Aquaculture International

, Volume 27, Issue 2, pp 475–496 | Cite as

Intestinal microbiota of salmonids and its changes upon introduction of soy proteins to fish feed

  • Svetlana V. Kononova
  • Dmitry V. ZinchenkoEmail author
  • Tatyana A. Muranova
  • Nataliya A. Belova
  • Anatoly I. Miroshnikov


World tendency in partial substitution of fishmeal-based diet in feeding fish reared in aquaculture systems for plant proteins is caused by exhaustion of fishery resources. The use of products of fat-free soy processing in feeds has provoked troubles in salmonid health, in particular the onset of inflammation in the intestine. Numerous investigations devoted to the analysis of reasons for such negative consequences have attracted attention to the intestinal microbiota of fish. In this review, we analyze the studies on the effect of soy proteins in feed on the intestinal microbiota of salmonids.


Microbiota Salmonids Aquaculture Feeds Soy protein 



Operational taxonomic units



The research was supported by the Russian Science Foundation (project no. 16-14-00133).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval statement

The research was approved by the Ethics Commission.


  1. Abbott DW, Boraston AB (2008) Structural biology of pectin degradation by Enterobacteriaceae. Microbiol Mol Biol Rev 72(2):301–316PubMedPubMedCentralGoogle Scholar
  2. Abid A, Davies SJ, Waines P, Emery M, Castex M, Gioacchini G, Carnevali O, Bickerdike R, Romero J, Merrifield DL (2013) Dietary synbiotic application modulates Atlantic salmon (Salmo salar) intestinal microbial communities and intestinal immunity. Fish Shellfish Immun 35(6):1948–1956Google Scholar
  3. Baeverfjord G, Krogdahl Å (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(5):375–387Google Scholar
  4. Bakke AM, Chikwati EM, Venold FF, Sahlman C, Holm H, Penn MH, Oropeza-Moe M, Krogdahl Å (2014) Bile enhances glucose uptake, reduces permeability, and modulates effects of lectins, trypsin inhibitors and saponins on intestinal tissue. Comp Biochem Physiol A Mol Integr Physiol 168:96–109PubMedGoogle Scholar
  5. Bakke I, Coward E, Andersen T, Vadstein O (2015) Selection in the host structures the microbiota associated with developing cod larvae (Gadus morhua). Environ Microbiol 17(10):3914–3924PubMedGoogle Scholar
  6. Bakke-McKellep AM, Penn MH, Salas PM, Refstie S, Sperstad S, Ringø E, Krogdahl Å (2007) 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.). Brit J Nutr 97(4):699–713PubMedGoogle Scholar
  7. Barnes ME, Brown ML, Bruce T, Sindelar S, Neiger R (2014) Rainbow trout rearing performance, intestinal morphology, and immune response after long-term feeding of high levels of fermented soybean meal. N Am J Aquac 76(4):333–345Google Scholar
  8. Bøgwald J, Dalmo RA (2014) Gastrointestinal pathogenesis in aquatic animals. In: Merrifield DL, Ringo E (eds) Aquaculture nutrition: gut health, probiotics and prebiotics. Wiley-Blackwell, NJ, pp 53–74Google Scholar
  9. Björnsson BT, Stefansson SO, McCormick SD (2011) Environmental endocrinology of salmon smoltification. Gen Comp Endocrinol 170(2):290–298PubMedGoogle Scholar
  10. Bolnick DI, Snowberg LK, Caporaso JG, Lauber C, Knight R, Stutz WE (2014) Major histocompatibility complex class IIb polymorphism influences gut microbiota composition and diversity. Mol Ecol 23919:4831–4845Google Scholar
  11. Boyd JM, Dacanay A, Knickle LC, Touhami A, Brown LL, Jericho MH, Johnson SC, Reith M (2008) Contribution of type IV pili to the virulence of Aeromonas salmonicida subsp. salmonicida in Atlantic salmon (Salmo salar L.). Infect Immun 76(4):1445–1455PubMedPubMedCentralGoogle Scholar
  12. Choct M, Dersjant-Li Y, McLeish J, Peisker M (2010) Soy oligosaccharides and soluble non-starch polysaccharides: a review of digestion, nutritive and anti-nutritive effects in pigs and poultry. Asian-Australas J Anim Sci 23(10):1386–1398Google Scholar
