Skip to main content
SpringerLink
Log in

Effects of Red Yeast (Sporidiobolus pararoseus) on Growth, Innate Immunity, Expression of Immune-related Genes and Disease Resistance of Nile Tilapia (Oreochromis niloticus)

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

The purpose of this study was to evaluate the effects of red yeast (Sporidiobolus pararoseus) produced from crude glycerol, as a by-product of the biodiesel production process, on the growth, innate immunity, expression of immune-related gene, and resistance of Nile tilapia against challenge with Streptococcus agalactiae. Fish were fed diets supplied with different concentrations of S. pararoseus dried cells at 0.0 (control; T1), 5.0 (T2), 10.0 (T3), and 20.0 (T4) g kg−1 diets for 90 days. The results showed that final body weight, weight gain, and average daily gain were significantly higher in fish fed T3 and T4 compared to the control group (p < 0.05). Likewise, significant (p < 0.05) increases in total carotenoid content, liver superoxide dismutase activity (SOD), and serum lysozyme and albumin were observed in Nile tilapia fed S. pararoseus, with the highest (p < 0.05) values displayed in fish fed the T4 diet. Moreover, up-regulation of IL-1β transcription in Nile tilapia spleen and liver was observed in fish feeding group T4. In a challenge test against S. agalactiae, the fish survival rate was significantly higher in fish fed red yeast compared to the control group (p < 0.05). The highest bactericidal activity found in the T4 group (p < 0.05). However, no significant differences were found in hematology, blood chemical, malondialdehyde (MDA), body chemical composition, organosomatic indices, and myeloperoxidase (p > 0.05) in all treatments. The present results suggested that red yeast S. pararoseus (20.0 g kg−1) can be used as a potential supplementation on growth, immune response, and disease resistance of Nile tilapia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

The authors confirm that the data of this study are available within the article.

References

  1. Lv HB, Ma Yy HuCT, Lin QY, Jjy Y, Chen LQ, Zhang ML, Du ZY, Qiao F (2021) The individual and combined effects of hypoxia and high-fat diet feeding on nutrient composition and flesh quality in Nile tilapia (Oreochromis niloticus). Food Chem 343:128479. https://doi.org/10.1016/j.foodchem.2020.128479

    Article  CAS  PubMed  Google Scholar 

  2. Abu-Elala NM, Ali TES, Ragaa NM, Ali SE, Abd-Elsalam RM, Younis NA, Abdel-Moneam DA, Hamdien AH, Bonato M, Dawood MA (2021) Analysis of the productivity, immunity, and health performance of Nile tilapia (Oreochromis niloticus) broodstock-fed dietary fermented extracts sourced from Saccharomyces cerevisiae (Hilyses): a field trial. Animals 11(3):815. https://doi.org/10.3390/ani11030815

    Article  PubMed  PubMed Central  Google Scholar 

  3. FAO (2020) The State of World Fisheries and Aquaculture 2020. Sustainability in action. Rome. https://doi.org/10.4060/ca9229en

  4. Herrera M, Mancera JM, Costas B (2019) The use of dietary additives in fish stress mitigation: comparative endocrine and physiological responses. Front Endocrinol 10:447. https://doi.org/10.3389/fendo.2019.00447

    Article  Google Scholar 

  5. Delannoy CMJ, Samai H, Labrie L (2021) Streptococcus agalactiae serotype IV in farmed tilapia. Aquaculture 544(6):737033. https://doi.org/10.1016/j.aquaculture.2021.737033

    Article  Google Scholar 

  6. Fernández Sánchez JL, Le Breton A, Brun E, Vendramin N, Spiliopoulos G, Furones D, Basurco B (2022) Assessing the economic impact of diseases in Mediterranean grow-out farms culturing European sea bass. Aquaculture 547:737530. https://doi.org/10.1016/j.aquaculture.2021.737530

    Article  Google Scholar 

  7. Mohd Yazid SH, Mohd Daud H, Azmai MNA, Mohamad N, Mohd Nor N (2021) Estimating the economic loss due to vibriosis in net-cage cultured Asian seabass (Lates calcarifer): evidence from the East coast of Peninsular Malaysia. Front Vet Sci 8:644009. https://doi.org/10.3389/fvets.2021.644009

    Article  PubMed  PubMed Central  Google Scholar 

  8. Chen J, Yang Y, Jiang X, Ke Y, He T, Xie S (2022) Metagenomic insights into the profile of antibiotic resistomes in sediments of aquaculture wastewater treatment system. Res J Environ Sci 113:345–355. https://doi.org/10.1016/j.jes.2021.06.026

