Hostname: page-component-76fb5796d-2lccl Total loading time: 0 Render date: 2024-04-27T16:35:15.638Z Has data issue: false hasContentIssue false

Biotherapeutic microbial supplementation for ameliorating fish health: developing trends in probiotics, prebiotics, and synbiotics use in finfish aquaculture

Published online by Cambridge University Press:  04 January 2023

Parul Puri
Affiliation:
Department of Biotechnology, Delhi Technological University, Delhi, India Department of Zoology, Sri Aurobindo College, University of Delhi, Delhi, India
Jai Gopal Sharma*
Affiliation:
Department of Biotechnology, Delhi Technological University, Delhi, India
Ram Singh
Affiliation:
Department of Applied Chemistry, Delhi Technological University, Delhi, India
*
Author for correspondence: Jai Gopal Sharma, E-mail: sharmajaigopal@dce.ac.in

Abstract

Nutrition demands in aquaculture can be realized through quality aquafeeds as compounded diets that contribute to the growth and health of aquaculture species. Functional additives in feed, notably probiotics, prebiotics, and their admixture synbiotics, have been recently recognized for their biotherapeutic role as immunostimulants capable of conferring disease resistance, stress tolerance, and gastrointestinal health; counteracting the negative effects of anti-nutrients, pathogenic prevalence, and antimicrobials in finfish aquaculture. Formulated diets based on probiotics, prebiotics, and as a supplemental combination for synbiotics can significantly influence fish gut microbiomes, establishing the modalities of microbial dynamics to maximize host-associated benefits. These microbial functional-feed supplements are acclaimed to be biocompatible, biodegradable, and safe for dietary consumption as well as the environment. In fed fish aquaculture, prebiotic appended probiotic diet ‘synbiotic’ has propounded larger attention for its additional health and nutritional benefits. Synbiotic, prebiotic, and probiotic usage as functional feeds for finfish aquaculture thus provides promising prospects. Developing trends in their intended application are reviewed here forth.

Type
Review Article
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abid, A, Davies, SJ, Waines, P, Emery, M, Castex, M, Gioacchini, G, Carnevali, O, Bickerdike, R, Romero, J and Merrifield, DL (2013) Dietary synbiotic application modulates Atlantic salmon (Salmo salar) intestinal microbial communities and intestinal immunity. Fish and Shellfish Immunology 35, 19481956.CrossRefGoogle ScholarPubMed
Aftabgard, M, Salarzadeh, A, Mohseni, M, Shabanipour, AHB and Zorriehzahra, MEJ (2019) The combined efficiency of dietary isomaltooligosaccharides and Bacillus spp. on the growth, hemato-serological, and intestinal microbiota indices of Caspian brown trout (Salmo trutta caspius Kessler, 1877). Probiotics and Antimicrobial Proteins 11, 198206.CrossRefGoogle ScholarPubMed
Aguilar-Toalá, JE, Garcia-Varela, R, Garcia, H, Mata-Haro, V, González-Córdova, A, Vallejo-Cordoba, B and Hernández-Mendoza, A (2018) Postbiotics: an evolving term within the functional foods field. Trends in Food Science and Technology 75, 105114.CrossRefGoogle Scholar
Akbary, P and Jahanbakhshi, A (2018) Growth yield, survival, carcass quality, haematological, biochemical parameters and innate immune responses in the grey mullet (Mugilcephalus Linneaus, 1758) fingerling induced by Immunogen® prebiotic. Journal of Applied Animal Research 46, 1016.CrossRefGoogle Scholar
Akmal, M, Rahimi-Midani, A, Hafeez-ur-Rehman, M, Hussain, A and Choi, T-J (2020) Isolation, characterization, and application of a bacteriophage infecting the fish pathogen Aeromonas hydrophila. Pathogens (Basel, Switzerland) 9, 215.Google ScholarPubMed
Akrami, R, Abdolmajid, H, Abbas, M and Abdolmohammad, AK (2009) Effect of dietary prebiotic inulin on growth performance, intestinal microflora, body composition and hematological parameters of juvenile Beluga, Huso huso (Linnaeus, 1758). Journal of the World Aquaculture Society 40, 771779.Google Scholar
Akramienė, D, Kondrotas, A, Didžiapetrienė, J and Kėvelaitis, E (2007) Effects of beta-glucans on the immune system. Medicina (Kaunas) 43, 597606.CrossRefGoogle ScholarPubMed
Ali, SSR, Ambasankar, K, Nandakumar, S, Praveena, PE and Syamadayal, J (2016) Effect of dietary prebiotic inulin on growth, body composition and gut microbiota of Asian seabass (Lates calcarifer). Animal Feed Science and Technology 217, 8794.Google Scholar
Amir, I, Zuberi, A, Kamran, M, Imran, M and Murtaza, MH (2019) Evaluation of commercial application of dietary encapsulated probiotic (Geotrichum candidum QAUGC01): effect on growth and immunological indices of rohu (Labeo rohita, Hamilton 1822) in semi-intensive culture system. Fish and Shellfish Immunology 95, 464472.CrossRefGoogle Scholar
Andersson, H, Asp, N-G, Bruce, A, Ross, S, Wadström, T and Wold, AE (2001) Health effects of probiotics and prebiotics: a literature review on human studies. Scandinavian Journal of Nutrition 45, 5875.Google Scholar
Armada, CD and Simora, RMC (2016) Isolation and identification of protease-producing Pseudomonas sp. PD14 in the gut of rabbitfish Siganus guttatus (Bloch 1787). Asian Fisheries Science 29, 8295.CrossRefGoogle Scholar
Asadian, M, Shahsavani, D and Kazerani, HR (2015) Growth promoting effects of a multi-strain probiotic on common carp (Cyprinus carpio) fingerlings. Iranian Journal of Veterinary Science and Technology 7, 6374.Google Scholar
Askarian, F, Kousha, A, Salma, W and 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. Aquaculture Nutrition 17, 488497.CrossRefGoogle Scholar
Austin, B and Austin, DA (2007) Bacterial Fish Pathogens: Disease in Farmed and Wild Fish, 4th Edn, Chichester, UK: Springer, Praxis Publishing.Google Scholar
Azevedo, RV, Filho, JCF, Pereira, SL, Cardoso, LD, Andrade Ricardo de, D and Vidal Júnior, MV (2016) Dietary mannan oligosaccharide and Bacillus subtilis in diets for Nile tilapia (Oreochromis niloticus). Acta Scientiarum. Animal Sciences 38, 347353.CrossRefGoogle Scholar
Balcazar, JL, Blas, I, Ruiz-Zarzuela, I, Cunningham, D, Vendrell, D and Múzquiz, JL (2006) The role of probiotics in aquaculture. Veterinary Microbiology 114, 173186.CrossRefGoogle ScholarPubMed
Berg, RD (1996) The indigenous gastrointestinal microflora. Trends in Microbiology 4, 430435.CrossRefGoogle ScholarPubMed
Betiku, OC, Yeoman, CJ, Gaylord, TG, Duff, GC, Hamerly, T, Bothner, B, Block, SS and Sealey, WM (2018) Differences in amino acid catabolism by gut microbes with/without prebiotics inclusion in GDDY-based diet affect feed utilization in rainbow trout. Aquaculture 490, 108119.CrossRefGoogle Scholar
Bindels, LB, Delzenne, NM, Cani, PD and Walter, J (2015) Towards a more comprehensive concept for prebiotics. Nature Reviews Gastroenterology and Hepatology 12, 303310.CrossRefGoogle Scholar
Bird, AR, Conlon, MA, Christophersen, CT and Topping, DL (2010) Resistant starch, large bowel fermentation and a broader perspective of prebiotics and probiotics. Beneficial Microbes 1, 423431.CrossRefGoogle Scholar
Blanch, A, Alsina, M, Simon, M and Jofre, J (1997) Determination of bacteria associated with reared turbot (Scophthalmus maximus) larvae. Journal of Applied Microbiology 82, 729734.CrossRefGoogle Scholar