  13. Clements KD, Angert ER, Montgomery WL, Choat JH (2014) Intestinal microbiota in fishes: what's known and what's not. Mol Ecol 23(8):1891–1898PubMedGoogle Scholar
  14. Cockburn DW, Koropatkin NM (2016) Polysaccharide degradation by the intestinal microbiota and its influence on human health and disease. J Mol Biol 428(16):3230–3252PubMedGoogle Scholar
  15. Dai D, Nanthakumar NN, Savidge TC, Newburg DS, Walker WA (2002) Region-specific ontogeny of α-2,6-sialyltransferase during normal and cortisone-induced maturation in mouse intestine. Am J Physiol Gastrointest Liver Physiol 282(3):G480–G490PubMedGoogle Scholar
  16. Dale OB, Tørud B, Kvellestad A, Koppang HS, Koppang EO (2009) From chronic feed-induced intestinal inflammation to adenocarcinoma with metastases in salmonid fish. Cancer Res 69(10):4355–4362PubMedGoogle Scholar
  17. Dehler CE, Secombes CJ, Martin SA (2017a) Environmental and physiological factors shape the gut microbiota of Atlantic salmon parr (Salmo salar L.). Aquaculture 467:149–157PubMedPubMedCentralGoogle Scholar
  18. Dehler CE, Secombes CJ, Martin SA (2017b) Seawater transfer alters the intestinal microbiota profiles of Atlantic salmon (Salmo salar L.). Sci Rep 7:13877. PubMedPubMedCentralGoogle Scholar
  19. Desai AR, Links MG, Collins SA, Mansfield GS, Drew MD, Van Kessel AG, Hill JE (2012) Effects of plant-based diets on the distal gut microbiome of rainbow trout (Oncorhynchus mykiss). Aquaculture 350:134–142Google Scholar
  20. FAO (2016) The state of world fisheries and aquaculture 2016—FAO
  21. Fuente MDL, Miranda CD, Jopia P, González-Rocha G, Guiliani N, Sossa K, Urrutia H (2015) Growth inhibition of bacterial fish pathogens and quorum-sensing blocking by bacteria recovered from Chilean salmonid farms. J Aquac Anim Health 27(2):112–122Google Scholar
  22. Gajardo K, Jaramillo-Torres A, Kortner TM, Merrifield DL, Tinsley J, Bakke AM, Krogdahl Å (2017) Alternative protein sources in the diet modulate microbiota and functionality in the distal intestine of Atlantic salmon (Salmo salar). Appl Environ Microbiol 83(5):e02615–e02616PubMedPubMedCentralGoogle Scholar
  23. Ganguly S, Prasad A (2012) Microflora in fish digestive tract plays significant role in digestion and metabolism. Rev Fish Biol Fish 22(1):11–16Google Scholar
  24. Gomez D, Sunyer JO, Salinas I (2013) The mucosal immune system of fish: the evolution of tolerating commensals while fighting pathogens. Fish Shellfish Immun 35(6):1729–1739Google Scholar
  25. Green TJ, Smullen R, Barnes AC (2013) Dietary soybean protein concentrate-induced intestinal disorder in marine farmed Atlantic salmon, Salmo salar is associated with alterations in gut microbiota. Vet Microbiol 166(1–2):286–292PubMedGoogle Scholar
  26. Hartviksen M, Vecino JLG, Ringø E, Bakke AM, Wadsworth S, Krogdahl Å, Ruohonen K, Kettunen A (2014) Alternative dietary protein sources for Atlantic salmon (Salmo salar L.) effect on intestinal microbiota, intestinal and liver histology and growth. Aquac Nutr 20(4):381–398Google Scholar
  27. Heikkinen J, Vielma J, Kemiläinen O, Tiirola M, Eskelinen P, Kiuru T, Navia-Paldanius A, von Wright A (2006) Effects of soybean meal based diet on growth performance, gut histopathology and intestinal microbiota of juvenile rainbow trout (Oncorhynchus mykiss). Aquaculture 261(1):259–268Google Scholar
  28. Hemre GI, Mommsen TP, Krogdahl Å (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8(3):175–194Google Scholar
  29. Hemre GI, Sandnes K, Lie Ø, Torrissen O, Waagbø R (1995) Carbohydrate nutrition in Atlantic salmon, Salmo salar L.: growth and feed utilization. Aquac Res 26(3):149–154Google Scholar
  30. Hooper LV, Gordon JI (2001) Glycans as legislators of host–microbial interactions: spanning the spectrum from symbiosis to pathogenicity. Glycobiology 11(2):1R–10RPubMedGoogle Scholar
