Cited by 1,073Aquaculture disease management and microbiotaAquaculture Nutrition and GrowthGut microbiota and health

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Role of gastrointestinal microbiota in fish

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Nayak, Sukanta K·2010·Aquaculture Research

DOI 10.1111/j.1365-2109.2010.02546.x

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Abstract

The gastrointestinal (GI) tract of an animal consists of a very complex and dynamic microbial ecosystem that is very important from a nutritional, physiological and pathological point of view. A wide range of microbes derived from the surrounding aquatic environment, soil/sediment and feed are found to colonize in the GI tract of fish. Among the microbial groups, bacteria (aerobic, facultative anaerobic and obligate aneraobic forms) are the principal colonizers in the GI tract of fish, and in some fish, yeasts are also reported. The common bacterial colonizers in the GI tract of freshwater and marine fish include Vibrio, Aeromonas, Flavobacterium, Plesiomonas, Pseudomonas, Enterobacteriaceae, Micrococcus, Acinetobacter, Clostridium, Fusarium and Bacteroides, which may vary from species to species as well as environmental conditions. Besides, several unknown bacteria belonging to Mycoplasma, Arthrobacter, Brochothrix, Jeotgailbacillus, Ochrobactrum, Psychrobacter and Sejongia species in the GI tract of different fish species have now been identified successfully using culture-independent techniques. Gnotobiotic and conventional studies indicate the involvement of GI microbiota in fish nutrition, epithelial development, immunity as well as disease outbreak. This review also highlights the need for manipulating the gut microbiota with useful beneficial microbes through probiotic, prebiotic and synbiotic concepts for better fish health management.