Boonanuntanasarn, S, Ditthab, K, Jangprai, A and Nakharuthai, C (2019) Effects of microencapsulated Saccharomyces cerevisiae on growth, hematological indices, blood chemical, and immune parameters and intestinal morphology in striped catfish, Pangasianodon hypophthalmus. Probiotics and Antimicrobial Proteins 11, 427437.CrossRefGoogle ScholarPubMed
Burr, G and Gatlin, DM III (2009) Effects of the prebiotics GroBiotic®-A and inulin on the intestinal microbiota of red drum, Sciaenops ocellatus. Journal of the World Aquaculture Society 40, 440449.CrossRefGoogle Scholar
Cahill, MM (1990) Bacterial flora of fishes: a review. Microbial Ecology 19, 2141.CrossRefGoogle ScholarPubMed
Carballo, C, Pinto, PIS, Mateus, AP, Berbel, C, Guerreiro, CC, Martinez-Blanch, JF, Codoñer, FM, Mantecon, L, Power, DM and Manchado, M (2019) Yeast β-glucans and microalgal extracts modulate the immune response and gut microbiome in Senegalese sole (Solea senegalensis). Fish and Shellfish Immunology 92, 3139.CrossRefGoogle ScholarPubMed
Castillo, D and Middelboe, M (2016) Genomic diversity of bacteriophages infecting the fish pathogen Flavobacterium psychrophilum. FEMS Microbiology Letters 363, fnw272.CrossRefGoogle ScholarPubMed
Casula, G and Cutting, SM (2002) Bacillus probiotics: spore germination in the gastrointestinal tract. Applied and Environmental Microbiology 68, 23442352.CrossRefGoogle ScholarPubMed
Cerezuela, R, Cuesta, A, Meseguer, J and Esteban, MA (2008) Effects of inulin on gilthead seabream (Sparus aurata L.) innate immune parameters. Fish and Shellfish Immunology 24, 663668.CrossRefGoogle ScholarPubMed
Chandrarathna, HPSU, Nikapitiya, C, Dananjaya, SHS, De Silva, BCJ, Heo, G-J, De Zoysa, M and Lee, J (2020) Isolation and characterization of phage AHP-1 and its combined effect with chloramphenicol to control Aeromonas hydrophila. Brazilian Journal of Microbiology 51, 409416.CrossRefGoogle ScholarPubMed
Chapman, CMC, Gibson, GR and Rowland, I (2011) Health benefits of probiotics: are mixtures more effective than single strains? European Journal of Nutrition 50, 117.CrossRefGoogle ScholarPubMed
Chen, L, Yuan, S, Liu, Q, Mai, G, Yang, J, Deng, D, Zhang, B, Liu, C and Ma, Y (2018 a) In vitro design and evaluation of phage cocktails against Aeromonas salmonicida. Frontiers in Microbiology 9, 1476.CrossRefGoogle ScholarPubMed
Chen, M, Wu, Y, Yan, Q, Lv, Z, He, M, Feng, L, Zhao, J and Duan, Z (2018 b) Growth performance, lipid deposition and hepatic lipid metabolism related gene expression in Schizothorax prenanti fed with dietary acidolysis-oxidized konjac glucomannan supplementation. Journal of Aquaculture Research and Development 9, 1.Google Scholar
Chen, D-D, Yao, Y-Y, Cui, Z-W, Zhang, X-Y, Guo, X, Zhou, Y-Y and Zhang, Y-A (2019 a) Comparative study of the immunoprotective effect of two grass carp-sourced Bacillus subtilis spore-based vaccines against grass carp reovirus. Aquaculture 504, 8895.CrossRefGoogle Scholar
Chen, M, Wu, Y, Yan, Q, Zhao, J, Feng, L, He, M and Lv, Z (2019 b) Effects of dietary konjac oligosaccharide supplementation on serum immune parameters and intestinal immunity of Schizothorax prenanti. Fisheries Science 85, 157165.CrossRefGoogle Scholar
Clements, KD, Angert, ER, Montgomery, WL and Choat, JH (2014) Intestinal microbiota in fishes: what's known and what's not. Molecular Ecology 23, 18911898.CrossRefGoogle ScholarPubMed
Culot, A, Grosset, N and Gautier, M (2019) Overcoming the challenges of phage therapy for industrial aquaculture: a review. Aquaculture 513, 734423.CrossRefGoogle Scholar
Das, P, Mandal, S, Khan, A, Manna, SK and Ghosh, K (2014) Distribution of extracellular enzyme-producing bacteria in the digestive tracts of 4 brackish water fish species. Turkish Journal of Zoology 38, 7988.CrossRefGoogle Scholar
Dawood, MAO, Koshio, S, Ishikawa, M and Yokoyama, S (2015) Effects of heat killed Lactobacillus plantarum (LP20) supplemental diets on growth performance, stress resistance and immune response of red sea bream, Pagrus major. Aquaculture 442, 2936.CrossRefGoogle Scholar
Dawood, MAO, Mohamed, NE, Moustafa, EM and Mohamed, GS (2020) Synbiotic effects of Aspergillus oryzae and β-Glucan on growth and oxidative and immune responses of Nile Tilapia, Oreochromis niloticus. Probiotics and Antimicrobial Proteins 12, 172183.CrossRefGoogle ScholarPubMed
de Araújo, ERL, Barbas, LAL, Ishikawa, CM, Dias, DC, Sussel, FR, Marques, HLA and Tachibana, L (2018) Prebiotic, probiotic, and synbiotic in the diet of Nile tilapia post-larvae during the sex reversal phase. Aquaculture International 26, 8597.CrossRefGoogle Scholar
de Bruijn, I, Li, Y, Wiegertjes, GF and Raaijmakers, JM (2017) Exploring fish microbial communities to mitigate emerging diseases in aquaculture. FEMS Microbiology Ecology 94, fix161.Google Scholar
Détrée, C and Gonçalves, AT (2019) Transcriptome mining of apoptotic mechanisms in response to density and functional diets in Oncorhynchus mykiss and role in homeostatic regulation. Comparative Biochemistry and Physiology Part D Genomics Proteomics 31, 100595.CrossRefGoogle ScholarPubMed
Devi, G, Harikrishnan, R, Paray, BA, Al-Sadoon, MK, Hoseinifar, SH and Balasundaram, C (2019) Effect of symbiotic supplemented diet on innate-adaptive immune response, cytokine gene regulation and antioxidant property in Labeo rohita against Aeromonas hydrophila. Fish and Shellfish Immunology 89, 687700.CrossRefGoogle ScholarPubMed
Di, J, Chu, Z, Zhang, S, Huang, J, Du, H and Wei, Q (2019) Evaluation of the potential probiotic Bacillus subtilis isolated from two ancient sturgeons on growth performance, serum immunity and disease resistance of Acipenser dabryanus. Fish and Shellfish Immunology 93, 711719.CrossRefGoogle ScholarPubMed
Dimitroglou, A, Merrifield, DL, Carnevali, O, Picchietti, S, Avella, M, Daniels, C, Güroy, D and Davies, SJ (2011) Microbial manipulations to improve fish health and production – a Mediterranean perspective. Fish and Shellfish Immunology 30, 116.CrossRefGoogle ScholarPubMed
Djauhari, R, Widanarni, W, Sukenda, S, Suprayudi, MA and Zairin, M (2017) Application of microencapsulated synbiotic to improve the growth performance and health status of common carp (Cyprinus carpio) cultured in the ponds. Pakistan Journal of Biotechnology 14, 4347.Google Scholar
do Nascimento Veiga, PT, Owatari, MS, Nunes, AL, Rodrigues, RA, Kasai, RYD, Fernandes, CE and de Campos, CM (2020) Bacillus subtilis C-3102 improves biomass gain, innate defense and intestinal absorption surface of native Brazilian hybrid Surubim (Pseudoplatystoma corruscans×P. reticulatum). Aquaculture International 28, 11831193.CrossRefGoogle Scholar
El-Araby, DA, El-Didamony, G and Megahed, MTH (2016) New approach to use phage therapy against Aeromonas hydrophila induced motile Aeromonas septicemia in Nile Tilapia. Journal of Marine Science: Research & Development 6, 194.Google Scholar
FAO (2018) The State of World Fisheries and Aquaculture 2018-Meeting the Sustainable Development Goals. Rome: FAO.Google Scholar
FAO (2020) The State of World Fisheries and Aquaculture 2020: Sustainability in Action. Rome: FAO. Available at https://doi.org/10.4060/ca9229en.Google Scholar