  31. Hovda MB, Lunestad BT, Fontanillas R, Rosnes JT (2007) Molecular characterisation of the intestinal microbiota of farmed Atlantic salmon (Salmo salar L.). Aquaculture 272(1–4):581–588Google Scholar
  32. Ingerslev HC, von Gersdorff Jørgensen L, Strube ML, Larsen N, Dalsgaard I, Boye M, Madsen L (2014) The development of the gut microbiota in rainbow trout (Oncorhynchus mykiss) is affected by first feeding and diet type. Aquaculture 424:24–34Google Scholar
  33. Janda JM, Abbott SL (2010) The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin Microbiol Rev 23(1):35–73PubMedPubMedCentralGoogle Scholar
  34. Jin C, Padra JT, Sundell K, Sundh H, Karlsson NG, Lindén SK (2015) Atlantic salmon carries a range of novel O-glycan structures differentially localized on skin and intestinal mucins. J Proteome Res 14(8):3239–3251PubMedGoogle Scholar
  35. Kapetanović D, Kurtović B, Teskeredžić E (2005) Differences in bacterial population in rainbow trout (Oncorhynchus mykiss Walbum) fry after transfer from incubator to pools. Food Technol Biotechnol 43(2):189–193Google Scholar
  36. Kaushik SJ, Seiliez I (2010) Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs. Aquac Res 41(3):322–332Google Scholar
  37. Kazakov AE, Rodionov DA, Alm E, Arkin AP, Dubchak I, Gelfand MS (2009) Comparative genomics of regulation of fatty acid and branched-chain amino acid utilization in Proteobacteria. J Bacteriol 191(1):52–64PubMedGoogle Scholar
  38. Knudsen D, Røn Ø, Baardsen G, Smedsgaard J, Koppe W, Frøkiær H (2006) Soyasaponins resist extrusion cooking and are not degraded during gut passage in Atlantic salmon (Salmo salar L.). J Agric Food Chem 54(17):6428–6435PubMedGoogle Scholar
  39. Korkea-Aho TL, Papadopoulou A, Heikkinen J, Von Wright A, Adams A, Austin B, Thompson KD (2012) Pseudomonas M162 confers protection against rainbow trout fry syndrome by stimulating immunity. J Appl Microbiol 113(1):24–35PubMedGoogle Scholar
  40. Krogdahl A, Bakke-McKellep AM, Roed KH, Baeverfjord G (2000) Feeding Atlantic salmon Salmo salar L. soybean products: effects on disease resistance (furunculosis), and lysozyme and IgM levels in the intestinal mucosa. Aquac Nutr 6(2):77–84Google Scholar
  41. Krogdahl Å, Nordrum S, Sorensen M, Brudeseth L, Rosjo C (1999) Effects of diet composition on apparent nutrient absorption along the intestinal tract and of subsequent fasting on mucosal disaccharidase activities and plasma nutrient concentration in Atlantic salmon Salmo salar L. Aquac Nutr 5(2):121–134Google Scholar
  42. Krogdahl Å, Penn M, Thorsen J, Refstie S, Bakke AM (2010) Important antinutrients in plant feedstuffs for aquaculture: an update on recent findings regarding responses in salmonids. Aquac Res 41(3):333–344Google Scholar
  43. Krogdahl Å, Sundby A, Holm H (2015) Characteristics of digestive processes in Atlantic salmon (Salmo salar). Enzyme pH optima, chyme pH, and enzyme activities. Aquaculture 449:27–36Google Scholar
  44. Krogdahl Å, Sundby A, Olli JJ (2004) Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss) digest and metabolize nutrients differently. Effects of water salinity and dietary starch level. Aquaculture 229(1–4):335–360Google Scholar
  45. Kuz’mina VV, Skvortsova EG, Shalygin MV, Kovalenko KE (2015) Role of peptidases of the intestinal microflora and prey in temperature adaptations of the digestive system in planktivorous and benthivorous fish. Fish Physiol Biochem 41(6):1359–1368PubMedGoogle Scholar
  46. Li X, Yu Y, Feng W, Yan Q, Gong Y (2012) Host species as a strong determinant of the intestinal microbiota of fish larvae. J Microbiol 50(1):29–37PubMedGoogle Scholar
  47. Liu H, Guo X, Gooneratne R, Lai R, Zeng C, Zhan F, Wang W (2016) The gut microbiome and degradation enzyme activity of wild freshwater fishes influenced by their trophic levels. Sci Rep 6:24340. PubMedPubMedCentralGoogle Scholar
