Probing into the Impacts of Endogenous and Exogenous Short-Chain Fatty Acids (SCFAS) in Fish Health and Growth – A Review

Kalaiselvan, Pandi; Malarvizhi, Kavitha; Ranjan, Amit

doi:10.2478/aoas-2024-0050

Abstract

Short-chain fatty acids (SCFAs) are small organic acids that exist in the fish gastrointestinal tract, mainly acetate, propionate, and butyrate. These SCFAs are produced through anaerobic fermentation of dietary non-digestible carbohydrates by gut microbes. Though enough studies have been devoted to showcasing the potential of SCFAs in human nutrition, the research on their production, potential, and existence in fish has been comparatively limited until recently. This review aims to provide a comprehensive overview of the current knowledge regarding SCFAs in aquaculture. It starts with commenting on the different sources, such as substrate and microbial species that are responsible for the production of SCFAs and their transportation and ends up depicting the relationship between biofloc technology and SCFA production. This review also discusses the factors influencing SCFA production, such as environment, diet, and feeding habits of fish. Furthermore, the biological functions of SCFAs have been highlighted, and critical findings were compiled, including immunomodulatory effects, physiological response, gut health, and immunity.

References

Abdel-Mohsen H.H., Wassef E.A., El-Bermawy N.M., Abdel-Meguid N.E., Saleh N.E., Barakat K.M., Shaltout O.E. (2018). Advantageous effects of dietary butyrate on growth, immunity response, intestinal microbiota and histomorphology of European seabass (Dicentrarchus labrax) fry. Egypt. J. Aquat. Biol. Fish., 22: 93–110.
Search in Google Scholar Back to article
Abell G.C., Cooke C.M., Bennett C.N., Conlon M.A., McOrist A.L. (2008). Phylotypes related to Ruminococcus bromii are abundant in the large bowel of humans and increase in response to a diet high in resistant starch. FEMS Microb. Ecol., 66: 505–515.
Search in Google Scholar Back to article
Adel M., El-Sayed A.F.M., Yeganeh S., Dadar M., Giri S.S. (2017). Effect of potential probiotic Lactococcus lactis subsp. lactis on growth performance, intestinal microbiota, digestive enzyme activities, and disease resistance of Litopenaeus vannamei. Prob. Antimicrob. Proteins., 9: 150–156.
Search in Google Scholar Back to article
Allameh S.K., Ringø E., Yusoff F.M., Daud H.M., Ideris A. (2017). Dietary supplement of Enterococcus faecalis on digestive enzyme activities, short-chain fatty acid production, immune system response and disease resistance of Javanese carp (Puntius gonionotus, Bleeker 1850). Aquacult. Nutr., 23: 331–338.
Search in Google Scholar Back to article
Annunziata G., Arnone A., Ciampaglia R., Tenore G.C., Novellino E. (2020). Fermentation of foods and beverages as a tool for increasing availability of bioactive compounds. Focus on short-chain fatty acids. Foods, 9: 999.
Search in Google Scholar Back to article
Asaduzzaman Md., Iehata S., Akter S., Kader Md.A., Ghosh S.K., Khan M.N.A., Abol-Munafi A.B. (2018). Effects of host gut-derived probiotic bacteria on gut morphology, microbiota composition and volatile short chain fatty acids production of Malaysian mahseer Tor tambroides. Aquacult. Rep., 9: 53–61.
Search in Google Scholar Back to article
Avnimelech Y. (2009). Biofloc technology: a practical guide book. World Aquaculture Society publication, Baton Rouge, USA, pp. 182.
Search in Google Scholar Back to article
Baek G., Saeed M., Choi H.-K. (2021). Duckweeds: Their utilization, metabolites and cultivation. Appl. Biol. Chem., 64: 73.
Search in Google Scholar Back to article
Banakar P., Ally K., Lokesh E., Saseendran A., Dominic G., Jaafar J. (2017). In vitro assessment of nutritive value of unconventional feed resource as livestock feed. Int. J. Livest. Res, 7: 159–169.
Search in Google Scholar Back to article
Benjamin J.L., Hedin C.R., Koutsoumpas A., Ng S.C., McCarthy N.E., Hart A.L., Kamm M.A., Sanderson J.D., Knight S.C., Forbes A., Stagg A.J., Whelan K., Lindsay J.O. (2011). Randomised, double-blind, placebo-controlled trial of fructo-oligosaccharides in active Crohn’s disease. Gut, 60: 923–929.
Search in Google Scholar Back to article
Bhatt P., Kumaresan V., Palanisamy R., Ravichandran G., Mala K.,
Search in Google Scholar Back to article
Amin S.M.N., Arshad A., Yusoff F.Md., Arockiaraj J. (2018). A mini review on immune role of chemokines and its receptors in snakehead murrel Channa striatus. Fish Shellfish Immunol., 72: 670–678.
Search in Google Scholar Back to article
Bolívar Ramírez N.C., Rodrigues M.S., Guimarães A.M., Guertler C., Rosa J.R., Seiffert W.Q., Andreatta E.R., Vieira F.N. (2017). Effect of dietary supplementation with butyrate and probiotic on the survival of Pacific white shrimp after challenge with Vibrio alginolyticus. Rev. Bras. de Zootec., 46: 471–477.
Search in Google Scholar Back to article
Canfora E.E., Jocken J.W., Blaak E.E. (2015). Short-chain fatty acids in control of body weight and insulin sensitivity. Nat. Rev. Endocrinol., 11: 577–591.
Search in Google Scholar Back to article
Castillo S., Rosales M., Pohlenz C., Gatlin D.M. (2014). Effects of organic acids on growth performance and digestive enzyme activities of juvenile red drum Sciaenops ocellatus. Aquaculture, 433: 6–12.
Search in Google Scholar Back to article
Chen Y., Wang C., Xu C. (2020). Nutritional evaluation of two marine microalgae as feedstock for aquafeed. Aquacult. Res., 51: 946–956.