FAO/WHO (2002) Report of a Joint FAO/WHO Expert Consultation on Guidelines for the Evaluation of Probiotics in Food. London, Ontario, Canada: World Health Organization and Food and Agriculture Organization of the United Nations.Google Scholar
Fehlbaum, S, Prudence, K, Kieboom, J, Heerikhuisen, M, van den Broek, T, Schuren, F, Steinert, RE and Raederstorff, D (2018) In vitro fermentation of selected prebiotics and their effects on the composition and activity of the adult gut microbiota. International Journal of Molecular Sciences 19, 3097.CrossRefGoogle ScholarPubMed
Feng, W, Zhang, J, Jakovlić, I, Xiong, F, Wu, S, Zou, H, Li, W, Li, M and Wang, G (2019) Gut segments outweigh the diet in shaping the intestinal microbiota composition in grass carp Ctenopharyngodon idellus. AMB Express 9, 44.CrossRefGoogle ScholarPubMed
Forsatkar, MN, Ali, M, Rafiee, NG, Farahmand, H and Lawrence, C (2018) Effects of the prebiotic mannan-oligosaccharide on feed deprived zebrafish: growth and reproduction. Aquaculture Research 49, 28222832.CrossRefGoogle Scholar
Gabriel, NN, Wilhelm, MR, Habte-Tsion, H-M, Chimwamurombe, P, Omoregie, E, Iipinge, LN and Shimooshili, K (2019) Effect of dietary Aloe vera polysaccharides supplementation on growth performance, feed utilization, hemato-biochemical parameters, and survival at low pH in African catfish (Clarias gariepinus) fingerlings. International Aquatic Research 11, 5772.CrossRefGoogle Scholar
Gajardo, K, Rodiles, A, Kortner, TM, Krogdahl, Å, Bakke, AM, Merrifield, DL and Sørum, H (2016) A high-resolution map of the gut microbiota in Atlantic salmon (Salmo salar): a basis for comparative gut microbial research. Scientific Reports 6, 30893.CrossRefGoogle ScholarPubMed
Ganguly, S, Dora, KC, Sarkar, S and Chowdhury, S (2013) Supplementation of prebiotics in fish feed: a review. Reviews in Fish Biology and Fisheries 23, 195199.CrossRefGoogle Scholar
Gatesoupe, FJ (1999) The use of probiotics in aquaculture. Aquaculture 180, 147165.CrossRefGoogle Scholar
Gatesoupe, FJ (2005) Probiotics and prebiotics for fish culture, at the parting of the ways. Aqua Feeds: Formulation and Beyond 2, 35.Google Scholar
Geng, X, Dong, XH, Tan, BP, Yang, QH, Chi, SY, Liu, HY and Liu, XQ (2011) Effects of dietary chitosan and Bacillus subtilis on the growth performance, non-specific immunity and disease resistance of cobia, Rachycentron canadum. Fish and Shellfish Immunology 31, 400406.CrossRefGoogle ScholarPubMed
Gentile, CL and Weir, TL (2018) The gut microbiota at the intersection of diet and human health. Science (New York, N.Y.) 362, 776780.CrossRefGoogle ScholarPubMed
Geraylou, Z, Souffreau, C, Rurangwa, E, Meester, L, Courtin, CM, Delcour, JA, Buyse, J and Ollevier, F (2013 a) Effects of dietary arabinoxylan-oligosaccharides (AXOS) and endogenous probiotics on the growth performance, non-specific immunity and gut microbiota of juvenile Siberian sturgeon (Acipenser baerii). Fish and Shellfish Immunology 35, 766775.CrossRefGoogle ScholarPubMed
Geraylou, Z, Souffreau, C, Rurangwa, E, Maes, GE, Spanier, KI, Courtin, CM, Delcour, JA, Buyse, J and Ollevier, F (2013 b) Prebiotic effects of arabinoxylan oligosaccharides on juvenile Siberian sturgeon (Acipenser baerii) with emphasis on the modulation of the gut microbiota using 454 pyrosequencing. FEMS Microbiology Ecology 86, 357371.CrossRefGoogle ScholarPubMed
Gibson, GR and Roberfroid, MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. The Journal of Nutrition 125, 14011412.CrossRefGoogle ScholarPubMed
Gibson, GR, Probert, HM, Loo, JV, Rastall, RA and Roberfroid, MB (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutrition Research Reviews 17, 259275.CrossRefGoogle ScholarPubMed
Gibson, GR, Scott, KP, Rastall, RA, Tuohy, KM, Hotchkiss, A, Dubert-Ferrandon, A, Gareau, M, Murphy, EF, Saulnier, D, Loh, G, Macfarlane, S, Delzenne, N, Ringel, Y, Kozianowski, G, Dickmann, R, Lenoir-Wijnkoop, I, Walker, C and Buddington, R (2010) Dietary prebiotics: current status and new definition. Food Science and Technology Bulletin: Functional Foods 7, 119.Google Scholar
Gibson, GR, Hutkins, R, Sanders, ME, Prescott, SL, Reimer, RA, Salminen, SJ, Scott, K, Stanton, C, Swanson, KS, Cani, PD, Verbeke, K and Reid, G (2017) The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nature Reviews Gastroenterology and Hepatology 14, 491502.CrossRefGoogle ScholarPubMed
Givens, CE, Ransom, B, Bano, N and Hollibaugh, JT (2015) Comparison of the gut microbiomes of 12 bony fish and 3 shark species. Marine Ecology Progress Series 518, 209223.CrossRefGoogle Scholar
Gomez, GD and Balcazar, JL (2008) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunology and Medical Microbiology 52, 145154.CrossRefGoogle ScholarPubMed
González-Félixa, ML, Gatlin, DM III, Urquidez-Bejarano, P, de la Reé-Rodrígueza, C, Duarte-Rodrígueza, L, Sánchez, F, Casas-Reyes, A, Yamamoto, FY, Ochoa-Leyva, A and Perez-Velazquez, M (2018) Effects of commercial dietary prebiotic and probiotic supplements on growth, innate immune responses, and intestinal microbiota and histology of Totoaba macdonaldi. Aquaculture 491, 239251.CrossRefGoogle Scholar
Grandclément, C, Tannières, M, Moréra, S, Dessaux, Y and Faure, D (2016) Quorum quenching: role in nature and applied developments. FEMS Microbiology Reviews 40, 86116.CrossRefGoogle ScholarPubMed
Guerreiro, I, Serra, CR, Oliva-Teles, A and Enes, P (2018) Gut microbiota of European sea bass (Dicentrarchus labrax) is modulated by short-chain fructooligosaccharides and xylooligosaccharides. Aquaculture International 26, 279288.CrossRefGoogle Scholar
Gupta, S, Lokesh, J, Abdelhafiz, Y, Siriyappagouder, P, Pierre, R, Sørensen, M, Fernandes, JMO and Kiron, V (2019) Macroalga-derived alginate oligosaccharide alters intestinal bacteria of Atlantic Salmon. Frontiers in Microbiology 10, 2037.CrossRefGoogle ScholarPubMed
Gupta, S, Bhathena, ZP, Kumar, S, Nuzaiba, PM, Srivastava, PP, Gupta, S and Jadhao, SB (2020) Comparative efficacy of mannan-oligosaccharides from two yeast species fed alone or in combination with probiotic Bacillus subtilis ATCC 6633 to Catla (Catla catla) juveniles. Aquaculture International 28, 691710.CrossRefGoogle Scholar
Haridas, DV and Pillai, D (2019) Evaluation of quorum quenching and probiotic activity of Bacillus thuringiensis QQ17 isolated from fish culture pond. International Journal of Current Microbiology and Applied Sciences 8, 16341649.CrossRefGoogle Scholar
Hassaan, MS, Soltan, MA and Ghonemy, MMR (2014) Effect of synbiotics between Bacillus licheniformis and yeast extract on growth, hematological and biochemical indices of the Nile tilapia (Oreochromis niloticus). Egyptian Journal of Aquatic Research 40, 199208.CrossRefGoogle Scholar
Hassani, MHS, Jourdehi, AY, Zelti, AH, Masouleh, AS and Lakani, FB (2020) Effects of commercial superzist probiotic on growth performance and hematological and immune indices in fingerlings Acipenser baerii. Aquaculture International 28, 377387.CrossRefGoogle Scholar
Hennersdorf, P, Kleinertz, S, Theisen, S, Abdul-Aziz, MA, Mrotzek, G, Palm, HW and Saluz, HP (2016) Microbial diversity and parasitic load in tropical fish of different environmental conditions. PLoS ONE 11, e0151594.CrossRefGoogle ScholarPubMed
