Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Dietary Exogenous α-Amylase Modulates the Nutrient Digestibility, Digestive Enzyme Activity, Growth-Related Gene Expression, and Diet Degradation Rate of Olive Flounder (Paralichthys olivaceus)

  • Md. Tawheed Hasan (Core-Facility Center for Tissue Regeneration, Dong-Eui University) ;
  • Hyeon Jong Kim (Aquafeed Research Center, National Institute of Fisheries Science) ;
  • Sang-Woo Hur (Aquafeed Research Center, National Institute of Fisheries Science) ;
  • Seong-Mok Jeong (Aquafeed Research Center, National Institute of Fisheries Science) ;
  • Kang-Woong Kim (Aquafeed Research Center, National Institute of Fisheries Science) ;
  • Seunghan Lee (Aquafeed Research Center, National Institute of Fisheries Science)
  • Received : 2023.03.21
  • Accepted : 2023.06.07
  • Published : 2023.10.28
Download PDF
⟨ Previous Next ⟩

Abstract

In this study, a 12-week feeding experiment was conducted to characterize the effects of exogenous α-amylase on the growth, feed utilization, digestibility, plasma α-amylase activity, feed degradation rate, and fecal particle size of olive flounder (Paralichthys olivaceus). Diet was supplemented with 0 (AA0; control), 100 (AA100), 200 (AA200), or 400 (AA400) mg/kg of α-amylase, respectively. Fish (273.1 ± 2.3 g) were stocked into 12 tanks (25 fish/1,000-L tank) and 3 tanks were randomly selected for each diet group. As a result, α-amylase was found to have no significant effects (p ≥ 0.05) on the growth, feed utilization parameters, and whole-body proximate compositions. α-Amylase-treated fish exhibited only a significant increase in the apparent digestibility coefficient of carbohydrates compared to the controls. In addition, in vitro analyses revealed that α-amylase dose-dependently increased (p < 0.05) the feed degradation rate, while photographs of the intestinal content after 2, 4, and 8 h of feeding demonstrated an improved degradation rate in the α-amylase-treated groups. Plasma α-amylase content was higher in the AA200 and AA400 groups, whereas the control group produced significantly larger-sized fecal particles (90% size class) than these two groups. In the intestine, no changes were observed in the expression levels of the immune-related TNF-α, IL-1β, IL-2, immunoglobulin-M, HSP-70, lysozyme, and amylase alpha-2A. However, growth-related genes IGF-1, IGF-2, TGF-β3, and growth hormone genes were upregulated in muscle tissues. Collectively, exogenous α-amylase has positive roles in the modulation of the digestibility coefficient, blood α-amylase concentration, growth-related gene expression, and diet degradation for improved digestion in olive flounder.

Keywords

Acknowledgement

This study was supported by the National Institute of Fisheries Science, Ministry of Oceans and Fisheries, Republic of Korea (R2023036).

References

  1. FAO Fisheries & Aquaculture -Species Fact Sheets-Paralichthys olivaceus (Temminck & Schlegel, 1846). (2021). Food and Agriculture Organization of the United Nations. Retrieved from http://www.fao.org/fishery/species/ 
  2. FishStatJ-FAO Fisheries and Aquaculture Software. (2020). [computer software]. FAO fisheries division. (Updated September 14, 2020). Retrieved from http://www.fao.org/fishery/statistics/software/fishstatj/en. 
  3. Suresh S, Suriyavathana M. 2011. Carbohydrate characterization of the cassava varieties (co5 and h226). J. Dairy. Food Home Sci. 30: 53-57. 
  4. Stone DAJ, Allan GL, Anderson AA. 2003. Carbohydrate utilization by juvenile silver perch, Bidyanus bidyanus (Mitchell). III. The protein-sparing effect of wheat starch-based carbohydrates. Aquac. Res. 34: 123-134.  https://doi.org/10.1046/j.1365-2109.2003.00774.x
  5. Wilson RP. 1994. Utilization of dietary carbohydrate by fish. Aquaculture 124: 67-80.  https://doi.org/10.1016/0044-8486(94)90363-8
  6. Kumar S, Chakravarty S. 2018. Amylases. In Enzymes in human and animal nutrition (Ed. C.S. Nunes and V. Kumar). Elsevier. Amsterdam, the Netherlands. pp.163-180. 
