Fisheries Science

, Volume 84, Issue 3, pp 523–533 | Cite as

Galactooligosaccharide and a combination of yeast and β-glucan supplements enhance growth and improve intestinal condition in striped catfish Pangasianodon hypophthalmus fed soybean meal diets

  • Amalia SutrianaEmail author
  • Roshada Hashim
  • Mst. Nahid Akter
  • Siti Azizah Mohd Nor
Original Article Aquaculture


The effects of galactooligosaccharide (GOS) and a combination of yeast and β-glucan (YβG) supplementation of dietary soybean meal (SBM) on the growth and digestive performance of striped catfish Pangasianodon hypophthalmus were evaluated. Four isonitrogenous (30% protein) and isocaloric (19 MJ/kg diet) diets were formulated to contain 100% fish meal (FM) protein, 55% FM protein/45% SBM protein, FM-SBM supplemented with 1% GOS, and a combination of 1% yeast and 0.1% β-glucan, respectively. Each diet was fed for 12 weeks to three groups of 30 striped catfish fingerlings (average weight 16.45 ± 0.07 g) maintained in circular fiberglass tanks (600 l). Growth, feed utilization, and muscle protein composition of fish improved significantly after supplementation with either GOS or YβG compared to the unsupplemented SBM diet, but were similar to those of fish fed the FM diet. Nutrient digestibility, digestive enzyme activities, villi and microvilli length were significantly increased in fish fed the supplemented SBM diets. The gut microbiota ranking profile showed that supplementing the SBM diet with YβG and GOS gave a ranking of Verrucomicrobia, Spirochaetes, Bacteriodetes, and Actinobacteria phyla similar to that of the FM diet. Thus, diet containing 45% protein from soybean supplemented with either GOS or YβG can be recommended to improve the growth and digestive performance of striped catfish.


Fish performance Nutrient digestibility Digestive enzyme Villi Gut microbiota 



Thanks are due to technical staff at the School of Biological Sciences, Universiti Sains Malaysia. We are grateful to Friesland Foods for supplying Vivinal GOS and to Biorigin, Macrogard for the β-glucan. This study was supported by the Malaysian Ministry of Higher Education ERGS grant no. 203/PBIOLOGY/6730134.