  48. Llewellyn M, Boutin S, Hoseinifar SH, Derome N (2014) Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries. Front Microbiol 5:207. PubMedPubMedCentralGoogle Scholar
  49. Llewellyn MS, McGinnity P, Dionne M, Letourneau J, Thonier F, Carvalho GR, Creer S, Derome N (2016) The biogeography of the Atlantic salmon (Salmo salar) gut microbiome. ISME J 10(5):1280–1284PubMedGoogle Scholar
  50. Lyons PP, Turnbull JF, Dawson KA, Crumlish M (2017) Phylogenetic and functional characterization of the distal intestinal microbiome of rainbow trout Oncorhynchus mykiss from both farm and aquarium settings. J Appl Microbiol 122(2):347–363PubMedGoogle Scholar
  51. Medvedova L, Knopp J, Farkas R (2003) Steroid regulation of terminal protein glycosyltransferase genes: molecular and functional homologies within sialyltransferase and fucosyltransferase families. Endocr Regul 37(4):203–210PubMedGoogle Scholar
  52. Merrifield DL, Rodiles A (2015) The fish microbiome and its interactions with mucosal tissues. In: Beck BH, Peatman E (eds) Mucosal health in aquaculture. Acad Press, London, pp 273–295Google Scholar
  53. Merrifield DL, Dimitroglou A, Bradley G, Baker RTM, Davies SJ (2009) Soybean meal alters autochthonous microbial populations, microvilli morphology and compromises intestinal enterocyte integrity of rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 32(9):755–766PubMedGoogle Scholar
  54. Mountfort DO, Campbell J, Clements KD (2002) Hindgut fermentation in three species of marine herbivorous fish. Appl Environ Microbiol 68(3):1374–1380PubMedPubMedCentralGoogle Scholar
  55. Namba A, Mano N, Hirose H (2007) Phylogenetic analysis of intestinal bacteria and their adhesive capability in relation to the intestinal mucus of carp. J Appl Microbiol 102(5):1307–1317PubMedGoogle Scholar
  56. Navarrete P, Espejo RT, Romero J (2009) Molecular analysis of microbiota along the digestive tract of juvenile Atlantic salmon (Salmo salar L.). Microb Ecol 57(5):550. PubMedGoogle Scholar
  57. Navarrete P, Fuentes P, la Fuente L, Barros L, Magne F, Opazo R, Ibacache C, Espejo R, Romero J (2013) Short-term effects of dietary soybean meal and lactic acid bacteria on the intestinal morphology and microbiota of Atlantic salmon (Salmo salar). Aquac Nutr 19(5):827–836Google Scholar
  58. Navarrete P, Magne F, Araneda C, Fuentes P, Barros L, Opazo R, Espejo R, Romero J (2012) PCR-TTGE analysis of 16S rRNA from rainbow trout (Oncorhynchus mykiss) gut microbiota reveals host-specific communities of active bacteria. PLoS One 7(2):e31335. PubMedPubMedCentralGoogle Scholar
  59. Nayak SK (2010) Role of gastrointestinal microbiota in fish. Aquac Res 41(11):1553–1573Google Scholar
  60. Nishinari K, Fang Y, Guo S, Phillips GO (2014) Soy proteins: a review on composition, aggregation and emulsification. Food Hydrocoll 39:301–318Google Scholar
  61. Nordrum S, Bakke-McKellep AM, Krogdahl Å, Buddington RK (2000) Effects of soybean meal and salinity on intestinal transport of nutrients in Atlantic salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B Biochem Mol Biol 125(3):317–335PubMedGoogle Scholar
  62. Padra JT, Sundh H, Jin C, Karlsson NG, Sundell K, Lindén SK (2014) Aeromonas salmonicida binds differentially to mucins isolated from skin and intestinal regions of Atlantic salmon in an N-acetylneuraminic acid-dependent manner. Infect Immun 82(12):5235–5245PubMedPubMedCentralGoogle Scholar
  63. Pedrolli DB, Monteiro AC, Gomes E, Carmona EC (2009) Pectin and pectinases: production, characterization and industrial application of microbial pectinolytic enzymes. Open Biotechnol J 3:9–18Google Scholar
  64. Pérez T, Balcázar JL, Ruiz-Zarzuela I, Halaihel N, Vendrell D, De Blas I, Múzquiz JL (2010) Host–microbiota interactions within the fish intestinal ecosystem. Mucosal Immunol 3(4):355–360PubMedGoogle Scholar