Hill, C, Guarner, F, Reid, G, Gibson, GR, Merenstein, DJ, Pot, B, Morelli, L, Canani, RB, Flint, HJ, Salminen, S, Calder, PC and Sanders, ME (2014) Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews Gastroenterology and Hepatology 11, 506514.CrossRefGoogle ScholarPubMed
Hoseinifar, SH, Khalili, M, Rostami, HK and Esteban, (2013) Dietary galactooligosaccharide affects intestinal microbiota, stress resistance, and performance of Caspian roach (Rutilus rutilus) fry. Fish and Shellfish Immunology 35, 14161420.CrossRefGoogle ScholarPubMed
Hoseinifar, SH, Soleimani, N and Ringø, E (2014) Effects of dietary fructo-oligosaccharide supplementation on the growth performance, haemato-immunological parameters, gut microbiota and stress resistance of common carp (Cyprinus carpio) fry. British Journal of Nutrition 112, 12961302.CrossRefGoogle ScholarPubMed
Hoseinifar, SH, Mirvaghefi, A, Amoozegar, MA, Merrifield, DL and Ringø, E (2017) In vitro selection of a synbiotic and in vivo evaluation on intestinal microbiota, performance and physiological response of rainbow trout (Oncorhynchus mykiss) fingerlings. Aquaculture Nutrition 23, 111118.CrossRefGoogle Scholar
Huang, K and Nitin, N (2019) Edible bacteriophage based antimicrobial coating on fish feed for enhanced treatment of bacterial infections in aquaculture industry. Aquaculture 502, 1825.CrossRefGoogle Scholar
Jafarzadeh, E, Khara, H and Ahmadnezhad, M (2015) Effects of synbiotic (Biomin IMBO) on haematological and immunological components of Russian sturgeon, Acipenser guldenstadti. Comparative Clinical Pathology 24, 13171323.CrossRefGoogle Scholar
Jami, MJ, Kenari, AA, Paknejad, H and Mohseni, M (2019) Effects of dietary β-glucan, mannan oligosaccharide, Lactobacillus plantarum and their combinations on growth performance, immunity and immune related gene expression of Caspian trout, Salmo trutta caspius (Kessler, 1877). Fish and Shellfish Immunology 91, 202208.CrossRefGoogle ScholarPubMed
Karimi, M, Paknejad, H, Hoseinifar, SH, Shabani, A and Mozanzadeh, MT (2020) The effects of dietary raffinose on skin mucus immune parameters and protein profile, serum non-specific immune parameters and immune related genes expression in common carp (Cyprinus carpio L.). Aquaculture 520, 734525.CrossRefGoogle Scholar
Karimzadeh, S, Amirkolaie, AK and Molla, AE (2013) Effects of different levels of immunogen on growth performance, intestinal bacteria colonization and survival rate in Rutilus kutum larvae. World Journal of Fish and Marine Sciences 5, 664669.Google Scholar
Khodadadi, M, Abbasi, N, Adorian, TJ, Farsani, HG, Hedayati, A and Hoseini, SM (2018) Growth performance, survival, body composition, hematological parameters, intestinal histomorphology, and digestive enzymes’ activity in juvenile rainbow trout (Oncorhynchus mykiss) fed dietary Immunogen®. Journal of Applied Aquaculture 30, 174186.CrossRefGoogle Scholar
Kolida, S and Gibson, GR (2011) Synbiotics in health and disease. The Annual Review of Food Science and Technology 2, 373393.CrossRefGoogle ScholarPubMed
Kowalska, JD, Kazimierczak, J, Sowińska, PJ, Wójcik, EA, Siwicki, AK and Dastych, J (2020) Growing trend of fighting infections in aquaculture environment – opportunities and challenges of phage therapy. Antibiotics 9, 301.CrossRefGoogle ScholarPubMed
Krumbeck, JA, Walter, J and Hutkins, RW (2018) Synbiotics for improved human health: recent developments, challenges, and opportunities. Annual Review of Food Science and Technology 9, 451479.CrossRefGoogle ScholarPubMed
Kuebutornye, FKA, Lu, Y, Abarike, ED, Wang, Z, Li, Y and Sakyi, ME (2020) In vitro assessment of the probiotic characteristics of three Bacillus species from the gut of Nile tilapia, Oreochromis niloticus. Probiotics and Antimicrobial Proteins 12, 412424.CrossRefGoogle ScholarPubMed
Kumar, P, Jain, KK and Sardar, P (2018) Effects of dietary synbiotic on innate immunity, antioxidant activity and disease resistance of Cirrhinus mrigala juveniles. Fish and Shellfish Immunology 80, 124132.CrossRefGoogle ScholarPubMed
Laanto, E, Bamford, JKH, Laakso, J and Sundberg, L-R (2012) Phage-driven loss of virulence in a fish pathogenic bacterium. PLoS ONE 7, e53157.CrossRefGoogle Scholar
Laanto, E, Bamford, JKH, Ravantti, JJ and Sundberg, L-R (2015) The use of phage FCL-2 as an alternative to chemotherapy against columnaris disease in aquaculture. Frontiers in Microbiology 6, 829.CrossRefGoogle ScholarPubMed
Larsen, AM, Mohammed, HH and Arias, CR (2014) Characterisation of the gut microbiota of three commercially valuable warmwater fish species. Journal of Applied Microbiology 116, 13961404.CrossRefGoogle ScholarPubMed
Lazado, CC, Caipang, CMA and Estante, EG (2015) Prospects of host-associated microorganisms in fish and penaeids as probiotics with immunomodulatory functions. Fish and Shellfish Immunology 45, 212.CrossRefGoogle ScholarPubMed
Ley, RE, Lozupone, CA, Hamady, M, Knight, R and Gordon, JI (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Reviews Microbiology 6, 776788.CrossRefGoogle ScholarPubMed
Li, M-F, Zhang, B-C, Li, J and Sun, L (2014) Sil: a Streptococcus iniae bacteriocin with dual role as an antimicrobial and an immunomodulator that inhibits innate immune response and promotes S. iniae infection. PLoS ONE 9, e96222.CrossRefGoogle Scholar
Li, X, Ringø, E, Hoseinifar, SH, Lauzon, HL, Birkbeck, H and Yang, D (2018) The adherence and colonization of microorganisms in fish gastrointestinal tract. Reviews in Aquaculture 11, 603618.CrossRefGoogle Scholar
Lin, S-M, Jiang, Y, Chen, Y-J, Luo, L, Doolgindachbaporn, S and Yuangsoi, B (2017) Effects of Astragalus polysaccharides (APS) and chitooligosaccharides (COS) on growth, immune response and disease resistance of juvenile largemouth bass, Micropterus salmoides. Fish and Shellfish Immunology 70, 4047.CrossRefGoogle ScholarPubMed
Liu, H, Guo, X, Gooneratne, R, Lai, R, Zeng, C, Zhan, F and Wang, W (2016) The gut microbiome and degradation enzyme activity of wild freshwater fishes influenced by their trophic levels. Scientific Reports 6, 24340.CrossRefGoogle ScholarPubMed
Liu, S, Wang, S, Cai, Y, Li, E, Ren, Z, Wu, Y, Guo, W, Sun, Y and Zhou, Y (2020) Beneficial effects of a host gut-derived probiotic, Bacillus pumilus, on the growth, non-specific immune response and disease resistance of juvenile golden pompano, Trachinotus ovatus. Aquaculture 514, 734446.CrossRefGoogle Scholar
Llewellyn, MS, Boutin, S, Hoseinifar, SH and Derome, N (2014) Teleost microbiomes: the state of the art in their characterisation, manipulation and importance in aquaculture and fisheries. Frontiers in Microbiology 5, 207.CrossRefGoogle ScholarPubMed
Lv, X, Ma, H, Sun, M, Lin, Y, Bai, F, Li, J and Zhang, B (2018) A novel bacteriocin DY4-2 produced by Lactobacillus plantarum from cutlassfish and its application as bio-preservative for the control of Pseudomonas fluorescens in fresh turbot (Scophthalmus maximus) fillets. Food Control 89, 2231.CrossRefGoogle Scholar
Madreseh, S, Ghaisari, HR and Hosseinzadeh, S (2019) Effect of lyophilized, encapsulated Lactobacillus fermentum and lactulose feeding on growth performance, heavy metals, and trace element residues in rainbow trout (Oncorhynchus mykiss) tissues. Probiotics and Antimicrobial Proteins 11, 12571263.CrossRefGoogle ScholarPubMed