  1. Abu-Elala N, Marzouk M, Moustafa M (2013) Use of different Saccharomyces cerevisiae biotic forms as immune-modulator and growth promoter for Oreochromis niloticus challenged with some fish pathogens. Int J Vet Sci Med 1:21–29CrossRefGoogle Scholar
  2. Akter MN, Sutriana A, Talpur AD, Hashim R (2015) Dietary supplementation with mannan oligosaccharide influences growth, digestive enzymes, gut morphology, and microbiota in juvenile striped catfish, Pangasianodon hypophthalmus. Aquac Int. Google Scholar
  3. Anguiano M, Pholenz C, Buentello A, Gatlin DM III (2013) The effects of prebiotics on the digestive enzymes and gut histomorphology of red drum (Sciaenops ocellatus) and hybrid striped bass (Morone chrysops × M. saxatilis). Br J Nutr 109:625–629CrossRefGoogle Scholar
  4. Association of Official Analytical Chemists (AOAC) (1997) Association of Official Analytical Chemists. Official Methods of Analysis of AOAC International, 16th edn, vol 1. AOAC, Arlington, VAGoogle Scholar
  5. Askarian F, Kousha A, Salma W, Ringø E (2011) The effect of lactic acid bacteria administration on growth, digestive enzymes activity and gut microbiota in Persian sturgeon (Acipenser persicus) and beluga (Huso huso) fry. Aquac Nutr 17:488–497CrossRefGoogle Scholar
  6. Backhed F (2011) Programming of host metabolism by the gut microbiota. Ann Nutr Metab 58:44–52CrossRefPubMedGoogle Scholar
  7. Baeverfjord G, Krogdahl A (1996) Development and regression of soybean meal induced enteritis in Atlantic salmon, Salmo salar L., distal intestine: a comparison with the intestines of fasted fish. J Fish Dis 19:375–387CrossRefGoogle Scholar
  8. Bakke-McKellep AM, Press CM, Baeverfjord G, Krogdahl A, Landsverk T (2000) Changes in immune and enzyme histochemical phenotypes of cells in the intestinal mucosa of Atlantic salmon, Salmo salar L., with soybean meal-induced enteritis. J Fish Dis 23:115–127CrossRefGoogle Scholar
  9. Bier M (1955) Lipases. Methods in enzymology. I. Academic Press, New YorkGoogle Scholar
  10. Bindels LB, Delzenne NM, Cani PD, Walter J (2015) Towards a more comprehensive concept for prebiotics. Nat Rev Gastroenterol Hepatol 12:303–310CrossRefPubMedGoogle Scholar
  11. Biswas KA, Kaku H, Ji SC, Seoka M, Takii K (2007) Use of soybean meal and phytase for partial replacement of fish meal in the diet of red sea bream, Pagrus major. Aquaculture 267:284–291CrossRefGoogle Scholar
  12. Blumberg R, Powrie F (2012) Microbiota, disease, and back to health: a metastable journey. Sci Transl Med 4(13rv7):1377. Google Scholar
  13. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  14. Buentello JA, Neill WH, Gatlin DM III (2010) Effects of dietary prebiotics on the growth, feed efficiency and non-specific immunity of juvenile red drum (Sciaenops ocellatus) fed soybean based diets. Aquac Res 41:411–418CrossRefGoogle Scholar
  15. Burr G, Hume M, Neil WH, Gatlin DM III (2008) Effects of prebiotics on nutrient digestibility of a soybean meal based diet by red drum Sciaenops ocellatus (Linnaeus). Aquac Res 39:1680–1686Google Scholar
  16. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J6:1621–1624CrossRefGoogle Scholar
  17. Clavel T, Desmarchelier C, Haller D, Gérard P, Rohn S, Lepage P, Daniel H (2014) Intestinal microbiota in metabolic diseases: from bacterial community structure and functions to species of pathophysiological relevance. Gut Microbes 5(4):544–551CrossRefPubMedGoogle Scholar
  18. Daniels CL, Merrifield DL, Boothroyd DP, Davies SJ, Factor JR, Arnold KE (2010) Effect of dietary Bacillus spp. and mannan oligosaccharides (MOS) on European lobster (Homarus gammarus L.) larvae growth performance, gut morphology and gut microbiota. Aquaculture 304:49–57CrossRefGoogle Scholar
  19. Denev S, Staykov Y, Moutafchieva R, Beev G (2009) Microbial ecology of the gastrointestinal tract of fish and the potential application of probiotics and prebiotics in finfish aquaculture. Int Aquat Res 1(1):1–29Google Scholar
  20. Dimitroglou A, Merrifield DL, Moate R, Davies SJ, Spring P, Sweetman J, Bradley G (2009) Dietary mannan oligosaccharide supplementation modulates intestinal microbial ecology and improves gut morphology of rainbow trout, Oncorhynchus mykiss (Walbaun). J Anim Sci 87:3226–3234CrossRefPubMedGoogle Scholar
  21. Dimitroglou A, Reynolds P, Ravnoy B, Johnsen F, Sweetman JW, Johansen J, Davies SJ (2011) The effect of mannan oligosaccharide supplementation on Atlantic salmon smolts (Salmo salar L.) fed diets with high levels of plant proteins. J Aquac Res. Google Scholar
  22. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509PubMedGoogle Scholar