  7. Zhao W, Wei HL, Wang ZQ, He XS, Niu J. 2022. Effects of dietary carbohydrate levels on growth performance, body composition, antioxidant capacity, immunity, and liver morphology in Oncorhynchus mykiss under cage culture with flowing freshwater. Aqua. Nut. 2022: 7820017. 
  8. Farhangi M, Carter CG. 2007. Effect of enzyme supplementation to dehulled lupin-based diets on growth, feed efficiency, nutrient digestibility and carcass composition of rainbow trout, Oncorhynchus mykiss (Walbaum). Aquac. Res. 38: 1274-1282.  https://doi.org/10.1111/j.1365-2109.2007.01789.x
  9. Takeuchi T, Jeong KS and Watanabe T. 1990. Availability of extruded carbohydrate ingredients to rainbow trout Oncorhynchus mykiss and carp Cyprinus carpio. Bul. Japanese Soc. 56: 1839-1845.  https://doi.org/10.2331/suisan.56.1839
  10. Qu H, Ke W, Wen Z, Guo B, Lu X, Zhao Y, Yang Y, et al. 2022. Effects of dietary carbohydrate on growth, feed utilization, hepatic glucose and lipid metabolism in endangered Yangtze sturgeon (Acipenser dabryanus). Aquac. Rep. 26: 101334. 
  11. Vasquez-Torres W and Arias-Castellanos JA. 2013. Effect of dietary carbohydrates and lipids on growth in cachama (Piaractus brachypomus). Aquac. Res. 44: 1768-1776.  https://doi.org/10.1111/j.1365-2109.2012.03183.x
  12. Cowieson AJ, Hruby M, Pierson EEM. 2006. Evolving enzyme technology: impact on commercial poultry nutrition. Nutr. Res. Rev. 19: 90-103.  https://doi.org/10.1079/NRR2006121
  13. Dalsgaard J, Verlhac V, Hjermitslev NH, Ekmann KS, Fischer M, Klausen M, et al. 2012. Effects of exogenous enzymes on apparent nutrient digestibility in rainbow trout (Oncorhynchus mykiss) fed diets with high inclusion of plant-based protein. Anim. Feed Sci. Technol. 171: 181-191.  https://doi.org/10.1016/j.anifeedsci.2011.10.005
  14. Jiang TT, Feng L, Liu Y, Jiang WD, Jiang J, Li SH, et al. 2014. Effects of exogenous xylanase supplementation in plant protein-enriched diets on growth performance, intestinal enzyme activities and microflora of juvenile Jian carp (Cyprinus carpio var. Jian). Aquac. Nutr. 20: 632-645.  https://doi.org/10.1111/anu.12125
  15. Adeola O, Cowieson AJ. 2011. Board-invited review: opportunities and challenges in using exogenous enzymes to improve nonruminant animal production. J. Anim. Sci. 89: 3189-3218.  https://doi.org/10.2527/jas.2010-3715
  16. Liang Q, Yuan M, Xu L, Lio E, Zhang F, Mou H, et al. 2022. Application of enzymes as a feed additive in aquaculture. Mar. Life. Sci. Technol. 4: 208-221.  https://doi.org/10.1007/s42995-022-00128-z
  17. LP Information Inc, 2022 Global animal feed enzymes market growth 2022-2028. Market Research.com. https:// www.marketresearch.com/LP-Information-Inc-v4134/Global-Animal-Feed-Enzym es-Growth-30499852/. Accessed Jan. 2023. 
  18. Upreti A, Byanju B, Fuyal M, Chhetri A, Pandey P, Ranjitkar R, et al. 2019. Evaluation of α-amylase, lipase inhibition and in-vivo pharmacological activities of Eucalyptus camaladulensis Dehnh leaf extract. J. Trad Complement. Med. 9: 312-318.  https://doi.org/10.1016/j.jtcme.2018.07.001
  19. Kumar S, Sahu NP, Pal AK, Sagar V, Sinha AK, Baruah K. 2009. Modulation of key metabolic enzyme of Labeo rohita (Hamilton) juvenile: effect of dietary starch type, protein level and exogenous α-amylase in the diet. Fish Physiol. Biochem. 35: 301-315.  https://doi.org/10.1007/s10695-008-9213-6
  20. Goda AMA, Mabrouk HAHH, Wafa MAEH, El-Afifi TM. 2012. Effect of using baker's yeast and exogenous digestive enzymes as growth promoters on growth, feed utilization and hematological indices of Nile tilapia, Oreochromis niloticus fingerlings. J. Agri. Sci. Tech. B 2: 15-28. 