Search in Google Scholar Back to article
Cholan P.M., Han A., Woodie B.R., Watchon M., Kurz A.R., Laird A.S., Britton W.J., Ye L., Holmes Z.C., McCann J.R., David L.A., Rawls J.F., Oehlers S.H. (2020). Conserved anti-inflammatory effects and sensing of butyrate in zebrafish. Gut Microb., 12: 1824563.
Search in Google Scholar Back to article
Christiansen R., Lückstädt C. (2008). Effects of different dosages of potassium diformate in fishmeal on the performance of Atlantic salmon Salmo salar. Abstract CD-Rom. World Aquacult. Soc., pp. 19–23.
Search in Google Scholar Back to article
Chuchird N., Rorkwiree P., Rairat T. (2015). Effect of dietary formic acid and astaxanthin on the survival and growth of Pacific white shrimp (Litopenaeus vannamei) and their resistance to Vibrio parahaemolyticus. Springer Plus, 4: 1–12.
Search in Google Scholar Back to article
Ciarlo E., Heinonen T., Herderschee J., Fenwick C., Mombelli M., Le Roy D., Roger T. (2016). Impact of the microbial derived short chain fatty acid propionate on host susceptibility to bacterial and fungal infections in vivo. Sci. Rep., 6: 1.
Search in Google Scholar Back to article
Corrêa-Oliveira R., Fachi J.L., Vieira A., Sato F.T., Vinolo M.A.R. (2016). Regulation of immune cell function by short-chain fatty acids. Clin. Transl. Immunol., 5: e73.
Search in Google Scholar Back to article
Cruz C.P.P. de la Alap L.P.B., Manalili E.V., Rafael R.R., Tolentino P.D.H. (2023). Prebiotic potential of Azolla pinnata (R.Br.) and dietary inclusion effect of pulverised azolla on the growth performance of milkfish fingerlings. J. Fish., 11: 1.
Search in Google Scholar Back to article
da Silva B.C., do Nascimento Vieira F., Pedreira Mouriño J.L., Ferreira G.S., Quadros Seiffert W. (2013). Salts of organic acids selection by multiple characteristics for marine shrimp nutrition. Aquaculture, 384: 104–110.
Search in Google Scholar Back to article
da Silva B.C., do Nascimento Vieira F., Pedreira Mouriño J.L., Bolivar N., Quadros Seiffert W. (2016). Butyrate and propionate improve the growth performance of Litopenaeus vannamei. Aquacult. Res., 47: 612–623.
Search in Google Scholar Back to article
Dawood M.A. (2021). Nutritional immunity of fish intestines: Important insights for sustainable aquaculture. Rev. Aquacult., 13: 642–663.
Search in Google Scholar Back to article
Dawood M.A., Eweedah N.M., Elbialy Z.I., Abdelhamid A.I. (2020). Dietary sodium butyrate ameliorated the blood stress biomarkers, heat shock proteins, and immune response of Nile tilapia (Oreochromis niloticus) exposed to heat stress. J. Therm. Biol., 88: 102500.
Search in Google Scholar Back to article
De Schryver P., Sinha A.K., Kunwar P.S., Baruah K., Verstraete W., Boon N., De Boeck G., Bossier P. (2010). Poly-β-hydroxybutyrate (PHB) increases growth performance and intestinal bacterial range-weighted richness in juvenile European sea bass, Dicentrarchus labrax. Appl. Microbiol. Biotechnol., 86: 1535–1541.
Search in Google Scholar Back to article
Den Besten G., Van Eunen K., Groen A.K., Venema K., Reijngoud D.J., Bakker B.M. (2013). The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res., 54: 2325–2340.
Search in Google Scholar Back to article
Desai A.R., Links M.G., Collins S.A., Mansfield G.S., Drew M.D., Van Kessel A.G., Hill J.E. (2012). Effects of plant-based diets on the distal gut microbiome of rainbow trout (Oncorhynchus mykiss). Aquaculture, 350: 134–142.
Search in Google Scholar Back to article
Duan Y., Zhang Y., Dong H., Wang Y., Zheng X., Zhang J. (2017). Effect of dietary Clostridium butyricum on growth, intestine health status and resistance to ammonia stress in Pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immunol., 65: 25–33.
Search in Google Scholar Back to article
Ebrahimi M., Daeman N.H., Chong C.M., Karami A., Kumar V., Hoseinifar S.H., Romano N. (2017). Comparing the effects of different dietary organic acids on the growth, intestinal short-chain fatty acids, and liver histopathology of red hybrid tilapia (Oreochromis sp.) and potential use of these as preservatives. Fish Physiol. Biochem., 43: 1195–1207.
Search in Google Scholar Back to article
Elala N.M.A., Ragaa N.M. (2015). Eubiotic effect of a dietary acidifier (potassium diformate) on the health status of cultured Oreochromis niloticus. J. Adv. Res., 6: 621–629.
Search in Google Scholar Back to article
El-Sayed A.F.M. (2021). Use of biofloc technology in shrimp aqua-culture: a comprehensive review, with emphasis on the last decade. Rev. Aquacult., 13: 676–705.
Search in Google Scholar Back to article
El-Sayed Ali T., El-Sayed A.M., Eissa M.A.R., Hanafi H.M. (2018). Effects of dietary Biogen and sodium butyrate on hematological parameters, immune response, and histological characteristics of Nile tilapia (Oreochromis niloticus) fingerlings. Aquacult. Int., 26: 139–150.
Search in Google Scholar Back to article
Estensoro I., Ballester-Lozano G., Benedito-Palos L., Grammes F., Martos-Sitcha J.A., Mydland L.T., Calduch-Giner J.A., Fuentes J., Karalazos V., Ortiz A. (2016). Dietary butyrate helps to restore the intestinal status of a marine teleost (Sparus aurata) fed extreme diets low in fish meal and fish oil. PLoS One, 11: e0166564.
Search in Google Scholar Back to article
Fabay R.V., Tumbokon B.L., Serrano Jr A.E. (2020). Effects of dietary pH and acid source on growth and feed efficiency of the Nile tilapia, Oreochromis niloticus fry. Isr. J. Aquacult., 72: 1114685.