  65. Ray AK, Ghosh K, Ringø E (2012) Enzyme-producing bacteria isolated from fish gut: a review. Aquac Nutr 18(5):465–492Google Scholar
  66. Reveco FE, Øverland M, Romarheim OH, Mydland LT (2014) Intestinal bacterial community structure differs between healthy and inflamed intestines in Atlantic salmon (Salmo salar L.). Aquaculture 420:262–269Google Scholar
  67. Ringø E, Hemre GI, Amlund H, Aursand M, Bakke-McKellep AM, Olsen RE, Svihus B (2009) Criteria for safe use of plant ingredients in diets for aquacultured fish. In: Opinion of the panel on animal feed of the Norwegian Scientific Committee for Food Safety, VKM, Oslo, pp 1–172Google Scholar
  68. Roberts SD, Powell MD (2005) The viscosity and glycoprotein biochemistry of salmonid mucus varies with species, salinity and the presence of amoebic gill disease. Comp Biochem Physiol B Biochem Mol Biol 175(1):1–11Google Scholar
  69. Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM, Guillemin K, Rawls JF (2011) Evidence for a core gut microbiota in the zebrafish. ISME J 5:1595–1608PubMedPubMedCentralGoogle Scholar
  70. Romero J, Ringø E, Merrifield DL (2014) The gut microbiota of fish. In: Merrifield DL, Ringo E (eds) Aquaculture nutrition: gut health, probiotics and prebiotics. Wiley & Sons Ltd, Chichester, pp 75–100Google Scholar
  71. Rudi K, Angell IL, Pope PB, Vik JO, Sandve SR, Snipen LG (2018) Stable core gut microbiota across the freshwater-to-saltwater transition for farmed Atlantic salmon. Appl Environ Microbiol 84(2):e01974–e02017PubMedPubMedCentralGoogle Scholar
  72. Sahlmann C, Gu J, Kortner TM, Lein I, Krogdahl Å, Bakke AM (2015) Ontogeny of the digestive system of Atlantic salmon (Salmo salar L.) and effects of soybean meal from start-feeding. PLoS One 10:e0124179. PubMedPubMedCentralGoogle Scholar
  73. Sahlmann C, Sutherland BJ, Kortner TM, Koop BF, Krogdahl Å, Bakke AM (2013) Early response of gene expression in the distal intestine of Atlantic salmon (Salmo salar L.) during the development of soybean meal induced enteritis. Fish Shellfish Immun 34(2):599–609Google Scholar
  74. Smith TB, Wahl DH, Mackie RI (1996) Volatile fatty acids and anaerobic fermentation in temperate piscivorous and omnivorous freshwater fish. J Fish Biol 48(5):829–841Google Scholar
  75. Spanggaard B, Huber I, Nielsen J, Nielsen T, Appel KF, Gram L (2000) The microflora of rainbow trout intestine: a comparison of traditional and molecular identification. Aquaculture 182:1–15Google Scholar
  76. Stephens WZ, Burns AR, Stagaman K, Wong S, Rawls JF, Guillemin K, Bohannan BJ (2016) The composition of the zebrafish intestinal microbial community varies across development. ISME J 10:644–655PubMedGoogle Scholar
  77. Sullam KE, Essinger SD, Lozupone CA, O’Connor MP, Rosen GL, Knight ROB, Kilham SS, Russell JA (2012) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol Ecol 21(13):3363–3378PubMedGoogle Scholar
  78. Taliercio E, Loveless T, Turano MJ (2015) Identification of epitopes of the A1aBx and A5A4B3 subunits of glycinin antigenic in three animal species. Food Agric Immunol 26(2):271–281Google Scholar
  79. Taliercio E, Loveless TM, Turano MJ, Kim SW (2014) Identification of epitopes of the β subunit of soybean β-conglycinin that are antigenic in pigs, dogs, rabbits and fish. J Sci Food Agric 94(11):2289–2294PubMedGoogle Scholar
  80. Vadstein O, Bergh Ø, Gatesoupe FJ, Galindo-Villegas J, Mulero V, Picchietti S, Scapigliati G, Makridis P, Olsen Y, Dierckens K, Defoirdt T, Boon N, De Schryver P, Bossier P (2013) Microbiology and immunology of fish larvae. Rev Aquac 5:S1–S25Google Scholar
  81. Van den Abbeele P, Van de Wiele T, Verstraete W, Possemiers S (2011) The host selects mucosal and luminal associations of coevolved gut microorganisms: a novel concept. FEMS Microbiol Rev 35(4):681–704PubMedGoogle Scholar