  21. Zamini A, Kanani HG, azam Esmaeili A, Ramezani S, Zoriezahra SJ. 2014. Effects of two dietary exogenous multi-enzyme supplementation, Natuzyme® and betamannanase (Hemicell®), on growth and blood parameters of Caspian salmon (Salmo trutta caspius). Comp. Clin. Pathol. 23: 187-192.  https://doi.org/10.1007/s00580-012-1593-4
  22. Yildirim YB, Turan F. 2010. Effects of exogenous enzyme supplementation in diets on growth and feed utilization in African catfish, Clarias gariepinus. J. Anim. Vet. Adv. 9: 27-331.  https://doi.org/10.3923/javaa.2010.27.31
  23. Zhou Y, Yuan X, Liang XF, Fang L, Li J, Guo X, et al. 2013. Enhancement of growth and intestinal flora in grass carp: the effect of exogenous cellulase. Aquaculture 416-417: 1-7.  https://doi.org/10.1016/j.aquaculture.2013.08.023
  24. Yigit NO, Olmez M. 2011. Effects of cellulase addition to canola meal in tilapia (Oreochromis niloticus L.) diets. Aquac. Nutr. 17: 494-500.  https://doi.org/10.1111/j.1365-2095.2010.00789.x
  25. Ogunkoya AE, Page GI, Adewolu MA, Bureau DP. 2006. Dietary incorporation of soybean meal and exogenous enzyme cocktail can affect physical characteristics of faecal material egested by rainbow trout (Oncorhynchus mykiss). Aquaculture 254: 466-475.  https://doi.org/10.1016/j.aquaculture.2005.10.032
  26. AOAC (Association of Official Analytical Chemists), Official Methods of Analysis, sixteenth ed., 1995. Arlington, Virginia. 
  27. Bureau DP, Harris AM, Cho CY. 1999. Apparent digestibility of rendered animal protein ingredients for rainbow trout (Oncorhynchus mykiss). Aquaculture 180: 345-358.  https://doi.org/10.1016/S0044-8486(99)00210-0
  28. Azarfar A, Tamminga S, Boer H. 2007. Effects of washing procedure, particle size and dilution on the distribution between non-washable, insoluble washable and soluble washable fractions in concentrate ingredients. J. Sci. Food Agric. 87: 2390-2398.  https://doi.org/10.1002/jsfa.2857
  29. Hasan MT, Jang WJ, Lee BJ, Kim KW, Hur SW, Lim SG, et al. 2019. Heat killed Bacillus sp. SJ-10 probiotic acts as a growth and humoral innate immunity response enhancer in olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol. 88: 424-431.  https://doi.org/10.1016/j.fsi.2019.03.018
  30. Jang WJ, Lee SJ, Jeon MH, KimTY, Lee JM, Hasan MT, et al. 2021. Characterization of a Bacillus sp. KRF-7 isolated from the intestine of rockfish (Sebastes schlegelii) and effects of dietary supplementation in the aquaculture industry. Fish Shellfish Immunol. 119: 182-192.  https://doi.org/10.1016/j.fsi.2021.09.039
  31. Ai Q, Mai K, Zhang W, Xu W, Tan B, Zhang C, et al. 2007. Effects of exogenous enzymes (phytase, non-starch polysaccharide enzyme) in diets on growth, feed utilization, nitrogen and phosphorus excretion of Japanese seabass, Lateolabrax japonicus. Comp. Biochem. Physiol. A 147: 502-508.  https://doi.org/10.1016/j.cbpa.2007.01.026
  32. Deguara S, Jauncey K, Feord J, Lopez J. 1999. Growth and feed utilization of gilthead sea bream, Sparus aurata, fed diets with supplementary enzymes. Feed Manufacturing in the Mediterranean Region: Recent Advances in Research and Technology (Ed. J. Brufau and A. Tacon). CIHEAM/IAMZ. Zaragoza, Spain. 37: 195-215 
  33. Vielma J, Makinen T, Ekholm P, Koskela J. 2000. Influence of dietary soy and phytase levels on performance and body composition of large rainbow trout (Oncorhynchus mykiss) and algal availability of phosphorus load. Aquaculture 183: 349-362.  https://doi.org/10.1016/S0044-8486(99)00299-9