Search in Google Scholar Back to article
Fabay R.V., Serrano Jr A.E., Alejos M.S., Fabay J.V. (2022). Effects of dietary acidification and acid source on fish growth and feed efficiency. World Acad. Sci. J., 4: 1–15.
Search in Google Scholar Back to article
Fernández J., Redondo-Blanco S., Gutiérrez-del-Río I., Miguélez E.M., Villar C.J., Lombó F. (2016). Colon microbiota fermentation of dietary prebiotics towards short-chain fatty acids and their roles as anti-inflammatory and antitumour agents: A review. J. Funct. Foods., 25: 511–522.
Search in Google Scholar Back to article
Flint H.J., Duncan S.H., Scott K.P., Louis P. (2015). Links between diet, gut microbiota composition and gut metabolism. Proc. Nutr. Soc., 74: 13–22.
Search in Google Scholar Back to article
Fowler E.C., Poudel P., White B., St-Pierre B., Brown M. (2021). Effects of a bioprocessed soybean meal ingredient on the intestinal microbiota of hybrid striped bass, Morone chrysops × M. saxatilis. Microorganisms, 9: 5.
Search in Google Scholar Back to article
Freitag M. (2007). Organic acids and salts promote performance and health in animal husbandry. Acidifiers Anim. Nutr., 31: 131–139.
Search in Google Scholar Back to article
Fuller R. (1989). Probiotics in man and animals. J. Appl. Bacteriol., 66: 365–378.
Search in Google Scholar Back to article
Gallo B.D., Farrell J.M., Leydet B.F. (2020). Fish gut microbiome: a primer to an emerging discipline in the fisheries sciences. Fisheries, 45: 271–282.
Search in Google Scholar Back to article
Gao Y., Storebakken T., Shearer K.D., Penn M., Øverland M. (2011). Supplementation of fishmeal and plant protein-based diets for rainbow trout with a mixture of sodium formate and butyrate. Aquaculture, 311: 233–240.
Search in Google Scholar Back to article
Gatesoupe F.J., Huelvan C., Le Bayon N., Sévère A., Aasen I.M., Degnes K.F., Mazurais D., Panserat S., Zambonino-Infante J.L., Kaushik S.J. (2014). The effects of dietary carbohydrate sources and forms on metabolic response and intestinal microbiota in sea bass juveniles, Dicentrarchus labrax. Aquaculture, 422: 47–53.
Search in Google Scholar Back to article
Geraylou Z., Souffreau C., Rurangwa E., D’Hondt S., Callewaert L., Courtin C.M., Delcour J.A., Buyse J., Ollevier F. (2012). Effects of arabinoxylan-oligosaccharides (AXOS) on juvenile Siberian sturgeon (Acipenser baerii) performance, immune responses and gastrointestinal microbial community. Fish Shellfish Immunol., 33: 718–724.
Search in Google Scholar Back to article
Gorkiewicz G., Thallinger G.G., Trajanoski S., Lackner S., Stocker G., Hinterleitner T., Gülly C., Högenauer C. (2013). Alterations in the colonic microbiota in response to osmotic diarrhea. PloS One, 8: e55817.
Search in Google Scholar Back to article
Guerreiro I., Oliva-Teles A., Enes P. (2018 a). Prebiotics as functional ingredients: Focus on Mediterranean fish aquaculture. Rev. Aqua-cult., 10: 800–832.
Search in Google Scholar Back to article
Guerreiro I., Serra C.R., Oliva-Teles A., Enes P. (2018 b). Short communication: gut microbiota of European sea bass (Dicentrarchus labrax) is modulated by short-chain fructooligosaccharides and xylooligosaccharides. Aquacult Int., 26: 279–288.
Search in Google Scholar Back to article
Hafer A., Krämer S., Duncker S., Krüger M., Manns M.P., Bischoff S.C. (2007). Effect of oral lactulose on clinical and immunohisto-chemical parameters in patients with inflammatory bowel disease: a pilot study. BMC Gastroenterol., 7: 1–11.
Search in Google Scholar Back to article
Hanai H., Kanauchi O., Mitsuyama K., Andoh A., Takeuchi K., Taka-yuki I., Araki Y., Fujiyama Y., Toyonaga A., Sata M., Kojima A., Fukuda M., Bamba T. (2004). Germinated barley foodstuff prolongs remission in patients with ulcerative colitis. Int. J. Mol. Med., 13: 643–647.
Search in Google Scholar Back to article
Hao Y.T., Wu S.G., Jakovlić I., Zou H., Li W.X., Wang G.T. (2017). Impacts of diet on hindgut microbiota and short-chain fatty acids in grass carp (Ctenopharyngodon idellus). Aquacult. Res., 48: 5595–5605.
Search in Google Scholar Back to article
Hassaan M.S., Wafa M.A., Soltan M.A., Goda A.S., Mogheth N.M.A. (2014). Effect of dietary organic salts on growth, nutrient digestibility, mineral absorption and some biochemical indices of Nile tilapia. Oreochromis niloticus, World Appl. Sci. J., 29: 47–55.
Search in Google Scholar Back to article
Hedemann M.S., Bach Knudsen K.E. (2007). Resistant starch for weaning pigs – effect on concentration of short chain fatty acids in digesta and intestinal morphology. Livest. Sci., 108: 175–177.
Search in Google Scholar Back to article
Hemalatha R., Ouwehand A.C., Saarinen M.T., Prasad U.V., Swetha K., Bhaskar V. (2017). Effect of probiotic supplementation on total lactobacilli, bifidobacteria and short chain fatty acids in 2–5-year-old children. Microb. Ecol. Health Disease, 28: 1298340.
Search in Google Scholar Back to article
Hoseinifar S.H., Zoheiri F., Caipang C.M. (2016). Dietary sodium propionate improved performance, mucosal and humoral immune responses in Caspian white fish (Rutilus frisii kutum) fry. Fish Shellfish Immunol., 55: 523–528.