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“Many exogenous and endogenous factors, such as species, age and developmental stage, bacterial colonisation during the larval stage, geographic location, seasonality and other environmental factors, especially temperature, antibiotic use during fish growth, or the individual genetics of each fish can alter the gut mic…”
Background
PCR-TTGE Analysis of 16S rRNA from Rainbow Trout (Oncorhynchus mykiss) Gut Microbiota Reveals Host-Specific Communities of Active Bacteria
Navarrete, P., Magne, F., Araneda, C., FUENTES, P. M., Barros, L., Opazo, R., Espejo, R. T., & Romero, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031335 · Cited by 189
“water temperature), rearing and farming conditions [3].”
Background
Dietary soybean meal affects intestinal homoeostasis by altering the microbiota, morphology and inflammatory cytokine gene expression in northern snakehead
Miao, S., Zhao, C., Zhu, J., Hu, J., Dong, X., & Sun, L. (2018) · Scientific Reports · doi:10.1038/s41598-017-18430-7 · Cited by 187
Altered gut microbiota associated with intestinal disease in grass carp (Ctenopharyngodon idellus)
Tran, N. T., Zhang, J., Xiong, F., Wang, G., Li, W., & Wu, S. (2018) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-018-2447-2 · Cited by 182
“Gut microbial communities is known to be important in the host digestive and immune system (Ganguly and Prasad 2012; Nayak 2010).”
BackgroundInfluential
Salmon gut microbiota correlates with disease infection status: potential for monitoring health in farmed animals
Bozzi, D., Rasmussen, J. A., Carøe, C., Sveier, H., Nordøy, K., Gilbert, M. T. P., & Limborg, M. T. (2021) · Animal Microbiome · doi:10.1186/s42523-021-00096-2 · Cited by 190
Next generation sequencing for gut microbiome characterization in rainbow trout (Oncorhynchus mykiss) fed animal by-product meals as an alternative to fishmeal protein sources
Rimoldi, S., Terova, G., Ascione, C., Giannico, R., & Brambilla, F. (2018) · PLoS ONE · doi:10.1371/journal.pone.0193652 · Cited by 193
Modulation of transcriptomic profile in aquatic animals: Probiotics, prebiotics and synbiotics scenarios
Dawood, M. A. O., Abo‐Al‐Ela, H. G., & Hasan, M. T. (2019) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2019.12.054 · Cited by 190
Administration of Probiotics in the Water in Finfish Aquaculture Systems: A Review
Jahangiri, L., & Esteban, M. Á. (2018) · Fishes · doi:10.3390/fishes3030033 · Cited by 178
“) are frequently used as probiotics in fish nutrition [16].”
Background
Multifaceted applications of probiotic Bacillus species in aquaculture with special reference to Bacillus subtilis
Nayak, S. K. (2020) · Reviews in Aquaculture · doi:10.1111/raq.12503 · Cited by 193
Diversity of gut microbiomes in marine fishes is shaped by host‐related factors
Huang, Q., Sham, R. C.-T., Deng, Y., Mao, Y., Wang, C., Zhang, T., & Leung, K. (2020) · Molecular Ecology · doi:10.1111/mec.15699 · Cited by 176
“The gastrointestinal tract is one of the major routes for the entry of some pathogens that may cause serious diseases such as vibriosis, enteric septicaemia and aeromoniasis (Nayak, 2010).”
Background
Effect of dietary arginine on growth, intestinal enzyme activities and gene expression in muscle, hepatopancreas and intestine of juvenile Jian carp (Cyprinus carpiovar. Jian)
Chen, G., Feng, L., Kuang, S., Liu, Y., Jiang, J., Hu, K., Jiang, W., Li, S., Tang, L. Y., & Zhou, X. (2011) · British Journal Of Nutrition · doi:10.1017/s0007114511005459 · Cited by 173
“The intestinal microbiota contributes to host health status, and alterations in the microbial balance may produce detrimental effects in hosts((36,37)).”
Background
Combined effects of exogenous enzymes and probiotic on Nile tilapia (Oreochromis niloticus) growth, intestinal morphology and microbiome
Adeoye, A. A., Yomla, R., Jaramillo-Torres, A., Rodiles, A., Merrifield, D. L., & Davies, S. J. (2016) · Aquaculture · doi:10.1016/j.aquaculture.2016.05.028 · Cited by 175
“According to Nayak (2010), GI microbiota are involved in major nutritional functions which include digestion, nutrient utilisation and the production of specific amino acids, enzymes, short-chain fatty acids, vitamins and mineral availability.”
Bacterial symbiosis in the fish gut and its role in health and metabolism
Banerjee, G., & Ray, A. K. (2016) · Symbiosis · doi:10.1007/s13199-016-0441-8 · Cited by 181
“Dietary supplementation of useful probiotic bacteria in fish at early developmental stages can be helpful in increasing the sub-populations of specific acidophilic granulocytes (Nayak 2010).”
Background
Bacterial Signatures of “Red-Operculum” Disease in the Gut of Crucian Carp (Carassius auratus)
Li, T., Li, H., Gatesoupe, F.-J., She, R., Lin, Q., Yan, X., Li, J., & Li, X. (2017) · Microbial Ecology · doi:10.1007/s00248-017-0967-1 · Cited by 173
Dietary live yeast and increased water temperature influence the gut microbiota of rainbow trout
Huyben, D. C., Sun, L., Moccia, R. D., Kiessling, A., Dicksved, J., & Lundh, T. (2018) · Journal of Applied Microbiology · doi:10.1111/jam.13738 · Cited by 183
“…and yeast in the gut play an important role in the supply of nutrients, antagonism towards pathogens and maintenance of mucosal immunity in fish (Nayak 2010; Llewellyn et al. 2014; Wang Journal of Applied Microbiology 124, 1377--1392 © 2018 The Society for Applied Microbiology 1377 et al. 2017).”