    Article  Google Scholar 

  9. Shao Y, Wang Y, Yuan Y, Xie Y (2021) A systematic review on antibiotics misuse in livestock and aquaculture and regulation implications in China. Sci Total Environ 798:149205. https://doi.org/10.1016/j.scitotenv.2021.149205

    Article  CAS  PubMed  Google Scholar 

  10. Pepi M, Focardi S (2021) Antibiotic-resistant bacteria in aquaculture and climate change: a challenge for health in the mediterranean area. Int J Environ Res Public Health 18(11):5723. https://doi.org/10.3390/ijerph18115723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Hoseini SM, Yousefi M (2018) Beneficial effects of thyme (Thymus vulgaris) extract on oxytetracycline-induced stress response, immunosuppression, oxidative stress and enzymatic changes in rainbow trout (Oncorhynchus mykiss). Aqua Nutr 25(2):298–309. https://doi.org/10.1111/anu.12853

    Article  CAS  Google Scholar 

  12. Zargar A, Mirghaed AT, Mirzargar SS, Ghelichpour M, Yousefi M, Hoseini SM (2020) Dietary ginger administration attenuates oxidative stress and immunosuppression caused by oxytetracycline in rainbow trout (Oncorhynchus mykiss). Aquac Res 51(10):4215–4224. https://doi.org/10.1111/are.14763

    Article  CAS  Google Scholar 

  13. Nakano T, Hayashi S, Nagamine N (2018) Effect of excessive doses of oxytetracycline on stress-related biomarker expression in coho salmon. Environ Sci Pollut Res Int 25(8):7121–7128. https://doi.org/10.1007/s11356-015-4898-4

    Article  CAS  PubMed  Google Scholar 

  14. Abdel-Latif HMR, Yilmaz E, Dawood MAO, Ringø E, Ahmadifar E, Yilmaz S (2022) Shrimp vibriosis and possible control measures using probiotics, postbiotics, prebiotics, and synbiotics: a review. Aquaculture 551:737951. https://doi.org/10.1016/j.aquaculture.2022.737951

    Article  Google Scholar 

  15. Yilmaz S, Yilmaz E, Dawood MAO, Ringø E, Ahmadifar E, Abdel-Latif HMR (2022) Probiotics, prebiotics, and synbiotics used to control vibriosis in fish: a review. Aquaculture 547:737514. https://doi.org/10.1016/j.aquaculture.2021.737514

    Article  CAS  Google Scholar 

  16. El-Saadony MT, Alagawany M, Patra AK, Kar I, Tiwari R, Dawood MAO, Dhama K, Abdel-Latif HMR (2021) The functionality of probiotics in aquaculture: an overview. Fish Shellfish Immunol 117:36–52. https://doi.org/10.1016/j.fsi.2021.07.007

    Article  PubMed  Google Scholar 

  17. Richard N, Costas B, Machado M, Fernández-Boo S, Girons A, Dias J, Corraze G, Terrier F, Marchand Y, Skiba-Cassy S (2021) Inclusion of a protein-rich yeast fraction in rainbow trout plant-based diet: consequences on growth performances, flesh fatty acid profile and health-related parameters. Aquaculture 544(4):737132. https://doi.org/10.1016/j.aquaculture.2021.737132

    Article  CAS  Google Scholar 

  18. Hashemi SS, Karimi K, Taherzadeh MJ (2021) Integrated process for protein, pigments, and biogas production from baker’s yeast wastewater using filamentous fungi. Bioresour Technol 337:125356. https://doi.org/10.1016/j.biortech.2021.125356

    Article  CAS  Google Scholar 

  19. Siddik MAB, Foysal MJ, Fotedar R, Francis DS, Gupta SK (2022) Probiotic yeast Saccharomyces cerevisiae coupled with Lactobacillus casei modulates physiological performance and promotes gut microbiota in juvenile barramundi. Lates calcarifer Aquaculture 546:737346. https://doi.org/10.1016/j.aquaculture.2021.737346

    Article  CAS  Google Scholar 

  20. Yousefi S, Shokri MM, Noveirian HA, Hoseinifar SH (2020) Effects of dietary yeast cell wall on biochemical indices, serum and skin mucus immune responses, oxidative status and resistance against Aeromonas hydrophila in juvenile Persian sturgeon (Acipenser persicus). Fish Shellfish Immunol 106:464–472. https://doi.org/10.1016/j.fsi.2020.08.007