Search in Google Scholar Back to article
Hoseinifar S.H., Sun Y.Z., Caipang C.M. (2017). Short-chain fatty acids as feed supplements for sustainable aquaculture: An updated view. Aquacult. Res., 48: 1380–1391.
Search in Google Scholar Back to article
Huan D., Li X., Chowdhury M.A.K., Yang H., Liang G., Leng X. (2018). Organic acid salts, protease and their combination in fish meal-free diets improved growth, nutrient retention and digestibility of tilapia (Oreochromis niloticus × O. aureus). Aquacult. Nutr., 24: 1813–1821.
Search in Google Scholar Back to article
Ige B.A. (2013). Probiotics use in intensive fish farming. Afr. J. Microb. Res., 7: 2701–2711.
Search in Google Scholar Back to article
Jesus G.F., Pereira S.A., Owatari M.S., Addam K., Silva B.C., Sterzelecki F.C., Sugai J.K., Cardoso L., Jatobá A., Mouriño J.L. (2019). Use of protected forms of sodium butyrate benefit the development and intestinal health of Nile tilapia during the sexual reversion period. Aquaculture, 504: 326–333.
Search in Google Scholar Back to article
Joossens M., De Preter V., Ballet V., Verbeke K., Rutgeerts P., Vermeire S. (2012). Effect of oligofructose-enriched inulin (OF-IN) on bacterial composition and disease activity of patients with Crohn’s disease: results from a double-blinded randomised controlled trial. Gut, 61: 958–958.
Search in Google Scholar Back to article
Kanauchi O., Mitsuyama K., Homma T., Takahama K., Fujiyama Y., Andoh A., Araki Y., Suga T., Hibi T., Naganuma M., Asakura H., Nakano H., Shimoyama T., Hida N., Haruma K., Koga H., Sata M., Tomiyasu N., Toyonaga A., Fukuda M., Kojima A., Bamba T. (2003). Treatment of ulcerative colitis patients by long-term administration of germinated barley foodstuff: multi-center open trial. Int. J. Mol. Med., 12: 701–704.
Search in Google Scholar Back to article
Khanjani M.H., Mohammadi A., Emerenciano M.G.C. (2022). Microorganisms in biofloc aquaculture system. Aquacult Rep., 26: 101300.
Search in Google Scholar Back to article
Kihara M. (2008). Production of short-chain fatty acids from dietary lactosucrose in the hindgut and its effects on digestive organs of a marine teleost, red sea bream Pagrus major. Aquacult. Sci., 56: 327–333.
Search in Google Scholar Back to article
Kles K.A., Chang E.B. (2006). Short-chain fatty acids impact on intestinal adaptation, inflammation, carcinoma, and failure. Gastroenterology, 130: S100–S105.
Search in Google Scholar Back to article
Koh A., De Vadder F., Kovatcheva-Datchary P., Bäckhed F. (2016). From dietary fiber to host physiology: Short-chain fatty acids as key bacterial metabolites. Cell, 165: 1332–1345.
Search in Google Scholar Back to article
Krajmalnik-Brown R., Ilhan Z.E., Kang D.W., DiBaise J.K. (2012). Effects of gut microbes on nutrient absorption and energy regulation. Nutr. Clin. Pract., 27: 201–214.
Search in Google Scholar Back to article
Kumar S., Sahu N.P., Gupta S., Deo A.D., Shamna N., Ranjan A. (2017). Inclusion level of deoiled rice bran (DORB) in the diet of Labeo rohita (Hamilton, 1882) fingerlings: Effect on growth and gene expression of IGF-I and IGF-II. Aquaculture, 481: 211–217.
Search in Google Scholar Back to article
Leenhouwers J.I., Pellikaan W.F., Huizing H.F.A., Coolen R.O.M., Verreth J.A.J., Schrama J.W. (2008). Fermentability of carbohydrates in an in vitro batch culture method using inocula from Nile tilapia (Oreochromis niloticus) and European sea bass (Dicentrarchus labrax). Aquacult. Nutr., 14: 523–532.
Search in Google Scholar Back to article
Ley R.E., Lozupone C.A., Hamady M., Knight R., Gordon J.I. (2008). Worlds within worlds: Evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol., 6: 10.
Search in Google Scholar Back to article
Li S., Sang C., Turchini G.M., Wang A., Zhang J., Chen N. (2020). Starch in aquafeeds: The benefits of a high amylose to amylopectin ratio and resistant starch content in diets for the carnivorous fish, largemouth bass (Micropterus salmoides). Br. J. Nutr., 124: 1145–1155.
Search in Google Scholar Back to article
Li S., Heng X., Guo L., Lessing D. J., Chu W. (2022). SCFAs improve disease resistance via modulate gut microbiota, enhance immune response and increase antioxidative capacity in the host. Fish Shellfish Immunol., 120: 560–568.
Search in Google Scholar Back to article
Li T., Long M., Li H., Gatesoupe F.J., Zhang X., Zhang Q., Feng D., Li A. (2017). Multi-omics analysis reveals a correlation between the host phylogeny, gut microbiota and metabolite profiles in cyprinid fishes. Front. Microbiol., 8: 454.
Search in Google Scholar Back to article
Liebert F., Mohamed K., Lückstädt C. (2010). Effects of diformates on growth and feed utilization of all male Nile tilapia fingerlings (Oreochromis niloticus) reared in tank culture. XIV International Symposium on Fish Nutrition and Feeding, Qingdao, China, Book of Abstracts, p. 190.
Search in Google Scholar Back to article
Lim C., Klesius P.H., Luckstadt C. (2010). Effects of dietary levels of potassium diformate on growth, feed utilization and resistance to Streptococcus iniae of Nile tilapia, Oreochromis niloticus. Proc. 14th International Symposium on Fish Nutrition and Feeding. Qingdao, China, p. 472.
Search in Google Scholar Back to article
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.
Search in Google Scholar Back to article
Liu M., Guo W., Wu F., Qu Q., Tan Q., Gong W. (2017). Dietary supplementation of sodium butyrate may benefit growth performance and intestinal function in juvenile grass carp (Ctenopharyngodon idellus). Aquacult. Res., 48: 4102–4111.
