassist: a comprehensive web server for comparative metagenomics. Nucleic acids research. 2012;40(W1):W88–W95.

31. Øvrum Hansen J, Hofossæter M, Sahlmann C, Ånestad R, Reveco-Urzua FE, Press CM, et al. Effect of Candida utilis on growth and intestinal health of Atlantic salmon (Salmo salar) parr. Aquaculture. 2019;511:734239. https://doi.org/10.1016/j.aquaculture.2019.734239.

32. Bakke-McKellep AM, Frøystad MK, Lilleeng E, Dapra F, Refstie S, Krogdahl Å, et al. Response to soy: T-cell-like reactivity in the intestine of Atlantic salmon, Salmo salar L. Journal of Fish Diseases. 2007;30(1):13–25. doi: 10.1111/j.1365-2761.2007.00769.x 17241401

33. Miadoková E, Svidová S, Vlčková V, Dúhová V, Nad’ová S, Rauko P, et al. Diverse biomodulatory effects of glucomannan from Candida utilis. Toxicology in Vitro. 2006;20(5):649–57. https://doi.org/10.1016/j.tiv.2005.12.001 16413741

34. Venold FF, Penn MH, Krogdahl Å, Overturf KJA. Severity of soybean meal induced distal intestinal inflammation, enterocyte proliferation rate, and fatty acid binding protein (Fabp2) level differ between strains of rainbow trout (Oncorhynchus mykiss). 2012;364:281–92.

35. Gajardo K, Jaramillo-Torres A, Kortner TM, Merrifield DL, Tinsley J, Bakke AM, et al. Alternative protein sources in the diet modulate microbiota and functionality in the distal intestine of Atlantic salmon (Salmo salar). 2017;83(5):e02615–16.

36. Gajardo K, Rodiles A, Kortner TM, Krogdahl Å, Bakke AM, Merrifield DL, et al. A high-resolution map of the gut microbiota in Atlantic salmon (Salmo salar): A basis for comparative gut microbial research. Scientific Reports. 2016;6:30893. doi: 10.1038/srep30893 https://www.nature.com/articles/srep30893#supplementary-information. 27485205

37. Hu H, Kortner TM, Gajardo K, Chikwati E, Tinsley J, Krogdahl Å. Intestinal Fluid Permeability in Atlantic Salmon (Salmo salar L.) Is Affected by Dietary Protein Source. PLOS ONE. 2016;11(12):e0167515. doi: 10.1371/journal.pone.0167515 27907206

38. Medrano-Fernandez I, Bestetti S, Bertolotti M, Bienert GP, Bottino C, Laforenza U, et al. Stress regulates aquaporin-8 permeability to impact cell growth and survival. Antioxidants & redox signaling. 2016;24(18):1031–44.

39. Krogdahl A, Bakke-McKellep AM, Baeverfjord G. Effects of raded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon. Aquaculture Nutrition. 2003.

40. Kortner TM, Penn MH, Bjӧrkhem I, Måsøval K, Krogdahl Å. Bile components and lecithin supplemented to plant based diets do not diminish diet related intestinal inflammation in Atlantic salmon. BMC Veterinary Research. 2016;12(1):190. doi: 10.1186/s12917-016-0819-0 27604133

41. Izuhara K, Arima K, Ohta S, Suzuki S, Inamitsu M, Yamamoto K-i. Periostin in Allergic Inflammation. Allergology International. 2014;63(2):143–51. https://doi.org/10.2332/allergolint.13-RAI-0663.

42. Izuhara K, Nunomura S, Nanri Y, Ono J, Takai M, Kawaguchi A. Periostin: An emerging biomarker for allergic diseases. Allergy. 2019;0(0). Epub 2019/04/10. doi: 10.1111/all.13814

43. Shimoyama Y, Tamai K, Shibuya R, Nakamura M, Mochizuki M, Yamaguchi K, et al. Periostin attenuates tumor growth by inducing apoptosis in colitis-related colorectal cancer. Oncotarget. 2018;9(28):20008–17. doi: 10.18632/oncotarget.25026 29731999.

44. Bao S, Ouyang G, Bai X, Huang Z, Ma C, Liu M, et al. Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell. 2004;5(4):329–39. https://doi.org/10.1016/S1535-6108(04)00081-9 15093540

45. Devani M, Cugno M, Vecchi M, Ferrero S, Di Berardino F, Avesani EC, et al. Kallikrein-kinin system activation in Crohn’s disease: differences in intestinal and systemic markers. The American journal of gastroenterology. 2002;97(8):2026–32. Epub 2002/08/23. 12190172.