    Article  CAS  PubMed  Google Scholar 

  21. Zhang P, Yang F, Hu J, Han D, Liu H, Jin J, Yang Y, Yi J, Zhu X, Xie S (2020) Optimal form of yeast cell wall promotes growth, immunity and disease resistance in gibel carp (Carassius auratus gibelio). Aquac Rep 18:100465. https://doi.org/10.1016/j.aqrep.2020.100465

    Article  Google Scholar 

  22. Huyben D, Nyman A, Vidaković A, Passoth V, Moccia R, Kiessling A, Dicksved J, Lundh T (2017) Effects of dietary inclusion of the yeasts Saccharomyces cerevisiae and Wickerhamomyces anomalus on gut microbiota of rainbow trout. Aquaculture 473:528–537. https://doi.org/10.1016/j.aquaculture.2017.03.024

    Article  CAS  Google Scholar 

  23. Reyes-Becerril M, Guluarte C, Ceballos-Francisco D, Angulo C, Esteban MÁ (2017) Dietary yeast Sterigmatomyces halophilus enhances mucosal immunity of gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 64:165–175. https://doi.org/10.1016/j.fsi.2017.03.027

    Article  CAS  PubMed  Google Scholar 

  24. Han M, Xu Zy DuC, Qian H, Zhang WG (2016) Effects of nitrogen on the lipid and carotenoid accumulation of oleaginous yeast Sporidiobolus pararoseus. Bioprocess Biosyst Eng 39:1425–1433. https://doi.org/10.1007/s00449-016-1620-y

    Article  CAS  PubMed  Google Scholar 

  25. Lopes NA, Remedi RD, dos Santos SC, Burkert CAV, de Medeiros Burkert JF (2017) Different cell disruption methods for obtaining carotenoids by Sporodiobolus pararoseus and Rhodothorula mucilaginosa. Food Sci Biotechnol 26:759–766. https://doi.org/10.1007/s10068-017-0098-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Valduga E, Rausch Ribeiro AH, Cence K, Colet R, Tiggemann L, Zeni J, Toniazzo G (2014) Carotenoids production from a newly isolated Sporidiobolus pararoseus strain using agroindustrial substrates. Biocatal Agric Biotechnol 3:207–213. https://doi.org/10.1016/j.bcab.2013.10.001

    Article  Google Scholar 

  27. Chaiyaso T, Manowattana A (2018) Enhancement of carotenoids and lipids production by oleaginous red yeast Sporidiobolus pararoseus KM281507. Prep Biochem Biotechnol 48:13–23. https://doi.org/10.1080/10826068.2017.1381620

    Article  CAS  PubMed  Google Scholar 

  28. Frengova GI, Beshkova DM (2009) Carotenoids from Rhodotorula and Phaffia: yeasts of biotechnological importance. J Ind Microbiol Biotechnol 36(2):163–180. https://doi.org/10.1007/s10295-008-0492-9

    Article  CAS  PubMed  Google Scholar 

  29. Blomqvist J, Pickova J, Tilami SK, Sampels S, Mikkelsen N, Brandenburg J, Sandgren M, Passoth V (2018) Oleaginous yeast as a component in fish feed. Sci Rep 8:1–8. https://doi.org/10.1038/s41598-018-34232-x

    Article  CAS  Google Scholar 

  30. Yang SP, Wu ZH, Jian JC, Zhang XZ (2010) Effect of marine red yeast Rhodosporidium paludigenum on growth and antioxidant competence of Litopenaeus vannamei. Aquaculture 309:62–65. https://doi.org/10.1016/j.aquaculture.2010.09.032

    Article  CAS  Google Scholar 

  31. Yun L, Wang W, Li Y, Xie M, Chen T, Hu C, Luo P, Li D (2021) Potential application values of a marine red yeast, Rhodosporidiums sphaerocarpum YLY01, in aquaculture and tail water treatment assessed by the removal of ammonia nitrogen, the inhibition to Vibrio spp., and nutrient composition. PloS one 16(2): e0246841. https://doi.org/10.1371/journal.pone.0246841

  32. Zhou C, Lin H, Xia D, Yang K, Yang Y, Huang Z, Wei Y (2016) Effect of dietary marine red yeast Rhodotorula mucilaginosa on the growth performance, and also non-specific immune responses of juvenile golden pompano Trachinotus ovatus when challenged with Vibrio harveyi. J Aquacult Bamid 68:20829. https://doi.org/10.46989/001c.20829