Search in Google Scholar Back to article
Liu W., Yang Y., Zhang J., Gatlin D.M., Ringø E., Zhou Z. (2014). Effects of dietary microencapsulated sodium butyrate on growth, intestinal mucosal morphology, immune response and adhesive bacteria in juvenile common carp (Cyprinus carpio) pre-fed with or without oxidised oil. Bri. J. Nutr., 112: 15–29.
Search in Google Scholar Back to article
Liu P., Wang Y., Yang G., Zhang Q., Meng L., Xin Y., Jiang X. (2021). The role of short-chain fatty acids in intestinal barrier function, inflammation, oxidative stress, and colonic carcinogenesis. Pharmacol. Res., 165: 105420.
Search in Google Scholar Back to article
Liu Y., Chen Z., Dai J., Yang P., Xu W., Ai Q., Zhang W., Zhang Y., Zhang Y., Mai, K. (2019). Sodium butyrate supplementation in high-soybean meal diets for turbot (Scophthalmus maximus L.): Effects on inflammatory status, mucosal barriers and microbiota in the intestine. Fish Shellfish Immunol., 88: 65–75.
Search in Google Scholar Back to article
Llewellyn M.S., Boutin S., Hoseinifar S.H., Derome N. (2014). Teleost microbiomes: The state of the art in their characterization, manipulation and importance in aquaculture and fisheries. Front. Microbiol., 5: 207.
Search in Google Scholar Back to article
Lückstädt C. (2008 a). The use of acidifiers in fish nutrition. CABI Rev 3(044), Perspect. Agric. Vet., 3: 1–8.
Search in Google Scholar Back to article
Lückstädt C. (2008 b). Effect of organic acid containing additives in worldwide aquaculture–sustainable production the non-antibiotic way. Acidifiers in Animal Nutrition.
Search in Google Scholar Back to article
Magouz F.I., Essa M., Mansour M., Paray B.A., Van Doan H., Dawood M.A. (2020). Supplementation of AQUAGEST as a source of medium-chain fatty acids and taurine improved the growth performance, intestinal histomorphology, and immune response of common carp fed low fish meal diets. Ann. Anim. Sci., 20: 1453–1469.
Search in Google Scholar Back to article
Martin-Gallausiaux C., Marinelli L., Blottière H.M., Larraufie P., Lapaque N. (2021). SCFA: Mechanisms and functional importance in the gut. Proc. Nutr. Soc., 80: 37–49.
Search in Google Scholar Back to article
Martins N., Magalhães R., Vieria L., Couto A., Serra C.R., Maia M.R.G, Fonseca A.J.M., Cabrita A.R.J., Pousão-Ferreira P., Castro C., Peres H., Oliva-Teles A. (2023). Dietary oleic acid supplementation improves feed efficiency and modulates fatty acid profile and cell signaling pathway in European sea bass (Dicentrarchus labrax) juveniles fed high-lipid diets. Aquaculture, 576: 739870.
Search in Google Scholar Back to article
McFarland LV. (2014). Use of probiotics to correct dysbiosis of normal microbiota following disease or disruptive events: a systematic review. BMJ Open, 4(8): e005047.
Search in Google Scholar Back to article
Michl S.C., Ratten J.M., Beyer M., Hasler M., LaRoche J., Schulz C. (2017). The malleable gut microbiome of juvenile rainbow trout (Oncorhynchus mykiss): Diet-dependent shifts of bacterial community structures. PloS One, 12: e0177735.
Search in Google Scholar Back to article
Montalban-Arques A., De Schryver P., Bossier P., Gorkiewicz G., Mulero V., Gatlin D.M., Galindo-Villegas J. (2015). Selective manipulation of the gut microbiota improves immune status in vertebrates. Front. Immunol., 6: 153393.
Search in Google Scholar Back to article
Modesto M., D’Aimmo M.R., Stefanini I., Trevisi P., De Filippi S., Casini L., Mazzoni M., Bosi P., & Biavati B. (2009). A novel strategy to select Bifidobacterium strains and prebiotics as natural growth promoters in newly weaned pigs. Livest. Sci., 122: 248–258.
Search in Google Scholar Back to article
Morken T., Kraugerud O.F., Barrows F.T., Sørensen M., Storebakken T., Øverland M. (2011). Sodium diformate and extrusion temperature affect nutrient digestibility and physical quality of diets with fish meal and barley protein concentrate for rainbow trout (Oncorhynchus mykiss). Aquaculture, 317: 138–145.
Search in Google Scholar Back to article
Morken T., Moyano F.J., Márquez L., Sørensen M., Mydland L.T., Øverland M. (2012). Effects of autoclaving and sodium diformate supplementation to diets on amino acid composition, in vivo digestibility in mink (Neovison vison) and in vitro bioavailability using digestive enzymes from Atlantic salmon (Salmo salar). Anim. Feed Sci. Technol., 178: 84–94.
Search in Google Scholar Back to article
Morrison D.J., Preston T. (2016). Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes, 7: 189–200.
Search in Google Scholar Back to article
Mountfort D.O., Campbell J., Clements K.D. (2002). Hindgut fermentation in three species of marine herbivorous fish. Appl. Environ. Microbiol., 68: 1374–1380.
Search in Google Scholar Back to article
Mua J.P., Jackson D.S. (1997). Fine structure of corn amylose and amylopectin fractions with various molecular weights. J. Agri. Food Chem., 45: 3840–3847.
Search in Google Scholar Back to article
Nawaz A., Bakhsh javaid A., Irshad S., Hoseinifar S.H., Xiong H. (2018). The functionality of prebiotics as immunostimulant: Evidences from trials on terrestrial and aquatic animals. Fish Shellfish Immunol., 76: 272–278.
Search in Google Scholar Back to article
Nayak S.K. (2010). Role of gastrointestinal microbiota in fish. Aqua-cult. Res., 41: 1553–1573.