Mahious, AS, Gatesoupe, FJ, Hervi, MR, Metailler, R and Olivier, F (2006) Effect of dietary inulin and oligosaccharides as prebiotics for weaning turbot, Psetta maxima (Linnaeus, C. 1758). Aquaculture International 14, 219229.CrossRefGoogle Scholar
Malik, DJ, Sokolov, IJ, Vinner, GK, Mancuso, F, Cinquerrui, S, Vladisavljevic, GT, Clokie, MRJ, Garton, NJ, Stapley, GFA and Kirpichnikova, A (2017) Formulation, stabilisation and encapsulation of bacteriophage for phage therapy. Advances in Colloid and Interface Science 249, 100133.CrossRefGoogle ScholarPubMed
McDonald, RC, Watts, JEM and Schreier, HJ (2019) Effect of diet on the enteric microbiome of the wood-eating catfish Panaque nigrolineatus. Frontiers in Microbiology 10, 2687.CrossRefGoogle ScholarPubMed
Mehrabi, F, Khalesi, MK and Hazaie, K (2018) Effects of pre- and probiotics on growth, survival, body composition, and hematology of common carp (Cyprinus carpio L.) fry from the Caspian Sea. Turkish Journal of Fisheries and Aquatic Sciences 18, 597602.CrossRefGoogle Scholar
Meng, X, Wang, J, Wan, W, Xu, M and Wang, T (2017) Influence of low molecular weight chitooligosaccharides on growth performance and non-specific immune response in Nile tilapia Oreochromis niloticus. Aquaculture International 25, 12651277.CrossRefGoogle Scholar
Merrifield, DL, Dimitroglou, A, Foey, A, Davies, SJ, Baker, RTM, Bøgwald, J, Castex, M and Ringø, E (2010) The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture 302, 118.CrossRefGoogle Scholar
Michl, SC, Ratten, J-M, Beyer, M, Hasler, M, LaRoche, J and Schulz, C (2017) The malleable gut microbiome of juvenile rainbow trout (Oncorhynchus mykiss): diet-dependent shifts of bacterial community structures. PLoS ONE 12, e0177735.CrossRefGoogle ScholarPubMed
Midhun, SJ, Neethu, S, Vysakh, A, Radhakrishnan, EK and Jyothis, M (2018) Antagonism against fish pathogens by cellular components/preparations of Bacillus coagulans (MTCC-9872) and it's in vitro probiotic characterisation. Current Microbiology 75, 11741181.CrossRefGoogle ScholarPubMed
Miest, JJ, Arndt, C, Adamek, M, Steinhagen, D and Reusch, TBH (2016) Dietary β-glucan (MacroGard®) enhances survival of first feeding turbot (Scophthalmus maximus) larvae by altering immunity, metabolism and microbiota. Fish and Shellfish Immunology 48, 94104.CrossRefGoogle ScholarPubMed
Mo, WY, Cheng, Z, Choi, WM, Lun, CHI, Man, YB, Wong, JTF, Chen, XW, Lau, SCK and Wong, MH (2015) Use of food waste as fish feeds: effects of prebiotic fibers (inulin and mannanoligosaccharide) on growth and non-specific immunity of grass carp (Ctenopharyngodon idella). Environmental Science and Pollution Research 22, 1766317671.CrossRefGoogle ScholarPubMed
Modanloo, M, Soltanian, S, Akhlaghi, M and Hoseinifar, SH (2017) The effects of single or combined administration of galactooligosaccharide and Pediococcus acidilactici on cutaneous mucus immune parameters, humoral immune responses and immune related genes expression in common carp (Cyprinus carpio) fingerlings. Fish and Shellfish Immunology 70, 391397.CrossRefGoogle ScholarPubMed
Mohammadian, T, Nasirpour, M, Tabandeh, MR and Mesbah, M (2019) Synbiotic effects of β-glucan, mannan oligosaccharide and Lactobacillus casei on growth performance, intestine enzymes activities, immune-hematological parameters and immune-related gene expression in common carp, Cyprinus carpio: an experimental infection with Aeromonas hydrophila. Aquaculture 511, 634197.CrossRefGoogle Scholar
Mouriño, JLP, Vieira, FN, Jatobá, A, Silva, BC, Pereira, GV, Jesus, GFA, Ushizima, TT, Seiffert, WQ and Martins, ML (2017) Symbiotic supplementation on the hemato-immunological parameters and survival of the hybrid surubim after challenge with Aeromonas hydrophila. Aquaculture Nutrition 23, 276284.CrossRefGoogle Scholar
Mousavi, E, Mohammadiazarm, H, Mousavi, SM and Ghatrami, ER (2016) Effects of inulin, savory and onion powders in diet of juvenile's carp Cyprinus carpio (Linnaeus 1758) on Gut microflora, immune response and blood biochemical parameters. Turkish Journal of Fisheries and Aquatic Sciences 16, 831838.CrossRefGoogle Scholar
Mukherjee, A, Chandra, G and Ghosh, K (2019) Single or conjoint application of autochthonous Bacillus strains as potential probiotics: effects on growth, feed utilization, immunity and disease resistance in Rohu, Labeo rohita (Hamilton). Aquaculture 512, 734302.CrossRefGoogle Scholar
Mukherjee, A, Rodiles, A, Merrifield, DL, Chandra, G and Ghosh, K (2020) Exploring intestinal microbiome composition in three Indian major carps under polyculture system: a high-throughput sequencing based approach. Aquaculture 524, 735206.CrossRefGoogle Scholar
Nayak, SK (2010) Role of gastrointestinal microbiota in fish. Aquaculture Research 41, 15531573.CrossRefGoogle Scholar
Neish, AS (2009) Microbes in gastrointestinal health and disease. Gastroenterology 136, 6580.CrossRefGoogle ScholarPubMed
Niu, K-M, Khosravi, S, Kothari, D, Lee, W-D, Lim, J-M, Lee, B-J, Kim, K-W, Lim, S-G, Lee, S-M and Kim, S-K (2019) Effects of dietary multi-strain probiotics supplementation in a low fishmeal diet on growth performance, nutrient utilization, proximate composition, immune parameters, and gut microbiota of juvenile olive flounder (Paralichthys olivaceus). Fish and Shellfish Immunology 93, 258268.CrossRefGoogle Scholar
Niu, K-M, Lee, B-J, Kothari, D, Lee, W-D, Hur, S-W, Lim, S-G, Kim, KW, Kim, KD, Kim, NN and Kim, SK (2020) Dietary effect of low fish meal aquafeed on gut microbiota in olive flounder (Paralichthys olivaceus) at different growth stages. MicrobiologyOpen 9, e992.CrossRefGoogle ScholarPubMed
Onarheim, AM, Wiik, R, Burghardt, J and Stackebrandt, E (1994) Characterisation and identification of two Vibrio species indigenous to the intestine of fish in cold sea water; description of Vibrio iliopiscarius sp. nov. Systematic and Applied Microbiology 17, 370379.CrossRefGoogle Scholar
Parada Venegas, V, De la Fuente, MK, Landskron, G, González, MJ, Quera, R, Dijkstra, G, Harmsen, HJM, Faber, KN and Hermoso, MA (2019) Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Frontiers in Immunology 10, 277.CrossRefGoogle ScholarPubMed
Patel, S and Goyal, A (2011) Functional oligosaccharides: production, properties and applications. World Journal of Microbiology and Biotechnology 27, 11191128.CrossRefGoogle Scholar
Paz, AL, Mota da Silva, J, Marques da Silva, KM and Val, AL (2019) Protective effects of the fructooligosaccharide on the growth performance, hematology, immunology indicators and survival of tambaqui (Colossoma macropomum, Characiformes: Serrasalmidae) infected by Aeromonas hydrophila. Aquaculture Reports 15, 100222.CrossRefGoogle Scholar
Pękala-Safińska, A (2018) Contemporary threats of bacterial infections in freshwater fish. Journal of Veterinary Research 62, 261267.CrossRefGoogle ScholarPubMed
Pilarski, F, Ferreira de Oliveira, CA, Darpossolo de Souza, FPB and Zanuzzo, FS (2017) Different β-glucans improve the growth performance and bacterial resistance in Nile tilapia. Fish and Shellfish Immunology 70, 2529.CrossRefGoogle ScholarPubMed
Pineiro, M, Asp, NG, Reid, G, Macfarlane, S, Morelli, L, Brunser, O and Tuohy, K (2008) FAO Technical meeting on prebiotics. Journal of Clinical Gastroenterology 42, S156S159.CrossRefGoogle ScholarPubMed