  33. Zhang P, Cao S, Zou T, Han D, Liu H, Jin J, Yang Y, Zhu X, Xie S, Zhou W (2018) Effects of dietary yeast culture on growth performance, immune response and disease resistance of gibel carp (Carassius auratus gibel CA III). Fish Shellfish Immunol 82:400–407. https://doi.org/10.1016/j.fsi.2018.08.044

    Article  CAS  PubMed  Google Scholar 

  34. Burgents JE, Burnett KG, Burnett LE (2004) Disease resistance of Pacific white shrimp, Litopenaeus vannamei, following the dietary administration of a yeast culture food supplement. Aquaculture 231(1–4):1–8. https://doi.org/10.1016/j.aquaculture.2003.09.003

    Article  Google Scholar 

  35. Tapingkae W, Yindee P, Moonmanee T (2016) Effect of dietary red yeast (Sporidiobolus pararoseus) supplementation on small intestinal histomorphometry of laying hens. J Anim Plant Sci 26:909–915

    CAS  Google Scholar 

  36. Tapingkae W, Panyachai K, Yachai M, Doan HV (2017) Effects of dietary red yeast (Sporidiobolus pararoseus) on production performance and egg quality of laying hens. J Anim Physiol Anim Nutr (Berl) 102:e337–e344. https://doi.org/10.1111/jpn.12751

    Article  CAS  PubMed  Google Scholar 

  37. Sutthi N, Thaimuangphol W (2020) Effects of yeast (Saccharomyces cerevisiae) on growth performances, body composition and blood chemistry of Nile tilapia (Oreochromis niloticus Linnaeus, 1758) under different salinity conditions. Iran J Fish Sci 19:1428–1446. https://doi.org/10.22092/IJFS.2019.119254

  38. Hoseini SM, Yousefi M, Hoseinifar SH, Doan HV (2019) Cytokines’ gene expression, humoral immune and biochemical responses of common carp (Cyprinus carpio, Linnaeus, 1758) to transportation density and recovery in brackish water. Aquaculture 504:13–21. https://doi.org/10.1016/j.aquaculture.2019.01.049

    Article  CAS  Google Scholar 

  39. Van Doan H, Wangkahart E, Thaimuangphol W, Panase P, Sutthi N (2021) Effects of Bacillus spp. mixture on growth, immune responses, expression of immune related genes, and resistance of Nile tilapia against Streptococcus agalactiae infection. Probiotics Antimicrob Proteins https://doi.org/10.1007/s12602-021-09845-w

  40. AOAC (1995) Official methods of analysis of AOAC International, 16th edition. AOAC International Arlington. 1.

  41. Rodriguez-Amaya DB, Kimura M (2004) Harvestplus handbook for carotenoid analysis. HarvestPlus Technical Monograph 2. Washington DC. 1–63.

  42. Biswas AK, Takeuchi T (2003) Effects of photoperiod and feeding interval on food intake and growth rate of Nile tilapia Oreochromis niloticus L. Fish Sci 69:1010–1016. https://doi.org/10.1046/j.1444-2906.2003.00720.x

    Article  CAS  Google Scholar 

  43. Da CT, Lundh T, Lindberg JE (2012) Evaluation of local feed resources as alternatives to fish meal in terms of growth performance, feed utilisation and biological indices of striped catfish (Pangasianodon hypophthalmus) fingerlings. Aquaculture 364:150–156. https://doi.org/10.1016/j.aquaculture.2012.08.010

    Article  Google Scholar 

  44. Panase P, Kamee B, Moungmor S, Tipdacho P, Matidtor J, Sutthi N (2018) Effects of Euphorbia hirta plant leaf extract on growth performance, hematological and organosomatic indices of hybrid catfish, Clarias macrocephalus×C. gariepinus. Fish Sci 84:1025–1036. https://doi.org/10.1007/s12562-018-1234-1

    Article  CAS  Google Scholar 

  45. Sutthi N, Thaimuangphol W, Rodmongkoldee M, Leelapatra W, Panase P (2018) Growth performances, survival rate, and biochemical parameters of Nile tilapia (Oreochromis niloticus) reared in water treated with probiotic. Comp Clin Pathol 27:597–603. https://doi.org/10.1007/s00580-017-2633-x

    Article  CAS  Google Scholar 

  46. Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175

    Article  CAS  PubMed  Google Scholar 

  47. Mansour ATE, Goda AA, Omar EA, Khalil HS, Esteban MÁ (2017) Dietary supplementation of organic selenium improves growth, survival, antioxidant and immune status of meagre, Argyrosomus regius, juveniles. Fish Shellfish Immunol 68:516–524. https://doi.org/10.1016/j.fsi.2017.07.060