46. Devani M, Vecchi M, Ferrero S, Avesani EC, Arizzi C, Chao L, et al. Kallikrein–kinin system in inflammatory bowel diseases: Intestinal involvement and correlation with the degree of tissue inflammation. Digestive and Liver Disease. 2005;37(9):665–73. https://doi.org/10.1016/j.dld.2005.01.021 15949977

47. Moschen AR, Adolph TE, Gerner RR, Wieser V, Tilg H. Lipocalin-2: A Master Mediator of Intestinal and Metabolic Inflammation. Trends in Endocrinology & Metabolism. 2017;28(5):388–97. doi: 10.1016/j.tem.2017.01.003 28214071

48. Stallhofer J, Friedrich M, Konrad-Zerna A, Wetzke M, Lohse P, Glas J, et al. Lipocalin-2 Is a Disease Activity Marker in Inflammatory Bowel Disease Regulated by IL-17A, IL-22, and TNF-alpha and Modulated by IL23R Genotype Status. Inflamm Bowel Dis. 2015;21(10):2327–40. Epub 2015/08/12. doi: 10.1097/MIB.0000000000000515 26263469.

49. Yousaf MN, Powell MD. The effects of heart and skeletal muscle inflammation and cardiomyopathy syndrome on creatine kinase and lactate dehydrogenase levels in Atlantic salmon (Salmo salar L.). TheScientificWorldJournal. 2012;2012:741302. Epub 2012/06/16. doi: 10.1100/2012/741302 22701371.

50. DiScipio R, Chakravarti D, Muller-Eberhard H, Fey GJJoBC. The structure of human complement component C7 and the C5b-7 complex. 1988;263(1):549–60.

51. Kishore U, Reid KBM. C1q: Structure, function, and receptors. Immunopharmacology. 2000;49(1):159–70. https://doi.org/10.1016/S0162-3109(00)80301-X.

52. Ringø E, Erik Olsen R, Gonzalez Vecino JL, Wadsworth S. Use of Immunostimulants and Nucleotides in Aquaculture: A Review. Journal of Marine Science: Research & Development. 2011;02(01). doi: 10.4172/2155-9910.1000104

53. Dalmo RA, Bøgwald J. ß-glucans as conductors of immune symphonies. Fish & Shellfish Immunology. 2008;25(4):384–96. https://doi.org/10.1016/j.fsi.2008.04.008.

54. Bagni M, Archetti L, Amadori M, Marino GJJoVM, Series B. Effect of long‐term oral administration of an immunostimulant diet on innate immunity in sea bass (Dicentrarchus labrax). 2000;47(10):745–51.

55. Bagni M, Romano N, Finoia M, Abelli L, Scapigliati G, Tiscar PG, et al. Short-and long-term effects of a dietary yeast β-glucan (Macrogard) and alginic acid (Ergosan) preparation on immune response in sea bass (Dicentrarchus labrax). 2005;18(4):311–25.

56. Verlhac V, Obach A, Gabaudan J, SCHÜEP W, Hole RJF, Immunology S. Immunomodulation by dietary vitamin C and glucan in rainbow trout (Oncorhynchus mykiss). 1998;8(6):409–24.

57. Yuan X-Y, Liu W-B, Liang C, Sun C-X, Xue Y-F, Wan Z-D, et al. Effects of partial replacement of fish meal by yeast hydrolysate on complement system and stress resistance in juvenile Jian carp (Cyprinus carpio var. Jian). Fish & Shellfish Immunology. 2017;67:312–21. https://doi.org/10.1016/j.fsi.2017.06.028.

58. Engstad RE, Robertsen B, Frivold E. Yeast glucan induces increase in lysozyme and complement-mediated haemolytic activity in Atlantic salmon blood. Fish & Shellfish Immunology. 1992;2(4):287–97. doi: 10.1016/S1050-4648(06)80033-1

59. Padmini E. Physiological adaptations of stressed fish to polluted environments: role of heat shock proteins. Reviews of environmental contamination and toxicology. 2010;206:1–27. Epub 2010/07/24. doi: 10.1007/978-1-4419-6260-7_1 20652666.


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