Search in Google Scholar Back to article
Negesse T., Makkar H.P.S., Becker K. (2009). Nutritive value of some non-conventional feed resources of Ethiopia determined by chemical analyses and an in vitro gas method. Anim. Feed Sci. Technol., 154: 204–217.
Search in Google Scholar Back to article
Ng W.K., Koh C.B. (2017). The utilization and mode of action of organic acids in the feeds of cultured aquatic animals. Rev. Aqua-cult., 9: 342–368.
Search in Google Scholar Back to article
Ng W.K., Koh C.B., Sudesh K., Siti-Zahrah A. (2009). Effects of dietary organic acids on growth, nutrient digestibility and gut microflora of red hybrid tilapia, Oreochromis sp., and subsequent survival during a challenge test with Streptococcus agalactiae. Aquacult. Res., 40: 1490–1500.
Search in Google Scholar Back to article
Nguyen T.L., Chun W.K., Kim A., Kim N., Roh H.J., Lee Y., Yi M., Kim S., Park C.I., Kim D.H. (2018). Dietary probiotic effect of Lactococcus lactis WFLU12 on low-molecular-weight metabolites and growth of olive flounder (Paralichythys olivaceus). Front. Microbiol., 9: 398882.
Search in Google Scholar Back to article
Nhan D.T., Wille M., De Schryver P., Defoirdt T., Bossier P., Sorgeloos P. (2010). The effect of poly β-hydroxybutyrate on larviculture of the giant freshwater prawn Macrobrachium rosenbergii. Aquaculture, 302: 76–81.
Search in Google Scholar Back to article
Nimalan N., Sørensen S.L., Fečkaninová A., Koščová J., Mudroňová D., Gancarčíková S., Vatsos I.N., Bisa S., Kiron V., Sørensen M. (2023). Supplementation of lactic acid bacteria has positive effects on the mucosal health of Atlantic salmon (Salmo salar) fed soybean meal. Aquacult. Rep., 28: 101461.
Search in Google Scholar Back to article
Nuez-Ortín W.G. (2013). Natural growth promoters in aquaculture practices. New additives and ingredients in the formulation of aquafeeds. Centro Tecnológico del Mar-Fundación, Pontevedra, Spain, pp. 9–26.
Search in Google Scholar Back to article
Ohira H., Tsutsui W., Fujioka Y. (2017). Are short chain fatty acids in gut microbiota defensive players for inflammation and atherosclerosis? J. Atheroscler. Thromb., 24: 660–672.
Search in Google Scholar Back to article
Owen M.A.G., Waines P., Bradley G., Davies S. (2006). The effect of dietary supplementation of sodium butyrate on the growth and microflora of Clarias gariepinus (Burchell 1822). Proc. XII International Symposium Fish Nutrition and Feeding, Biarritz, France, p. 147.
Search in Google Scholar Back to article
Papadimitriou K., Zoumpopoulou G., Foligné B., Alexandraki V., Kazou M., Pot B., Tsakalidou E. (2015). Discovering probiotic microorganisms: in vitro, in vivo, genetic and omics approaches. Front. Microbiol., 6: 58.
Search in Google Scholar Back to article
Piazzon M.C., Calduch-Giner J.A., Fouz B., Estensoro I., Simó-Mirabet P., Puyalto M., Karalazos V., Palenzuela O., Sitjà-Bobadilla A., Pérez-Sánchez J. (2017). Under control: How a dietary additive can restore the gut microbiome and proteomic profile, and improve disease resilience in a marine teleostean fish fed vegetable diets. Microbiome, 5: 164.
Search in Google Scholar Back to article
Pourmozaffar S., Hajimoradloo A., Miandare H.K. (2017). Dietary effect of apple cider vinegar and propionic acid on immune related transcriptional responses and growth performance in white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol., 60: 65–71.
Search in Google Scholar Back to article
Ramnani P., Chitarrari R., Tuohy K., Grant J., Hotchkiss S., Philp K., Campbell R., Gill C., Rowland I. (2012). In vitro fermentation and prebiotic potential of novel low molecular weight polysaccharides derived from agar and alginate seaweeds. Anaerobe, 18: 1–6.
Search in Google Scholar Back to article
Reda R.M., Mahmoud R., Selim K.M., El-Araby I.E. (2016). Effects of dietary acidifiers on growth, hematology, immune response and disease resistance of Nile tilapia, Oreochromis niloticus. Fish Shellfish Immunol., 50: 255–262.
Search in Google Scholar Back to article
Reichardt N., Vollmer M., Holtrop G., Farquharson F.M., Wefers D., Bunzel M., Duncan S.H., Drew J.E., Williams L.M., Milligan G. (2018). Specific substrate-driven changes in human faecal microbiota composition contrast with functional redundancy in short-chain fatty acid production. Int. Soc. Microb. Ecol. J., 12: 610–622.
Search in Google Scholar Back to article
Rimoldi S., Finzi G., Ceccotti C., Girardello R., Grimaldi A., Ascione C., Terova G. (2016). Butyrate and taurine exert a mitigating effect on the inflamed distal intestine of European sea bass fed with a high percentage of soybean meal. Fish. Aquat. Sci., 19: 1–14.
Search in Google Scholar Back to article
Ringø E. (1991). Effects of dietary lactate and propionate on growth and digesta in Arctic charr, Salvelinus alpinus (L.). Aquaculture, 96: 321–333.
Search in Google Scholar Back to article
Ringø E. (1992). Effects of dietary formate and acetate on growth and lipid digestibility in Arctic charr, Salvelinus alpinus (L.). Fisk. Skr. Ser. Ernæring., 5: 17–24.
Search in Google Scholar Back to article
Ringø E., Olsen R.E., Gifstad T. Ø., Dalmo R. A., Amlund H., Hemre G.I., Bakke A.M. (2010). Prebiotics in aquaculture: A review. Aquacult. Nutr., 16: 117–136.