Prieto, ML, O'Sullivan, L, Tan, SP, McLoughlin, P, Hughes, H, Gutierrez, M, Lane, JA, Hickey, RM, Lawlor, PG and Gardiner, GE (2014) In vitro assessment of marine Bacillus for use as livestock probiotics. Marine Drugs 12, 24222445.CrossRefGoogle ScholarPubMed
Rajasekaran, N, Sivakumar, R and Mathialagan, R (2014) Isolation and characterization of intestinal enzymes producing bacteria along with cultured and captured grass carp Ctenopharyngodon idella (Valenciennes, 1844) with reference to amylase, protease and lipase activity. Journal of Chemical, Biological and Physical Sciences B 4, 21752189.Google Scholar
Ramachandran, S and Ray, AK (2007) Nutritional evaluation of fermented black gram (Phaseolus mungo) seed meal in compound diets for rohu, Labeo rohita (Hamilton), fingerlings. Journal of Applied Ichthyology 23, 7479.CrossRefGoogle Scholar
Rameshkumar, P, Nazar, AKA, Pradeep, MA, Kalidas, C, Jayakumar, R, Tamilmani, G, Sakthivel, M, Samal, AK, Sirajudeen, S, Venkatesan, V and Nazeera, BM (2017) Isolation and characterization of pathogenic Vibrio alginolyticus from sea cage cultured cobia (Rachycentron canadum (Linnaeus 1766)) in India. Letters in Applied Microbiology 65, 423430.CrossRefGoogle ScholarPubMed
Reza, A, Abdolmajid, H, Abbas, M and Abdolmohammad, AK (2009) Effect of dietary prebiotic inulin on growth performance, intestinal microflora, body composition and hematological parameters of juvenile beluga, Huso huso (Linnaeus, 1758). Journal of the World Aquaculture Society 40, 771779.CrossRefGoogle Scholar
Richards, GP (2014) Bacteriophage remediation of bacterial pathogens in aquaculture: a review of the technology. Bacteriophage 4, e975540.CrossRefGoogle ScholarPubMed
Ringø, E and Birkbeck, TH (1999) Intestinal microflora of fish larvae and fry. Aquaculture Research 30, 7393.CrossRefGoogle Scholar
Ringø, E and Olsen, R (1999) The effect of diet on aerobic bacterial flora associated with intestine of Arctic charr (Salvelinus alpinus L.). Journal of Applied Microbiology 86, 2228.CrossRefGoogle ScholarPubMed
Ringø, E, Sperstad, S, Myklebust, R, Refstie, S and Krogdahl, A (2006) Characterisation of the microbiota associated with intestine of Atlantic cod (Gadus morhua L.): the effect of fish meal, standard soybean meal and a bioprocessed soybean meal. Aquaculture 261, 829841.CrossRefGoogle Scholar
Ringø, E, Olsen, RE, Gifstad, TO, Dalmo, RA, Amlund, H, Hemre, G-I and Bakke, AM (2010) Probiotics in aquaculture: a review. Aquaculture Nutrition 16, 117136.CrossRefGoogle Scholar
Ringø, E, Dimitroglou, A, Hoseinifar, SH and Davies, SJ (2014) Prebiotics in finfish: An update. In Merrifield, DL and Ringø, E (eds), Aquaculture Nutrition: Gut Health, Probiotics and Prebiotics. Chichester: John Wiley & Sons Ltd, pp. 360400.CrossRefGoogle Scholar
Ringø, E, Zhou, Z, Vecino, JLG, Wadsworth, S, Romero, J, Krogdahl, A, Olsen, RE, Dimitroglou, A, Foey, A, Davies, S, Owen, M, Lauzon, HL, Martinsen, LL, De Schryver, P, Bossier, P, Spersta, S and Merrifield, DS (2016) Effect of dietary components on the gut microbiota of aquatic animals. A never-ending story? Aquaculture Nutrition 22, 219282.CrossRefGoogle Scholar
Ríos-Covián, D, Ruas-Madiedo, P, Margolles, A, Gueimonde, M, de los Reyes-Gavilán, CG and Salazar, N (2016) Intestinal short chain fatty acids and their link with diet and human health. Frontiers in Microbiology 7, 185.CrossRefGoogle ScholarPubMed
Roberfroid, M (2007) Prebiotics: the concept revisited. The Journal of Nutrition 137, 830837.CrossRefGoogle ScholarPubMed
Rodriguez-Estrada, U, Satoh, S, Haga, Y, Fushimi, H and Sweetman, J (2009) Effects of single and combined supplementation of Enterococcus faecalis, mannanoligosaccharides and polyhydroxybutyrate acid growth performance and immune response of rainbow trout. Oncorhynchus mykiss. Aquaculture Science 57, 609617.Google Scholar
Roeselers, G, Mittge, EK, Stephens, WZ, Parichy, DM, Cavanaugh, CM, Guillemin, K and Rawls, JF (2011) Evidence for a core gut microbiota in the zebrafish. The ISME Journal 5, 15951608.CrossRefGoogle ScholarPubMed
Roy, T, Mondal, S and Ray, AK (2009) Phytase-producing bacteria in the digestive tracts of some freshwater fish. Aquaculture Research 40, 344353.CrossRefGoogle Scholar
Rubiolo, JA, Botana, LM and Martínez, P (2019) Insights into mussel microbiome. In Derome, N (ed.), Microbial Communities in Aquaculture Ecosystems, Improving Productivity and Sustainability. Cham, Switzerland: Springer, pp. 95120.CrossRefGoogle Scholar
Ruiz, ML, Owatari, MS, Yamashita, MM, Ferrarezi, JVS, Garcia, P, Cardoso, L, Martins, ML and Mouriño, JLP (2020) Histological effects on the kidney, spleen, and liver of Nile tilapia Oreochromis niloticus fed different concentrations of probiotic. Tropical Animal Health and Production 52, 167176.CrossRefGoogle ScholarPubMed
Rurangwa, E, Laranja, JL, Van Houdt, R, Delaedt, Y, Geraylou, Z, Van de Wiele, T, Van Loo, J, Van Craeyveld, V, Courtin, CM, Delcour, JA and Ollevier, F (2009) Selected nondigestible carbohydrates and prebiotics support the growth of probiotic fish bacteria mono cultures in vitro. Journal of Applied Microbiology 106, 932940.CrossRefGoogle ScholarPubMed
Saha, S and Ray, AK (2011) Evaluation of nutritive value of water hyacinth (Eichhornia crassipes) leaf meal in compound diets for rohu, Labeo rohita (Hamilton, 1822) fingerlings after fermentation with two bacterial strains isolated from fish gut. Turkish Journal of Fisheries and Aquatic Science 11, 199208.Google Scholar
Salaghi, Z, Imanpuor, M and Taghizadeh, V (2013) Effect of different levels of probiotic primalac on growth performance and survival rate of Persian Sturgeon (Acipenser persicus). Global Veterinaria 11, 238242.Google Scholar
Salehi-Farsani, A, Soltani, M, Kamali, A and Shamsaie, M (2014) Effect of immune motivator Macrogard and Spirulina platensis on some growth, carcass and biochemical indices of stellate sturgeon Acipenser stellatus. Aquaculture, Aquarium. Conservation & Legislation International Journal of the Bioflux Society 7, 137147.Google Scholar
Salinas, I, Abelli, L, Bertoni, F, Picchietti, S, Roque, A, Furones, D, Cuesta, A, Meseguer, J and Esteban, MA (2008) Monospecies and multispecies probiotic formulations produce different systemic and local immunostimulatory effects in the gilthead seabream (Sparus aurata L.). Fish and Shellfish Immunology 25, 114123.CrossRefGoogle ScholarPubMed
Schulz, P, Robak, S, Dastych, J and Siwicki, AK (2019 a) Influence of bacteriophages cocktail on European eel (Anguilla anguilla) immunity and survival after experimental challenge. Fish and Shellfish Immunology 84, 2837.CrossRefGoogle ScholarPubMed
Schulz, P, Pajdak-Czaus, J, Robak, S, Dastych, J and Siwicki, AK (2019 b) Bacteriophage-based cocktail modulates selected immunological parameters and post-challenge survival of rainbow trout (Oncorhynchus mykiss). Journal of Fish Diseases 42, 11511160.Google ScholarPubMed
Seghouani, H, Garcia-Rangel, C-E, Füller, J, Gauthier, J and Derome, N (2017) Walleye autochthonous bacteria as promising probiotic candidates against Flavobacterium columnare. Frontiers in Microbiology 8, 1349.CrossRefGoogle ScholarPubMed