    Article  CAS  PubMed  Google Scholar 

  48. Rehulka J (2003) Haematological analyses in rainbow trout Oncorhynchus mykiss affected by viral haemorrhagic septicaemia (VHS). Dis Aquat Organ 56:185–193. https://doi.org/10.3354/dao056185

    Article  CAS  PubMed  Google Scholar 

  49. Davis A, Maney D, Maerz J (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760–772. https://doi.org/10.1111/j.1365-2435.2008.01467.x

    Article  Google Scholar 

  50. Zhao H, Panase P, Zhang Z, Yao P, Zhang Y, Suwannapoom C (2018) Hematological and plasm biochemical values for Rhinogobio ventralis in the Yangtze River, China. Comp Clin Pathol 27:741–745. https://doi.org/10.1007/s00580-018-2660-2

    Article  CAS  Google Scholar 

  51. Parry RM Jr, Chandan RC, Shahani KM (1965) A rapid and sensitive assay of muramidase. Proc Soc Exp Biol Med 119:384–386. https://doi.org/10.3181/00379727-119-30188

    Article  CAS  PubMed  Google Scholar 

  52. Sahoo P, Kumari J, Mishra B (2005) Non-specific immune responses in juveniles of Indian major carps. J Appl Ichthyol 21:151–155. https://doi.org/10.1111/j.1439-0426.2004.00606.x

    Article  Google Scholar 

  53. Pirarat N, Pinpimai K, Endo M, Katagiri T, Ponpornpisit A, Chansue N, Maita M (2011) Modulation of intestinal morphology and immunity in Nile tilapia (Oreochromis niloticus) by Lactobacillus rhamnosus GG. Res Vet Sci 91:e92-97. https://doi.org/10.1016/j.rvsc.2011.02.014

    Article  CAS  PubMed  Google Scholar 

  54. Abdel-Tawwab M, Abdel-Rahman AM, Ismael NEM (2008) Evaluation of commercial live bakers’ yeast, Saccharomyces cerevisiae as a growth and immunity promoter for Fry Nile tilapia, Oreochromis niloticus (L.) challenged in situ with Aeromonas hydrophila. Aquaculture 280:185–189. https://doi.org/10.1016/j.aquaculture.2008.03.055

    Article  Google Scholar 

  55. Sutthi N, Van Doan H (2020) Saccharomyces crevices and Bacillus spp. effectively enhance health tolerance of Nile tilapia under transportation stress. Aquaculture 528:735527. https://doi.org/10.1016/j.aquaculture.2020.735527

  56. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  57. Wangkahart E, Wachiraamonloed S, Lee PT, Subramani PA, Qi Z, Wang B (2021) Impacts of Aegle marmelos fruit extract as a medicinal herb on growth performance, antioxidant and immune responses, digestive enzymes, and disease resistance against Streptococcus agalactiae in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 120:402–410. https://doi.org/10.1016/j.fsi.2021.11.015

    Article  CAS  PubMed  Google Scholar 

  58. Amend DF (1981) Potency testing of fish vaccines. Dev Biol Stand 49:8

    Google Scholar 

  59. Coyle SD, Tidwell JH, Webster CD (2000) Response of largemouth bass Micropterus salmoides to dietary supplementation of lysine, methionine, and highly unsaturated fatty acids. J World Aquac Soc 31:89–95. https://doi.org/10.1111/j.1749-7345.2000.tb00702.x

    Article  Google Scholar 

  60. De Silva SS, Anderson TA (1994) Fish nutrition in aquaculture. Chapman & Hall, London p, p 320

    Google Scholar 

  61. Kühlwein H, Merrifield DL, Rawling MD, Foey AD, Davies SJ (2014) Effects of dietary β-(1,3)(1,6)-D-glucan supplementation on growth performance, intestinal morphology and haemato-immunological profile of mirror carp (Cyprinus carpio L.). J Anim Physiol Anim Nutr (Berl) 98:279–289. https://doi.org/10.1111/jpn.12078

    Article  CAS  PubMed  Google Scholar 

  62. Li P, Gatlin DM III (2006) Nucleotide nutrition in fish: current knowledge and future applications. Aquaculture 251:141–152. https://doi.org/10.1016/j.aquaculture.2005.01.009