Search in Google Scholar Back to article
Ringø E.Z.Z.V., Zhou Z., Vecino J.G., Wadsworth S., Romero J., Krog-dahl Å., Olsen R.E., Dimitroglou A., Foey A., Davies S., Owen M., Lauzon H.L., Martinsen L.L., De Schryver P., Bossier P., Sperstad S., Merrifield D.L. (2016). Effect of dietary components on the gut microbiota of aquatic animals. A never-ending story? Aquacult. Nutr., 22: 219–282.
Search in Google Scholar Back to article
Ríos-Covián D., Ruas-Madiedo P., Margolles A., Gueimonde M., De Los Reyes-gavilán C.G., Salazar N. (2016). Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol., 7: 185.
Search in Google Scholar Back to article
Robles R., Lozano A.B., Sevilla A., Márquez L., Nuez-Ortín W., Moyano F.J. (2013). Effect of partially protected butyrate used as feed additive on growth and intestinal metabolism in sea bream (Sparus aurata). Fish Physiol. Biochem., 39:1567–1580.
Search in Google Scholar Back to article
Romano N., Simon W., Ebrahimi M., Fadel A.H., Chong C.M., Kamarudin M.S. (2016). Dietary sodium citrate improved oxidative stability in red hybrid tilapia (Oreochromis sp.) but reduced growth, health status, intestinal short chain fatty acids and induced liver damage. Aquaculture, 458: 170–176.
Search in Google Scholar Back to article
Rombout J.H.W.M., Abelli L., Picchietti S., Scapigliati G., Kiron V. (2011). Teleost intestinal immunology. Fish Shellfish Immunol., 31: 616–626.
Search in Google Scholar Back to article
Romero J., Ringø E., Merrifield D.L. (2014). Editors. The gut micro-biota of fish. Aquaculture nutrition: Gut health, probiotics and prebiotics, John Wiley & Sons, Inc. Hoboken, New Jersey, United States, 75–100 pp.
Search in Google Scholar Back to article
Rose D.J., Patterson J.A., Hamaker B.R. (2010). Structural differences among alkali-soluble arabinoxylans from maize (Zea mays), rice (Oryza sativa), and wheat (Triticum aestivum) brans influence human fecal fermentation profiles. J. Agri. Food Chem., 58: 493–499.
Search in Google Scholar Back to article
Roy C.C., Kien C.L., Bouthillier L., Levy E. (2006). Short-chain fatty acids: Ready for prime time? Nutr. Clin. Pract., 21: 351–366.
Search in Google Scholar Back to article
Rurangwa E., Delaedt Y., Geraylou Z., Van De Wiele T., Courtin C.M., Delcour J.A., Ollevier F. (2008). Dietary effect of arabinoxylan oligosaccharides on zootechnical performance and hindgut microbial fermentation in Siberian sturgeon and African catfish. Aqua-culture Europe, Kraków, Poland, 569–570 pp.
Search in Google Scholar Back to article
Safari R., Hoseinifar S.H., Kavandi M. (2016). Modulation of anti-oxidant defense and immune response in zebra fish (Danio rerio) using dietary sodium propionate. Fish Physiol. Biochem., 42: 1733–1739.
Search in Google Scholar Back to article
Sardar P., Shamna N., Sahu N.P. (2020). Acidifiers in aquafeed as an alternate growth promoter: A short review. Anim. Nutr. Feed Technol., 20: 353–366.
Search in Google Scholar Back to article
Shah A.M., Tarfeen N., Mohamed H., Song Y. (2023). Fermented foods: Their health-promoting components and potential effects on gut microbiota. Fermentation, 9: 118.
Search in Google Scholar Back to article
Sellin C. (1998). Short chain fatty acids in health and disease. Aliment. Pharmacol. Ther., 12: 499–507.
Search in Google Scholar Back to article
Simpson H.L., Campbell B.J. (2015). Review article: dietary fibre–microbiota interactions. Aliment. Pharmacol. Ther., 42: 158–179.
Search in Google Scholar Back to article
Subramanian D., Jang Y.H., Kim D.H., Kang B.J., Heo M.S. (2013). Dietary effect of Rubus coreanus ethanolic extract on immune gene expression in white leg shrimp, Penaeus vannamei. Fish Shellfish Immunol., 35: 808–814.
Search in Google Scholar Back to article
Sui L., Liu Y., Sun H., Wille M., Bossier P., De Schryver P. (2014). The effect of poly-β-hydroxybutyrate on the performance of Chinese mitten crab (Eriocheir sinensis Milne-Edwards) zoea larvae. Aquacult. Res., 45: 3.
Search in Google Scholar Back to article
Sullam K.E., Essinger S.D., Lozupone C.A., O’Connor M.P., Rosen G.L., Knight R.O.B., Kilham S.S., Russell J.A. (2012). Environmental and ecological factors that shape the gut bacterial communities of fish: A meta-analysis. Mol. Ecol., 21: 3363–3378.
Search in Google Scholar Back to article
Sylvain F.É., Cheaib B., Llewellyn M., Gabriel Correia T., Barros Fagundes D., Luis Val A., Derome N. (2016). pH drop impacts differentially skin and gut microbiota of the Amazonian fish tambaqui (Colossoma macropomum). Sci. Rep., 6: 32032.
Search in Google Scholar Back to article
Tacon A.G.J., Metian M. (2013). Fish matters: Importance of aquatic foods in human nutrition and global food supply. Rev. Fish. Sci., 21: 22–38.
Search in Google Scholar Back to article
Talwar C., Nagar S., Lal R., Negi R.K. (2018). Fish gut microbiome: Current approaches and future perspectives. Indian J. Microbiol., 58: 397–414.
Search in Google Scholar Back to article
Tian L., Zhou X.Q., Jiang W.D., Liu Y., Wu P., Jiang J., Kuang S.Y., Tang L., Tang W.N., Zhang Y.A., Xie F., Feng L. (2017). Sodium butyrate improved intestinal immune function associated with NF-κB and p38MAPK signalling pathways in young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol., 66: 548–563.
Search in Google Scholar Back to article
Titus E., Ahearn G.A. (1992). Vertebrate gastrointestinal fermentation: Transport mechanisms for volatile fatty acids. Am. J. Physiol., 262: 547–553.