  23. Furukawa A, Tsukuhara H (1966) On the acid digestion method for determination of chromic oxide as an index substance in the study of digestibility of fish feed. Bull Jpn Soc Sci Fish 32:502–506CrossRefGoogle Scholar
  24. Ganesh BP, Klopfleisch R, Loh G, Blaut M (2013) Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella typhimurium infected gnotobiotic mice. PLoS One 8(9):e74963. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Geraylou Z, Souffreau C, Rurangwa E, Maes GE, Spanier KI, Courtin CM, Delcour JA, Buyse J, Ollevier F (2013) Prebiotic effects of arabinoxylan oligosaccharides on juvenile Siberian sturgeon (Acipenser baerii) with emphasis on the modulation of the gut microbiota using 454 pyrosequencing. FEMS Microbiol Ecol 86:357–371CrossRefPubMedGoogle Scholar
  26. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359CrossRefPubMedPubMedCentralGoogle Scholar
  27. Greiner T, Backhed F (2011) Effects of the gut microbiota on obesity and glucose homeostasis. Trends Endocrinol Metab 22:117–123CrossRefPubMedGoogle Scholar
  28. Grisdale-Helland B, Helland SJ, Gatlin DM (2008) The effects of dietary supplementation with mannanoligosaccharide, fructooligosaccharide or galactooligosaccharide on the growth and feed utilization of Atlantic salmon (Salmo salar). Aquaculture 283:163–167CrossRefGoogle Scholar
  29. Gullian M, Thompson F, Rodriguez J (2004) Selection of probiotic bacteria and study of their immunostimulatory effect in Penaus vannamei. Aquaculture 233:1–4CrossRefGoogle Scholar
  30. Hoseinifar SH, Khalili M, Rostami HK, Esteban MA (2013) Dietary galactooligosaccharide affects intestinal microbiota, stress resistance, and performance of Caspian roach (Rutilus rutilus) fry. Fish Shellfish Immunol 35:1416–1420CrossRefPubMedGoogle Scholar
  31. Irianto A, Austin B (2002) Probiotics in aquaculture. J Fish Dis 25:633–642CrossRefGoogle Scholar
  32. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI (2011) Human nutrition, the gut microbiome and the immune system. Nature 474:327–336CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kim YS, Ho SB (2010) Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep 12:319–330CrossRefPubMedPubMedCentralGoogle Scholar
  34. Krogdahl A, Bakke-McKellep AM, Baeverfjord G (2003) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.). Aquac Nutr 9:361–371CrossRefGoogle Scholar
  35. 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 98:279–289CrossRefGoogle Scholar
  36. Lewis PR, Knight DP (1977) Staining methods for sectioned material. In: Glauert AM (ed) Practical methods in electron microscopy, vol 5. Elsevier/North Holland Biomedical Press, AmsterdamGoogle Scholar
  37. Li P, Gatlin DM III (2005) Evaluation of the prebiotic Grobiotic-A and brewer’s yeast as dietary supplements for sub-adult hybrid striped bass (Morone chrysops × M. Saxatilis) challenged in situ with Mycobacterium marinum. Aquaculture 248:197–205CrossRefGoogle Scholar
  38. Merrifield DL, Harper GM, Mustafa S, Carnevali O, Picchietti S, Davies SJ (2011) Effect of dietary alginic acid on juvenile tilapia (Oreochromis niloticus) intestinal microbial balance, intestinal histology and growth performance. Cell Tissue Res 344:135–146CrossRefPubMedGoogle Scholar
  39. Oliva-Teles A, Gouveia A, Gomes E, Rema P (1994) The effect of different processing treatments on soybean meal utilization by rainbow trout, Oncorhynchus mykiss. Aquaculture 124:343–349CrossRefGoogle Scholar
  40. Phumee P, Wei WY, Ramachandran S, Hashim R (2011) Evaluation of soybean meal in the formulated diets for juvenile Pangasianodon hypophthalmus (Sauvage, 1878). Aquac Nutr 17:214–222CrossRefGoogle Scholar
  41. Piccolo G, Centoducati G, Bovera F, Marrone R, Nizza A (2013) Effects of mannan oligosaccharide and inulin on sharpsnout seabream (Diplodus puntazzo) in the context of partial fish meal substitution by soybean meal. Ital J Anim Sci 12:133–138CrossRefGoogle Scholar
  42. Png CW, Linden SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, McGuckin MA, Florin THJ (2010) Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol 105:2420–2428CrossRefPubMedGoogle Scholar
  43. Refstie S, Storebakken T, Roem AJ (1998) Feed consumption and conversion in Atlantic salmon (Salmo salar) fed diets with fish meal, extracted soybean meal or soybean meal with reduced content of oligosaccharides, trypsin inhibitors, lectins and soya antigens. Aquaculture 162:301–312CrossRefGoogle Scholar
  44. Ringø E, Gatesoupe FJ (1998) Lactic acid bacteria in fish: a review. Aquaculture 160:177–203CrossRefGoogle Scholar
  45. Ringø E, Olsen RE, Gifstad TØ, Dalmo RA, Amlund H, Hemre GI, Bakke AM (2010) Prebiotics in aquaculture: a review. Aquac Nutr 16:117–136CrossRefGoogle Scholar