    Article  CAS  Google Scholar 

  63. Refstie S, Baeverfjord G, Seim RR, Elvebø O (2010) Effects of dietary yeast cell wall β-glucans and MOS on performance, gut health, and salmon lice resistance in Atlantic salmon (Salmo salar) fed sunflower and soybean meal. Aquaculture 305:109–116. https://doi.org/10.1016/j.aquaculture.2010.04.005

    Article  CAS  Google Scholar 

  64. Lara-Flores M, Olvera-Novoa MA, Guzmán-Méndez BE, López-Madrid W (2003) Use of the bacteria Streptococcus faecium and Lactobacillus acidophilus, and the yeast Saccharomyces cerevisiae as growth promoters in Nile tilapia (Oreochromis niloticus). Aquaculture 216:193–201. https://doi.org/10.1016/S0044-8486(02)00277-6

    Article  Google Scholar 

  65. Nakano T, Wiegertjes G (2020) Properties of carotenoids in fish fitness: a review. Mar Drugs 18(11):568. https://doi.org/10.3390/md18110568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Sefc KM, Brown AC, Clotfelter ED (2014) Carotenoid-based coloration in cichlid fishes. Comp Biochem Physiol A Mol Integr Physiol 173:42–51. https://doi.org/10.1016/j.cbpa.2014.03.006

    Article  CAS  PubMed Central  Google Scholar 

  67. Akbary P, Molazaei E, Aminikhoei Z (2018) Effect of dietary supplementation of Ulva rigida C. Agardh extract on several of physiological parameters of grey mullet, Mugil cephalus (Linnaeus). Iran J Aquat Anim Health 4:59–68. https://doi.org/10.29252/ijaah.4.1.59

  68. Hassaan MS, Soltan MA, Jarmołowicz S, Abdo HS (2018) Combined effects of dietary malic acid and Bacillus subtilis on growth, gut microbiota and blood parameters of Nile tilapia (Oreochromis niloticus). Aquac Nutr 24:83–93. https://doi.org/10.1111/anu.12536

    Article  CAS  Google Scholar 

  69. Baker M (2002) Albumin, steroid hormones and the origin of vertebrates. J Endocrinol 175:121–127. https://doi.org/10.1677/joe.0.1750121

    Article  CAS  PubMed  Google Scholar 

  70. Tahmasebi-Kohyani A, Keyvanshokooh S, Nematollahi A, Mahmoudi N, Pasha-Zanoosi H (2011) Dietary administration of nucleotides to enhance growth, humoral immune responses, and disease resistance of the rainbow trout (Oncorhynchus mykiss) fingerlings. Fish Shellfish Immunol 30:189–193. https://doi.org/10.1016/j.fsi.2010.10.005

    Article  CAS  PubMed  Google Scholar 

  71. Pakhira C, Nagesh T, Abraham T, Dash G, Behera S (2015) Stress responses in rohu, Labeo rohita transported at different densities. Aquac Rep 2:39–45. https://doi.org/10.1016/j.aqrep.2015.06.002

    Article  Google Scholar 

  72. Ajeniyi SA, Solomon JR (2014) Urea and creatinine of Clarias gariepinus in three different commercial ponds. Nat Sci 12:124–138

    Google Scholar 

  73. Hassaan MS, Mahmoud SA, Jarmolowicz S, El-Haroun ER, Mohammady EY, Davies SJ (2018) Effects of dietary baker’s yeast extract on the growth, blood indices and histology of Nile tilapia (Oreochromis niloticus L.) fingerlings. Aquac Nutr 24:1709–1717. https://doi.org/10.1111/anu.12805

    Article  CAS  Google Scholar 

  74. Winston GW (1991) Oxidants and antioxidants in aquatic animals. Comp Biochem Physiol C Comp Pharmacol Toxicol 100:173–176. https://doi.org/10.1016/0742-8413(91)90148-m

    Article  CAS  PubMed  Google Scholar 

  75. Fridovich I (1989) Superoxide dismutases: an adaptation to a paramagnetic gas. J Biol Chem 264:7761–7764. https://doi.org/10.1016/S0021-9258(18)83102-7

    Article  CAS  PubMed  Google Scholar 

  76. Zhang J, Li X, Leng X, Zhang C, Han Z, Zhang F (2013) Effects of dietary astaxanthins on pigmentation of flesh and tissue antioxidation of rainbow trout (Oncorhynchus mykiss). Aquacult Int 21:579–589. https://doi.org/10.1007/s10499-012-9590-9