Sewaka, M, Trullas, C, Chotik, A, Rodkhum, C, Chansue, N, Boonanuntanasarn, S and Pirarat, N (2019) Efficacy of synbiotic Jerusalem artichoke and Lactobacillus rhamnosus GG- supplemented diets on growth performance, serum biochemical parameters, intestinal morphology, immune parameters and protection against Aeromonas veronii in juvenile red tilapia (Oreochromis spp.). Fish and Shellfish Immunology 86, 260268.CrossRefGoogle ScholarPubMed
Sharpe, RL, Drolet, M and MacLatchy, DL (2006) Investigation of de novo cholesterol synthetic capacity in the gonads of goldfish (Carassius auratus) exposed to the phytosterol beta-sitosterol. Reproductive Biology and Endocrinology 4, 60.CrossRefGoogle Scholar
Shewale, RN, Sawale, PD, Khedkar, CD and Singh, A (2014) Selection criteria for probiotics: a review. International Journal of Probiotics and Prebiotics 9.Google Scholar
Shori, AB (2017) Microencapsulation improved probiotics survival during gastric transit. Hayati Journal of Biosciences 24, 15.CrossRefGoogle Scholar
Silva, YJ, Costa, L, Pereira, C, Cunha, Â, Calado, R, Gomes, NCM and Almeida, A (2013) Influence of environmental variables in the efficiency of phage therapy in aquaculture. Microbial Biotechnology 7, 401413.CrossRefGoogle Scholar
Silva, YJ, Costa, L, Pereira, C, Mateus, C, Cunha, Â, Calado, R, Gomes, NCM, Pardo, MA, Hernandez, I and Almeida, A (2014) Phage therapy as an approach to prevent Vibrio anguillarum infections in fish larvae production. PLoS ONE 9, e114197.CrossRefGoogle ScholarPubMed
Simora, RMC, Ferdinand, R, Traifalgar, M and Legario, FS (2015) Characterization of extracellular enzymes from culturable autochthonous gut bacteria in rabbitfish (Siganus guttatus). ELBA Bioflux 7, 6776.Google Scholar
Singh, G, Bhatnagar, A, Alok, K and Ajay, SA (2018) Enzymatic profiling and feeding preferences of catla: Catla catla, rohu: Labeo rohita and mrigala: Cirrhinus mrigala in rural polyculture ponds. Journal of Aquaculture Research and Development 9, 553.CrossRefGoogle Scholar
Singh, SK, Tiwari, VK, Chadha, NK, Munilkumar, S, Nilesh, CP and Pawar, A (2019) Effect of dietary synbiotic supplementation on growth, immune and physiological status of Labeo rohita juveniles exposed to low pH stress. Fish and Shellfish Immunology 91, 358368.CrossRefGoogle ScholarPubMed
Sissons, J and Fellows, CM (2014) Sensory, technological, and health aspects of adding fiber to wheat-based pasta. In Victor, RW and Zibadi, PS (eds), Wheat and Rice in Disease Prevention and Health, Benefits, Risks and Mechanisms of Whole Grains in Health Promotion. London: Academic Press, pp. 211226.CrossRefGoogle Scholar
Smith, CCR, Snowberg, LK, Caporaso, JG, Knight, R and Bolnick, DI (2015) Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota. The ISME Journal 9, 25152526.CrossRefGoogle ScholarPubMed
Solovyev, MM, Kashinskaya, EN, Bochkarev, NA, Andree, KB and Simonov, E (2019) The effect of diet on the structure of gut bacterial community of sympatric pair of whitefishes (Coregonus lavaretus): one story more. PeerJ 7, e8005.CrossRefGoogle Scholar
Soltani, M, Badzohreh, G, Mirzargar, S, Farhangi, M, Shekarabi, PH and Lymbery, A (2019) Growth behaviour and fatty acid production of probiotics, Pediococcus acidilactici and Lactococcus lactis, at different concentrations of fructooligosaccharide: studies validating clinical efficacy of selected synbiotics on growth performance of Caspian Roach (Rutilus frisii kutum) fry. Probiotics and Antimicrobial Proteins 11, 765773.CrossRefGoogle ScholarPubMed
Stappenbeck, TS, Hooper, LV and Gordon, JI (2002) Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proceedings of the National Academy of Sciences of the USA 99, 1545115455.CrossRefGoogle ScholarPubMed
Sudheesh, PS, Al-Ghabshi, A, Al-Mazrooei, N and Al-Habsi, S (2012) Comparative pathogenomics of bacteria causing infectious diseases in fish. International Journal of Evolutionary Biology 2012, 457264.CrossRefGoogle ScholarPubMed
Sugita, H, Tokuyama, K and Deguchi, Y (1985) The intestinal microflora of carp Cyprinus carpio, grass carp Ctenopharyngodon idella and tilapia Sarotherodon niloticus. Bulletin of Japanese Society Sciences of Fisheries 50, 13251329.CrossRefGoogle Scholar
Sullam, KE, Essinger, SD, Lozupone, CA, O'Connor, MP, Rosen, GL, Knight, ROB, Kilham, SS and Russell, JA (2012) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Molecular Ecology 21, 33633378.CrossRefGoogle ScholarPubMed
Sun, H, Shang, M, Tang, Z, Jiang, H, Dong, H, Zhou, X, Lin, Z, Shi, C, Ren, P, Zhao, L, Shi, M, Zhou, L, Pan, H, Chang, O, Xuerong Li, X, Huang, Y and Yu, X (2020 a) Oral delivery of Bacillus subtilis spores expressing Clonorchis sinensis paramyosin protects grass carp from cercaria infection. Applied Microbiology and Biotechnology 104, 16331646.CrossRefGoogle ScholarPubMed
Sun, R, Zhang, M, Hui Chen, H, Wei, Y and Ning, D (2020 b) Germination-arrest Bacillus subtilis spores as an oral delivery vehicle of grass carp reovirus (GCRV) Vp7 antigen augment protective immunity in grass carp (Ctenopharyngodon idella). Genes 11, 1351.CrossRefGoogle ScholarPubMed
Ta'ati, R, Soltani, M, Bahmani, M and Zamini, AA (2011) Effects of the prebiotics immunoster and immunowall on growth performance of juvenile beluga (Huso huso). Journal of Applied Ichthyology 27, 796798.CrossRefGoogle Scholar
Tamamdusturi, R, Widanarni, W and Yuhana, M (2016) Administration of microencapsulated probiotic Bacillus sp. NP5 and prebiotic mannan oligosaccharide for prevention of Aeromonas hydrophila infection on Pangasianodon hypophthalmus. Journal of Fisheries and Aquatic Science 11, 6776.CrossRefGoogle Scholar
Tarkhani, R, Imani, A, Hoseinifar, SH, Ashayerizadeh, O, Moghanlou, KS, Manaffar, R, Van Doan, H and Reverter, M (2020 a) Comparative study of host-associated and commercial probiotic effects on serum and mucosal immune parameters, intestinal microbiota, digestive enzymes activity and growth performance of roach (Rutilus rutilus caspicus) fingerlings. Fish and Shellfish Immunology 98, 661669.CrossRefGoogle ScholarPubMed
Tarkhani, R, Imani, A, Hoseinifar, SH, Moghanlou, KS and Manaffar, R (2020 b) The effects of host associated Enterococcus faecium CGMCC1.2136 on serum immune parameters, digestive enzymes activity and growth performance of the Caspian roach (Rutilus rutilus caspicus) fingerlings. Aquaculture 519, 734741.CrossRefGoogle Scholar
Tarnecki, AM, Burgos, FA, Ray, CL and Arias, CR (2017) Fish intestinal microbiome: diversity and symbiosis unravelled by metagenomics. Journal of Applied Microbiology 123, 217.CrossRefGoogle ScholarPubMed
Taverniti, V and Guglielmetti, S (2011) The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of paraprobiotic concept). Genes and Nutrition 6, 261274.CrossRefGoogle ScholarPubMed
Terpou, A, Papadaki, A, Lappa, IK, Kachrimanidou, V, Bosnea, LA and Kopsahelis, N (2019) Probiotics in food systems: significance and emerging strategies towards improved viability and delivery of enhanced beneficial value. Nutrients 11, 1591.CrossRefGoogle ScholarPubMed
Toutou, MM, Soliman, AAA, Farrag, MMS and Abouelwafa, AES (2016) Effect of probiotic and synbiotic food supplementation on growth performance and healthy status of Grass Carp, Ctenopharyngodon idella (Valenciennes, 1844). International Journal of Ecotoxicology and Ecobiology 1, 111117.Google Scholar