  82. Wang AR, Ran C, Ringø E, Zhou ZG (2017a) Progress in fish gastrointestinal microbiota research. Rev Aquac.
  83. Wang C, Sun G, Li S, Li X, Liu Y (2017b) Intestinal microbiota of healthy and unhealthy Atlantic salmon Salmo salar L. in a recirculating aquaculture system. Chin J Oceanol Limnol.
  84. Wilkins LG, Fumagalli L, Wedekind C (2016) Effects of host genetics and environment on egg-associated microbiotas in brown trout (Salmo trutta). Mol Ecol 25(19):4930–4945PubMedGoogle Scholar
  85. Willmott ME, Clements KD, Wells RM (2005) The influence of diet and gastrointestinal fermentation on key enzymes of substrate utilization in marine teleost fishes. J Exp Mar Biol Ecol 317(1):97–108Google Scholar
  86. Wong JM, De Souza R, Kendall CW, Emam A, Jenkins DJ (2006) Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 40(3):235–243PubMedGoogle Scholar
  87. Wong S, Rawls JF (2012) Intestinal microbiota composition in fishes is influenced by host ecology and environment. Mol Ecol 21(13):3100–3102PubMedPubMedCentralGoogle Scholar
  88. Wong S, Waldrop T, Summerfelt S, Davidson J, Barrows F, Kenney PB, Welch T, Wiens GD, Snekvik K, Rawls JF (2013) Aquacultured rainbow trout (Oncorhynchus mykiss) possess a large core intestinal microbiota that is resistant to variation in diet and rearing density. Appl Environ Microbiol 79(16):4974–4984PubMedPubMedCentralGoogle Scholar
  89. Yamamoto T, Iwashita Y, Matsunari H, Sugita T, Furuita H, Akimoto A, Okamatsu K, Suzuki N (2010) Influence of fermentation conditions for soybean meal in a non-fish meal diet on the growth performance and physiological condition of rainbow trout Oncorhynchus mykiss. Aquaculture 309(1–4):173–180Google Scholar
  90. Yan Q, Li J, Yu Y, Wang J, He Z, Van Nostrand JD, Kempher ML, Wu L, Wang Y, Liao L, Li X, Wu S, Ni J, Wang C, Zhou J (2016) Environmental filtering decreases with fish development for the assembly of gut microbiota. Environ Microbiol 18(2):4739–4754PubMedGoogle Scholar
  91. Yang Y, Wang Z, Wang R, Sui X, Qi B, Han F, Li Y, Jiang L (2016) Secondary structure and subunit composition of soy protein in vitro digested by pepsin and its relation with digestibility. Biomed Res Int.
  92. Zhang JX, Guo LY, Feng L, Jiang WD, Kuang SY, Liu Y, Hu K, Jiang J, Li SH, Tang L, Zhou XQ (2013) Soybean β-conglycinin induces inflammation and oxidation and causes dysfunction of intestinal digestion and absorption in fish. PLoS One 8:e58115. PubMedPubMedCentralGoogle Scholar
  93. Zhou Z, Ringø E, Olsen RE, Song SK (2018) Dietary effects of soybean products on gut microbiota and immunity of aquatic animals: a review. Aquac Nutr 24(1):644–665Google Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Institute of Protein ResearchRussian Academy of SciencesPushchinoRussia
  2. 2.Faculty of BiotechnologyMoscow State UniversityMoscowRussia

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