    Article  CAS  Google Scholar 

  77. Nakano T, Kanmuri T, Sato M, Takeuchi M (1999) Effect of astaxanthin rich red yeast (Phaffia rhodozyma) on oxidative stress in rainbow trout. Biochim Biophys Acta 1426:119–125. https://doi.org/10.1016/s0304-4165(98)00145-7

    Article  CAS  PubMed  Google Scholar 

  78. Reyes-Cerpa S, Vallejos-Vidal E, Gonzalez-Bown MJ, Morales-Reyes J, Pérez-Stuardo D, Vargas D, Imarai M, Cifuentes V, Spencer E, Sandino AM (2018) Effect of yeast (Xanthophyllomyces dendrorhous) and plant (Saint John’s wort, lemon balm, and rosemary) extract based functional diets on antioxidant and immune status of Atlantic salmon (Salmo salar) subjected to crowding stress. Fish Shellfish Immunol 74:250–259. https://doi.org/10.1016/j.fsi.2017.12.061

    Article  CAS  PubMed  Google Scholar 

  79. Reda RM, Selim KM, Mahmoud R, El-Araby IE (2018) Effect of dietary yeast nucleotide on antioxidant activity, non-specific immunity, intestinal cytokines, and disease resistance in Nile tilapia. Fish Shellfish Immunol 80:281–290. https://doi.org/10.1016/j.fsi.2018.06.016

    Article  CAS  PubMed  Google Scholar 

  80. Amengual J, Lobo GP, Golczak M, Li HNM, Klimova T, Hoppel CL, Wyss A, Palczewski K, Von Lintig J (2011) A mitochondrial enzyme degrades carotenoids and protects against oxidative stress. FASEB J 25:948–959. https://doi.org/10.1096/fj.10-173906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Milani A, Basirnejad M, Shahbazi S, Bolhassani A (2017) Carotenoids: biochemistry, pharmacology and treatment. Br J Pharmacol 174:1290–1324. https://doi.org/10.1111/bph.13625

    Article  CAS  PubMed  Google Scholar 

  82. Chaudhry H, Zhou J, Zhong Y, Ali MM, McGuire F, Nagarkatti PS, Nagarkatti M (2013) Role of cytokines as a double-edged sword in sepsis. In Vivo 27:669–684

    CAS  PubMed  Google Scholar 

  83. Wang T, Secombes CJ (2013) The cytokine networks of adaptive immunity in fish. Fish Shellfish Immunol 35:1703–1718. https://doi.org/10.1016/j.fsi.2013.08.030

    Article  CAS  PubMed  Google Scholar 

  84. Sakai M, Ji H, Kono T (2021) Fish cytokines: current research and applications. Fish Sci 87:1–9. https://doi.org/10.1007/s12562-020-01476-4

    Article  CAS  Google Scholar 

  85. Lokesh J, Fernandes JM, Korsnes K, Bergh Ø, Brinchmann MF, Kiron V (2012) Transcriptional regulation of cytokines in the intestine of Atlantic cod fed yeast derived mannan oligosaccharide or β-glucan and challenged with Vibrio anguillarum. Fish Shellfish Immunol 33:626–631. https://doi.org/10.1016/j.fsi.2012.06.017

    Article  CAS  PubMed  Google Scholar 

  86. Chansue N, Endo M, Kono T, Sakai M (2000) The stimulation of cytokine-like proteins in Tilapia (Oreochromis niloticus) orally treated with beta-1, 3-glucan. Asian Fish Sci 13:271–278

    Google Scholar 

  87. Sahlmann C, Djordjevic B, Lagos L, Mydland LT, Morales-Lange B, Hansen JØ, Ånestad R, Mercado L, Bjelanovic M, Press CM (2019) Yeast as a protein source during smoltification of Atlantic salmon (Salmo salar L.), enhances performance and modulates health. Aquaculture 513:734396. https://doi.org/10.1016/j.aquaculture.2019.734396

  88. Bruce TJ, Brown ML (2017) A review of immune system components, cytokines, and immunostimulants in cultured finfish species. Open J Anim Sci 7:267–288. https://doi.org/10.4236/ojas.2017.73021

    Article  CAS  Google Scholar 

  89. Anderson DP (1992) Immunostimulants, adjuvants, and vaccine carriers in fish: applications to aquaculture. Annu Rev Fish Dis 2:281–307. https://doi.org/10.1016/0959-8030(92)90067-8

    Article  Google Scholar 

  90. Sahoo L, Debnath C, Parhi J, Choudhury J, Choudhury TG, PaniPrasad K, Kandpal B (2020) Molecular characterization and immunostimulant-induced expression analysis of type I interferon gene in Labeo bata (Ham.). Aquac Rep 18:100490. https://doi.org/10.1016/j.aqrep.2020.100490