  46. Rumsey GL, Siwicki AK, Anderson DP, Bowser PR (1994) Effect of soybean protein on serological response, non-specific defense mechanisms, growth, and protein utilization in rainbow trout. Vet Immunol Immunopathol 41:323–339CrossRefPubMedGoogle Scholar
  47. Sang HM, Fotedar R (2010) Effects of mannan oligosaccharide dietary supplementation on performances of the tropical spiny lobster juvenile (Panulirus ornatus). Fish Shellfish Immunol 28:483–489CrossRefPubMedGoogle Scholar
  48. Sealey WM, Barrows FT, Smith CE, Hardy RW (2010) Dietary supplementation strategies to improve performance of rainbow trout Oncorhynchus mykiss fed plant-based diets. Bull FRA 31:15–23Google Scholar
  49. Smith CJ, Rocha ER, Paster BJ (2006) The medically important Bacteroides spp. in health and disease. Prokaryotes 7:38–427Google Scholar
  50. Smriga S, Sandin SA, Azam F (2010) Abundance, diversity, and activity of microbial assemblages associated with coral reef fish guts and feces. FEMS Microbiol Ecol 73:31–42PubMedGoogle Scholar
  51. Sutriana A (2017). The use of selected prebiotics and probiotic in feed development for striped catfish (Pangasianodon hypophthalmus, Sauvage, 1878) juveniles: effects on growth parameters and health status. Ph.D. dissertation, Universiti Sains Malaysia, MalaysiaGoogle Scholar
  52. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031CrossRefPubMedGoogle Scholar
  53. Uran PA, Goncalves AA, Taverne-Thiele JJ, Schrama JW, Verreth JA (2008) Soybean meal induces intestinal inflammation in common carp (Cyprinus carpio L.). Fish Shellfish Immunol 25:751–760CrossRefPubMedGoogle Scholar
  54. van den Ingh TS, Krogdahl A, Olli JJ, Hendriks HG, Koninkx JG (1991) Effects of soybean-containing diets on the proximal and distal intestines in Atlantic salmon (Salmo salar): a morphological study. Aquaculture 94:297–305CrossRefGoogle Scholar
  55. van den Ingh TSGAM, Olli JJ, Krogdahl Å (1996) Alcohol-soluble components in soybeans cause morphological changes in the distal intestine of Atlantic salmon, Salmo Salar L. J Fish Dis 19:47–53CrossRefGoogle Scholar
  56. van der Meulen R, Makras L, Verbrugghe K, Adriany T, De Vuyst L (2006) In vitro kinetic analysis of oligofructose consumption by Bacteroides and Bifidobacterium spp. indicates different degradation mechanisms. Appl Environ Microbiol 72(2):1006–1012CrossRefPubMedPubMedCentralGoogle Scholar
  57. van Kessel MAHJ, Dutilh BE, Neveling K, Kwint MP, Veltman JA, Flik G, Jetten SM, Klaren PHM, den Camp HJO (2011) Pyrosequencing of 16S rRNA gene amplicons to study the microbiota in the gastrointestinal tract of carp (Cyprinus carpio L.). AMB Express 1:41CrossRefPubMedPubMedCentralGoogle Scholar
  58. Velagapudi VR, Hezaveh R, Reigstad CS, Gopalacharyulu P, Yetukuri L (2010) The gut microbiota modulates host energy and lipid metabolism in mice. J Lipid Res 51:101–1112CrossRefGoogle Scholar
  59. Wache Y, Auffray F, Gatesoupe FJ, Zambonimo J, Gayet V, Labbe L, Quentel C (2006) Cross effect of the strain of dietary Saccharomyces cerevisiae and rearing conditions on the onset of intestinal microbiota and digestive enzymes in rainbow trout, Oncorhynchus mykiss fry. Aquaculture 258:470–478CrossRefGoogle Scholar
  60. Walter HE (1984) Proteinases: methods with hemoglobin, casein and azocoll as substrates. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol 5. Chemie, Weinheim, pp 270–277Google Scholar
  61. Worthington Enzyme Manual (1988) Alpha amylase. In: Worthington CC (ed) Enzyme and related biochemicals. Worthington Biochemical Corporation, Freehold, NJ, p 346Google Scholar
  62. Yamamoto T, Unuma T, Akiyama T (1998) Postprandial changes in plasma free amino acid concentrations of rainbow trout fed diets containing different protein sources. Fish Sci 64:474–481CrossRefGoogle Scholar
  63. Yilmaz E, Genc MA, Genc E (2007) Effects of dietary mannan oligosaccharides on growth, body composition, and intestine and liver histology of rainbow trout, Oncorhynchus mykiss. Isr J Aquac Bamidgeh 59:182–188Google Scholar
  64. Zhou QC, Buentello JA, Gatlin DM III (2010) Effects of dietary prebiotics on growth performance, immune response and intestinal morphology of red drum (Sciaenops ocellatus). Aquaculture 309:253–257CrossRefGoogle Scholar

Copyright information

© Japanese Society of Fisheries Science 2018

Authors and Affiliations

  1. 1.Faculty of Veterinary MedicineSyiah Kuala UniversityBanda AcehIndonesia
  2. 2.Faculty of Science and TechnologyUniversiti Sains Islam MalaysiaBandar Baru NilaiMalaysia
  3. 3.Faculty of FisheriesHajee Mohammad Danesh Science and Technology UniversityDinajpurBangladesh
  4. 4.Institute of Marine BiotechnologyUniversiti Malaysia TerengganuKuala TerengganuMalaysia

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