  34. Carter CG, Houlihan DF, Buchanan B, Mitchell AI. 1994. Growth and feed utilization efficiencies of seawater Atlantic salmon, Salmo salar L, fed a diet containing supplementary enzymes. Aquac. Res. 25: 37-46.  https://doi.org/10.1111/j.1365-2109.1994.tb00664.x
  35. Sajjadi M, Carter CG. 2004. Dietary phytase supplementation and the utilisation of phosphorus by Atlantic salmon (Salmo salar L.) fed a canola-meal-based diet. Aquaculture 240: 417-431.  https://doi.org/10.1016/j.aquaculture.2004.07.003
  36. Lin S, Mai K, Tan B. 2007. Effects of exogenous enzyme supplementation in diets on growth and feed utilization in tilapia, Oreochromis niloticus x O. aureus. Aquac. Res. 38: 1645-1653.  https://doi.org/10.1111/j.1365-2109.2007.01825.x
  37. Ng WK, Chong KK. 2002. The nutritive value of palm kernel and the effect of enzyme supplementation in practical diets for red hybrid tilapia (Oreochromis sp). Asian Fish. Sci. 15: 167-176.  https://doi.org/10.33997/j.afs.2002.15.2.008
  38. Kumar S, Sahu NP, Pal AK, Choudhury D, Mukherjee SC. 2006. Studies on digestibility and digestive enzyme activities in Labeo rohita (Hamilton) juveniles: effect of microbial α-amylase supplementation in non-gelatinized or gelatinized corn-based diet at two protein levels. Fish Physiol. Biochem. 32: 209-220.  https://doi.org/10.1007/s10695-006-9002-z
  39. Liu QZ, Zhang H, Dai HQ, Zhao P, Mao YF, Chen KX, et al. 2021. Inhibition of starch digestion: the role of hydrophobic domain of both α-amylase and substrates. Food Chem. 341: 28211. 
  40. Khalil M, Azmat H, Khan N, Javid A, Hussain A, Hussain S.M, et al. 2018. Growth responses of striped catfish Pangasianodon hypophthalmus (Sauvage, 1878) to exogenous enzyme added feed. Pakistan J. Zool. 50: 685-693.  https://doi.org/10.17582/journal.pjz/2018.50.2.685.693
  41. Hassaan MS, Mohammady EY, Soaudy MR, Abdel Rahman AAS. 2019. Exogenous xylanase improves growth, protein digestibility and digestive enzymes activities in Nile tilapia, Oreochromis niloticus, fed different ratios of fish meal to sunflower meal. Aquac. Nutr. 25: 841-853.  https://doi.org/10.1111/anu.12903
  42. Onderci M, Sahin N, Sahin K, Cikim G, Aydin A, Ozercan I, et al. 2006. Efficacy of supplementation of α-amylase-producing bacterial culture on the performance, nutrient use, and gut morphology of broiler chickens fed a corn-based diet. Poult. Sci. 85:505-510.  https://doi.org/10.1093/ps/85.3.505
  43. Mahagna M, Nir I, Larbier M, Nitsan Z. 1995. Effect of age and exogenous amylase and protease on development of the digestive tract, pancreatic enzyme activities and digestibility of nutrients in young meat-type chicks. Reprod. Nutr. Dev. 35: 201-212.  https://doi.org/10.1051/rnd:19950208
  44. Hasan MT, Jang WJ, Lee BJ, Hur SW, Lim SG, Kim KW, et al. 2021. Dietary supplementation of Bacillus sp. SJ-10 and Lactobacillus plantarum KCCM 11322 combinations enhance growth and cellular and humoral immunity in olive flounder (Paralichthys olivaceus). Probiotics Antimicrob. Proteins 13: 1277-1291.  https://doi.org/10.1007/s12602-021-09749-9
  45. Jang WJ, Lee JM, Hasan MT, Lee BJ, Lim SG, Kong IS. 2019. Effects of probiotic supplementation of a plant-based protein diet on intestinal microbial diversity, digestive enzyme activity, intestinal structure, and immunity in olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol. 92: 719-727.  https://doi.org/10.1016/j.fsi.2019.06.056
  46. Seo BS, Park SJ, Hwang SY, Lee YI, Lee SH, Hur SW, et al. 2022. Effects of decreasing fishmeal as main source of protein on growth, digestive physiology, and gut microbiota of olive flounder (Paralichthys olivaceus). Animals 12: 2043. 