  91. Wang E, Chen X, Wang K, Wang J, Chen D, Geng Y, Lai W, Wei X (2016) Plant polysaccharides used as immunostimulants enhance innate immune response and disease resistance against Aeromonas hydrophila infection in fish. Fish Shellfish Immunol 59:196–202. https://doi.org/10.1016/j.fsi.2016.10.039

    Article  CAS  PubMed  Google Scholar 

  92. Dalmo RA, Bogwald J (2008) Beta-glucans as conductors of immune symphonies. Fish Shellfish Immunol 25:384–396. https://doi.org/10.1016/j.fsi.2008.04.008

    Article  CAS  PubMed  Google Scholar 

  93. Ringø E, Olsen R, Vecino J, Wadsworth S, Song S (2012) Use of immunostimulants and nucleotides in aquaculture: a review. J Mar Sci Res Dev 2:104. https://doi.org/10.4172/2155-9910.1000104

    Article  Google Scholar 

  94. Rumsey GL, Winfree RA, Hughes SG (1992) Nutritional value of dietary nucleic acids and purine bases to rainbow trout (Oncorhynchus mykiss). Aquaculture 108:97–110. https://doi.org/10.1016/0044-8486(92)90321-B

    Article  CAS  Google Scholar 

  95. Burrells C, Williams P, Forno P (2001) Dietary nucleotides: a novel supplement in fish feeds: 1. Effects on resistance to disease in salmonids. Aquaculture 199:159–169. https://doi.org/10.1016/S0044-8486(01)00577-4

    Article  CAS  Google Scholar 

  96. Li P, Lewis DH, Gatlin DM (2004) Dietary oligonucleotides from yeast RNA influence immune responses and resistance of hybrid striped bass (Morone chrysops × Morone saxatilis) to Streptococcus iniae infection. Fish Shellfish Immunol 16:561–569. https://doi.org/10.1016/j.fsi.2003.09.005

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We gratefully thank Asst. Prof. Dr. Prapansak Srisapoome for kindly supplying the S. agalactiae used for this research. Special thanks also to Dr. Nanthana Pothakam, Conservation and Research Section, Animal Management Division, Chiang Mai Night Safari, for kindly supporting the laboratory collaboration. Finally, thanks to Mr. Thanasak Saleekiaw and Ms. Prapatson Netsongkram for their kind assistance during the preparation of this research.

Funding

This research project was financially supported by Mahasarakham University and partially, work was supported by Chiang Mai University.

Author information

Authors and Affiliations

  1. Department of Animal and Aquatic Sciences, Faculty of Agriculture, Chiang Mai University, Chiang Mai, 50200, Thailand

    Hien Van Doan & Wanaporn Tapingkae

  2. Innovative Agriculture Research Center, Faculty of Agriculture, Chiang Mai University, Chiang Mai, 50200, Thailand

    Hien Van Doan

  3. Division of Biotechnology, Faculty of Agro-Industry, Chiang Mai University, Chiang Mai, 50100, Thailand

    Thanongsak Chaiyaso

  4. Department of Agricultural Technology, Faculty of Technology, Mahasarakham University, Maha Sarakham, 44150, Thailand

    Eakapol Wangkahart, Ruamruedee Panchan & Nantaporn Sutthi

  5. Applied Animal and Aquatic Sciences Research Unit, Division of Fisheries, Faculty of Technology, Mahasarakham University, Maha Sarakham, 44150, Thailand

    Eakapol Wangkahart & Nantaporn Sutthi

Authors
  1. Hien Van Doan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wanaporn Tapingkae
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thanongsak Chaiyaso
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eakapol Wangkahart
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ruamruedee Panchan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nantaporn Sutthi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nantaporn Sutthi.

Ethics declarations

Ethics Approval

Animal use protocol was followed the Institutional Animal Care and Use Committee, Mahasarakham University (IACUC-MSU), Thailand (IACUC-MSU-014/2020).

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Van Doan, H., Tapingkae, W., Chaiyaso, T. et al. Effects of Red Yeast (Sporidiobolus pararoseus) on Growth, Innate Immunity, Expression of Immune-related Genes and Disease Resistance of Nile Tilapia (Oreochromis niloticus). Probiotics & Antimicro. Prot. 15, 1312–1326 (2023). https://doi.org/10.1007/s12602-022-09984-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-022-09984-8

Keywords

Search

Navigation