Vaezi, M, Khara, H and Shenavar, A (2016) Synbiotic (Biomin imbo) alters gut bacterial microflora of Russian sturgeon, Acipenser guldenstadti (Brandt & Ratzeburg, 1833) in a time-dependent pattern. Journal of Parasitic Diseases 40, 11891192.CrossRefGoogle Scholar
Van Doan, H, Tapingkae, W, Moonmanee, T and Seepai, A (2016) Effects of low molecular weight sodium alginate on growth performance, immunity, and disease resistance of tilapia. Oreochromis niloticus. Fish and Shellfish Immunology 55, 186194.CrossRefGoogle ScholarPubMed
Van Doan, H, Hoseinifar, SH, Khanongnuch, C, Kanpiengjai, A, Unban, K, Kim, VV and Srichaiyo, S (2018) Host-associated probiotics boosted mucosal and serum immunity, disease resistance and growth performance of Nile tilapia (Oreochromis niloticus). Aquaculture 491, 94100.CrossRefGoogle Scholar
Van Doan, H, Hoseinifar, SH, Tapingkae, W, Seelaudom, M, Jaturasitha, S, Dawood, MAO, Wongmaneeprateep, S, Thu, TTN and Esteban, (2019) Boosted growth performance, mucosal and serum immunity, and disease resistance Nile Tilapia (Oreochromis niloticus) fingerlings using corncob-derived xylooligosaccharide and Lactobacillus plantarum CR1T5. Probiotics and Antimicrobial Proteins 12, 400411.CrossRefGoogle Scholar
Vazirzadeha, A, Roostaa, H, Masoumia, H, Farhadia, A and Jeffs, A (2020) Long-term effects of three probiotics, singular or combined, on serum innate immune parameters and expressions of cytokine genes in rainbow trout during grow-out. Fish and Shellfish Immunology 98, 748757.CrossRefGoogle Scholar
Vetvicka, V, Vannucci, L and Sima, P (2013) The effects of β-glucan on fish immunity. North American Journal of Medical Sciences 5, 580588.CrossRefGoogle ScholarPubMed
Vyas, U and Ranganathan, N (2012) Probiotics, prebiotics, and synbiotics: gut and beyond. Gastroenterology Research and Practice 872716.Google Scholar
Wang, H, Wang, Y and Yang, R (2017) Recent progress in Bacillus subtilis spore-surface display: concept, progress, and future. Applied Microbiology and Biotechnology 101, 933949.CrossRefGoogle ScholarPubMed
Wang, AR, Ran, C, Ringø, E and Zhou, ZG (2018) Progress in fish gastrointestinal microbiota research. Reviews in Aquaculture 10, 626640.CrossRefGoogle Scholar
Wang, C, Liu, Y, Sun, G, Li, X and Liu, Z (2019) Growth, immune response, antioxidant capability, and disease resistance of juvenile Atlantic salmon (Salmo salar L.) fed Bacillus velezensis V4 and Rhodotorula mucilaginosa compound. Aquaculture 500, 6574.CrossRefGoogle Scholar
Wanka, KM, Damerau, T, Costas, B, Krueger, A, Schulz, C and Wuertz, S (2018) Isolation and characterisation of native probiotics for fish farming. BMC Microbiology 18, 119.CrossRefGoogle ScholarPubMed
Xia, J, Lin, G, Fu, G, Wan, Z, Lee, M, Wang, L, Liu, XJ and Yue, GH (2014) The intestinal microbiome of fish under starvation. BMC Genomics 15, 266.CrossRefGoogle ScholarPubMed
Yang, P, Hu, H, Liu, Y, Li, Y, Ai, Q, Xu, W, Zhang, W, Zhang, Y, Zhang, Y and Mai, K (2018) Dietary stachyose altered the intestinal microbiota profile and improved the intestinal mucosal barrier function of juvenile turbot, Scophthalmus maximus. Aquaculture 486, 98106.CrossRefGoogle Scholar
Yang, P, Hu, H, Li, Y, Ai, Q, Zhang, W, Zhang, Y and Mai, K (2019) Effect of dietary xylan on immune response, tight junction protein expression and bacterial community in the intestine of juvenile turbot (Scophthalmus maximus L.). Aquaculture 512, 734361.CrossRefGoogle Scholar
Yao, Y-Y, Chen, D-D, Cui, Z-W, Zhang, X-Y, Zhou, Y-Y, Guo, X, Li, A-H and Zhang, Y-A (2019) Oral vaccination of tilapia against Streptococcus agalactiae using Bacillus subtilis spores expressing Sip. Fish and Shellfish Immunology 86, 9991008.CrossRefGoogle ScholarPubMed
Ye, JD, Wang, K, Li, FD and Sun, YZ (2011) Single or combined effects of fructo-and mannanoligosaccharide supplements and Bacillus clausii on the growth, feed utilization, body composition, digestive enzyme activity, innate immune response and lipid metabolism of the Japanese flounder Paralichthys olivaceus. Aquaculture Nutrition 17, e902e911.CrossRefGoogle Scholar
Yi, C-C, Liu, C-H, Chuang, K-P, Chang, Y-T and Hu, S-Y (2019) A potential probiotic Chromobacterium aquaticum with bacteriocin-like activity enhances the expression of indicator genes associated with nutrient metabolism, growth performance and innate immunity against pathogen infections in zebrafish (Danio rerio). Fish and Shellfish Immunology 93, 124134.CrossRefGoogle ScholarPubMed
Yossa, R, Levesque, S, Groman, DB and Lora, JH (2018) Preliminary evaluation of purified lignin and hemicellulose as prebiotics candidates for Atlantic Salmon, Salmo salar L. Journal of Applied Aquaculture 30, 256271.CrossRefGoogle Scholar
Zaczek, M, Weber-Dąbrowska, B and Górski, A (2020) Phages as a cohesive prophylactic and therapeutic approach in aquaculture systems. Antibiotics 9, 564.CrossRefGoogle ScholarPubMed
Zhang, C-N, Li, X-F, Xu, W-N, Jiang, G-Z, Lu, K-L, Wang, L-N and Liu, W-B (2013) Combined effects of dietary fructooligosaccharide and Bacillus licheniformis on innate immunity, antioxidant capability and disease resistance of triangular bream (Megalobrama terminalis). Fish and Shellfish Immunology 35, 13801386.CrossRefGoogle ScholarPubMed
Zhang, Q, Yu, H, Tong, T, Tong, W, Dong, L, Xu, M and Wang, Z (2014) Dietary supplementation of Bacillus subtilis and fructooligosaccharide enhance the growth, non-specific immunity of juvenile ovate pompano, Trachinotus ovatus and its disease resistance against Vibrio vulnificus. Fish and Shellfish Immunology 38, 714.CrossRefGoogle ScholarPubMed
Zhao, D, Wu, S, Feng, W, Jakovlić, I, Tran, NT and Xiong, F (2020) Adhesion and colonization properties of potentially probiotic Bacillus paralicheniformis strain FA6 isolated from grass carp intestine. Fisheries Science 86, 153161.CrossRefGoogle Scholar
Zhou, Z, Shi, P, Yao, B, He, S, Su, Y and Ding, Z (2007) Comparison of the predominant bacterial community structure in the gastrointestinal wall between Lutjanus sebea and Ephippus orbis based in 16S sRNA PCR-DGGE fingerprint. Acta Hydrobiologica Sinica 31, 682688.Google Scholar
Zhou, S, Zhang, A, Yin, H and Chu, W (2016) Bacillus sp. QSI-1 modulate quorum sensing signals reduce Aeromonas hydrophila level and alter gut microbial community structure in fish. Frontiers in Cellular and Infection Microbiology 6, 184.CrossRefGoogle ScholarPubMed
Zhou, F, Jiang, X, Wang, T, Zhang, B and Zhao, H (2018) Lycium barbarum polysaccharide (LBP): a novel prebiotics candidate for Bifidobacterium and Lactobacillus. Frontiers in Microbiology 9, 1034.CrossRefGoogle Scholar
Zibiene, G and Zibas, A (2019) Impact of commercial probiotics on growth parameters of European catfish (Silurus glanis) and water quality in recirculating aquaculture systems. Aquaculture International 27, 17511766.CrossRefGoogle Scholar
Zou, HK, Hoseinifar, SH, Miandare, HK and Hajimoradloo, A (2016) Agaricus bisporus powder improved cutaneous mucosal and serum immune parameters and up-regulated intestinal cytokines gene expression in common carp (Cyprinus carpio) fingerlings. Fish and Shellfish Immunology 58, 380386.Google Scholar