  47. Castillo S, Gatlin III DM. 2015. Dietary supplementation of exogenous carbohydrase enzymes in fish nutrition: a review. Aquaculture 435: 286-292.  https://doi.org/10.1016/j.aquaculture.2014.10.011
  48. Mahr K, Grabner M, Hofer R, Moser H. 1983. Histological and physiological development of the stomach in Coregonus sp. Arch. Hyd-robiol. 98: 344-353. 
  49. Reindl KM, Kittilson JD, Bergan HE, Sheridan MA. 2011. Growth hormone-stimulated insulin-like growth factor-1 expression in rainbow trout (Oncorhynchus mykiss) hepatocytes is mediated by ERK, PI3K-AKT, and JAK-STAT. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301: 236-243.  https://doi.org/10.1152/ajpregu.00414.2010
  50. Cao YB, Chen XQ, Wang S, Chen XC, Wang YX, Chang JP, et al. 2009. Growth hormone and insulin-like growth factor of naked carp (Gymnocypris przewalskii) in Lake Qinghai: expression in different water environments. Gen. Comp. Endocrinol. 161: 400-406.  https://doi.org/10.1016/j.ygcen.2009.02.005
  51. Funkenstein B, Olekh E, Jakowlew SB. 2010. Identification of a novel transforming growth factor-β (TGF-β6) gene in fish: regulation in skeletal muscle by nutritional state. BMC Mol. Biol. 11: 37. 
  52. Hassaan MS, El-Sayed AIM, Soltan MA, Iraqi MM, Goda AM, Davies SJ, et al. 2019. Partial dietary fish meal replacement with cotton seed meal and supplementation with exogenous protease alters growth, feed performance, hematological indices and associated gene expression markers (GH, IGF-I) for Nile tilapia, Oreochromis niloticus. Aquaculture 503: 282-292.  https://doi.org/10.1016/j.aquaculture.2019.01.009
  53. Shi X, Luo Z, Chen F, Wei CC, Wu K, Zhu XM, et al. 2017. Effect of fish meal replacement by Chlorella meal with dietary cellulase addition on growth performance, digestive enzymatic activities, histology and myogenic genes' expression for crucian carp Carassius auratus. Aquac. Res. 48: 3244-3256.  https://doi.org/10.1111/are.13154
  54. Brinker A. 2007. Guar gum in rainbow trout (Oncorhynchus mykiss) feed: The influence of quality and dose on stabilisation of faecal solids. Aquaculture 267: 315-327.  https://doi.org/10.1016/j.aquaculture.2007.02.037
  55. Khorrami B, Kheirandish P, Zebeli Q, Castillo-Lopez E. 2022. Variations in fecal pH and fecal particle size due to changes in dietary starch: Their potential as an on-farm tool for assessing the risk of ruminal acidosis in dairy cattle. Res. Vet. Sci. 152: 678-686.  https://doi.org/10.1016/j.rvsc.2022.10.001
  56. Amirkolaie AK, Verreth JA, Schrama JW. 2006. Effect of gelatinization degree and inclusion level of dietary starch on the characteristics of digesta and faeces in Nile tilapia (Oreochromis niloticus (L.)). Aquaculture 260: 194-205.  https://doi.org/10.1016/j.aquaculture.2006.06.039
  57. do Carmo Gominho-Rosa M, Rodrigues APO, Mattioni B, de Francisco A, Moraes G, Fracalossi DM. 2015. Comparison between the omnivorous jundia catfish (Rhamdia quelen) and Nile tilapia (Oreochromis niloticus) on the utilization of dietary starch sources: Digestibility, enzyme activity and starch microstructure. Aquaculture 435: 92-99  https://doi.org/10.1016/j.aquaculture.2014.09.035
  58. Welker TL, Liu K, Overturf K, Abernathy J, Barrows FT. 2021. Effect of soy protein products and gum inclusion in feed on fecal particle size profile of rainbow trout. Aquac. J. 1: 14-25.  https://doi.org/10.3390/aquacj1010003
  59. Soltan MA. 2009. Effect of dietary fish meal replacement by poultry by-product meal with different grain source and enzyme supplementation on performance, feces recovery, body composition and nutrient balance of Nile tilapia. Pak. J. Nutr. 8: 395-407. https://doi.org/10.3923/pjn.2009.395.407