Search in Google Scholar Back to article
Tran N.T., Li Z., Wang S., Zheng H., Aweya J.J., Wen X., Li S. (2020). Progress and perspectives of short-chain fatty acids in aquaculture. Rev. Aquacult., 12: 283–298.
Search in Google Scholar Back to article
Vielma J., Lall S.P. (1997). Dietary formic acid enhances apparent digestibility of minerals in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquacult. Nutr., 3: 265–268.
Search in Google Scholar Back to article
Walker A.W., Duncan S.H., McWilliam Leitch E.C., Child M.W., Flint H.J. (2005). pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl. Environ. Microbiol., 71: 3692–3700.
Search in Google Scholar Back to article
Wang A.R., Ran C., Ringø E., Zhou Z.G. (2018). Progress in fish gastrointestinal microbiota research. Rev. Aquacult., 10: 626–640.
Search in Google Scholar Back to article
Wang J.F., Zhu Y.H., Li D.F., Wang Z., Jensen B.B. (2004). In vitro fermentation of various fiber and starch sources by pig fecal inocula. J. Anim. Sci., 82: 2615–2622.
Search in Google Scholar Back to article
Wang T., Zhang N., Yu X.B., Qiao F., Chen L.Q., Du Z.Y., Zhang M.L. (2021). Inulin alleviates adverse metabolic syndrome and regulates intestinal microbiota composition in Nile tilapia (Oreochromis niloticus) fed with high-carbohydrate diet. Bri. J. Nutr., 126: 161–171.
Search in Google Scholar Back to article
Wassef E.A., Abdel-Momen S.A.G., Saleh N.E.S., Al-Zayat A.M., Ashry A.M. (2017). Is sodium diformate a beneficial feed supplement for European seabass (Dicentrarchus labrax)? Effect on growth performance and health status. Egypt. J. Aquat. Res., 43: 229–234.
Search in Google Scholar Back to article
Wassef E.A., Saleh N.E., Abdel-Meguid N.E., Barakat K.M., Abdel-Mohsen H.H., El-bermawy N.M. (2020). Sodium propionate as a dietary acidifier for European seabass (Dicentrarchus labrax) fry: immune competence, gut microbiome, and intestinal histology benefits. Aquacult. Int., 28: 95–111.
Search in Google Scholar Back to article
Wassef E.A., Saleh N.E., Ashry A.M. (2021). Taurine or sodium difor-mate supplementation to a low fishmeal plant-based diet enhanced immunity and muscle cellularity of European sea-bass (Dicentrarchus labrax). Aquacult. Res., 54: 1513–1524.
Search in Google Scholar Back to article
Wassef E.A., Saleh N.E., Abdel-Latif H.M. (2023). Beneficial effects of some selected feed additives for European seabass (Dicentrarchus labrax L.): a review. Int. Aquat. Res., 15: 271–288.
Search in Google Scholar Back to article
Wongsasak U., Chaijamrus S., Kumkhong S., Boonanuntanasarn S. (2015). Effects of dietary supplementation with β-glucan and synbiotics on immune gene expression and immune parameters under ammonia stress in Pacific white shrimp. Aquaculture, 436: 179–187.
Search in Google Scholar Back to article
Wu P., Tian L. I., Zhou X.Q., Jiang W.D., Liu Y., Jiang J., Xie F., Kuang S.Y., Tang L., Tang W.N. (2018). Sodium butyrate enhanced physical barrier function referring to Nrf2, JNK and MLCK signaling pathways in the intestine of young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol., 73: 121–132.
Search in Google Scholar Back to article
Wu S., Wang G., Angert E.R., Wang W., Li W., Zou H. (2012). Composition, diversity, and origin of the bacterial community in grass carp intestine. PloS One, 7: e30440.
Search in Google Scholar Back to article
Yang J., Martínez I., Walter J., Keshavarzian A., Rose D.J. (2013). In vitro characterization of the impact of selected dietary fibers on fecal microbiota composition and short chain fatty acid production. Anaerobe, 23: 74–81.
Search in Google Scholar Back to article
Yao W., Gong Y., Li L., Hu X., You L. (2022). The effects of dietary fibers from rice bran and wheat bran on gut microbiota: An overview. Food Chem. X, 13: 100252.
Search in Google Scholar Back to article
Ye L., Amberg J., Chapman D., Gaikowski M., Liu W.T. (2014). Fish gut microbiota analysis differentiates physiology and behavior of invasive Asian carp and indigenous American fish. Int. Soc. Microb. Ecol. J., 8: 541–551.
Search in Google Scholar Back to article
Yukgehnaish K., Kumar P., Sivachandran P., Marimuthu K., Arshad A., Paray B.A., Arockiaraj J. (2020). Gut microbiota metagenomics in aquaculture: Factors influencing gut microbiome and its physiological role in fish. Rev. Aquacult., 12: 1903–1927.
Search in Google Scholar Back to article
Zhang C., Derrien M., Levenez F., Brazeilles R., Ballal S.A., Kim J., Degivry M.C., Quéré G., Garault P., van Hylckama Vlieg J.E. (2016). Ecological robustness of the gut microbiota in response to ingestion of transient food-borne microbes. Int. Soc. Microb. Ecol. J., 10: 2235–2245.
Search in Google Scholar Back to article
Zhou Z., Liu Y., He S., Shi P., Gao X., Yao B., Ringø E. (2009). Effects of dietary potassium diformate (KDF) on growth performance, feed conversion and intestinal bacterial community of hybrid tilapia (Oreochromis niloticus♀ × O. aureus♂). Aquaculture, 291: 89–94.
Search in Google Scholar Back to article
Zhu Y., Qiu X., Ding Q., Duan M., Wang C. (2014). Combined effects of dietary phytase and organic acid on growth and phosphorus utilization of juvenile yellow catfish Pelteobagrus fulvidraco. Aquaculture, 430: 1–8.
Search in Google Scholar Back to article

Probing into the Impacts of Endogenous and Exogenous Short-Chain Fatty Acids (SCFAS) in Fish Health and Growth – A Review

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