Background
Use of chitin and krill in aquaculture - the effect on gut microbiota and the immune system: a review
Ringø, E., Zhou, Z., Olsen, R. E., & Song, S. K. (2012) · Aquaculture Nutrition · doi:10.1111/j.1365-2095.2011.00919.x · Cited by 169
Application of dietary supplements (synbiotics and probiotics in combination with plant products and β-glucans) in aquaculture
Ringø, E., & Song, S. K. (2015) · Aquaculture Nutrition · doi:10.1111/anu.12349 · Cited by 168
Isolation and characterization of native probiotics for fish farming
Wanka, K. M., Damerau, T., Costas, B., Krueger, A., Schulz, C., & Wuertz, S. (2018) · BMC Microbiology · doi:10.1186/s12866-018-1260-2 · Cited by 166
Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies
Sullam, K. E., Rubin, B. E., Dalton, C. M., Kilham, S. S., Flecker, A. S., & Russell, J. A. (2015) · The ISME Journal · doi:10.1038/ismej.2014.231 · Cited by 160
“Colonization from the The ISME Journal surrounding environment is thought to be one of the primary mechanisms of microbiota acquisition for fish (Nayak, 2010), and is found in many other animal-microbe symbioses, including the Hawaiian bobtail squid and their luminescent Vibrio fischeri symbionts.”
Background
Fish nutrition research: past, present and future
Jobling, M. (2015) · Aquaculture International · doi:10.1007/s10499-014-9875-2 · Cited by 179
“It was revealed that melamine (66.7 % N by mass) had been used to adulterate milk produced in China, resulting in renal toxicity and several deaths of young children (Moore et al. 2010, 2012; Everstine et al. 2013; Domingo et al. 2014).”
MethodInfluential
Recent studies on probiotics as beneficial mediator in aquaculture: a review
Hasan, K. N., & Banerjee, G. (2020) · The Journal of Basic and Applied Zoology · doi:10.1186/s41936-020-00190-y · Cited by 160
“It is now well established that probiotics play a vital role in maintaining the gut health by modulation of microbial community structure (Nayak, 2010).”
Background
Aquaculture industry prospective from gut microbiome of fish and shellfish: An overview
Diwan, A. D., Harke, S. N., Gopalkrishna, & Panche, A. N. (2021) · Journal of Animal Physiology and Animal Nutrition · doi:10.1111/jpn.13619 · Cited by 157
The effects of Lactobacillus acidophilus as feed supplement on skin mucosal immune parameters, intestinal microbiota, stress resistance and growth performance of black swordtail (Xiphophorus helleri)
Hoseinifar, S. H., Roosta, Z., Hajimoradloo, A., & Vakili, F. (2014) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2014.12.003 · Cited by 151
Perturbation and restoration of the fathead minnow gut microbiome after low-level triclosan exposure
Narrowe, A. B., Lantz, M. A., Smith, E. P., Bower, K. J., Roane, T. M., Vajda, A. M., & Miller, C. S. (2015) · Microbiome · doi:10.1186/s40168-015-0069-6 · Cited by 163
“triclosan-sensitive members of the fish gut microbiome [24,73].”
BackgroundInfluential
Fish disease and intestinal microbiota: A close and indivisible relationship
Medina‐Félix, D., Garibay-Valdéz, E., Vargas‐Albores, F., & Martínez‐Porchas, M. (2022) · Reviews in Aquaculture · doi:10.1111/raq.12762 · Cited by 154
Therapeutic modulation of fish gut microbiota, a feasible strategy for aquaculture?
Vargas‐Albores, F., Martínez‐Córdova, L. R., Hernández‐Mendoza, A., Cicala, F., Lago‐Lestón, A., & Martínez‐Porchas, M. (2021) · Aquaculture · doi:10.1016/j.aquaculture.2021.737050 · Cited by 148
Effects of probiotics on digestive enzymes of fish (finfish and shellfish); status and prospects: a mini review
Assan, D., Kuebutornye, F. K. A., Hlordzi, V., Chen, H., Mráz, J., Mustapha, U. F., & Abarike, E. D. (2021) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2021.110653 · Cited by 147
Fish Skin and Gut Microbiomes Show Contrasting Signatures of Host Species and Habitat
Sylvain, F., Holland, A., Bouslama, S., Audet‐Gilbert, É., Lavoie, C., Val, A. L., & Derôme, N. (2020) · Applied and Environmental Microbiology · doi:10.1128/aem.00789-20 · Cited by 147
“repertoire of host species to study the nature of vertebrate microbial communities (2)”
Background
The effects of dietary inactive brewer's yeast Saccharomyces cerevisiae var. ellipsoideus on the growth, physiological responses and gut microbiota of juvenile beluga (Huso huso)
Hoseinifar, S. H., Mirvaghefi, A., & Merrifield, D. L. (2011) · Aquaculture · doi:10.1016/j.aquaculture.2011.04.043 · Cited by 143
“Such microbial communities, particularly lactic acid bacteria (LAB), have received much attention over the last decade as we begin to understand their importance to the host with regards to digestive function, development, immunity and disease resistance (Dimitroglou et al., 2011; Merrifield et al., 2010; Nayak, 2010;…”
Background
Probiotics, Prebiotics and Synbiotics for Nile tilapia: Growth performance and protection against Aeromonas hydrophila infection
Cavalcante, R. B., Telli, G. S., Tachibana, L., Dias, D. D. C., Oshiro, E., Natori, M. M., da Silva, W. F., & Ranzani‐Paiva, M. J. T. (2020) · Aquaculture Reports · doi:10.1016/j.aqrep.2020.100343 · Cited by 143
Alterations of the gut microbiome of largemouth bronze gudgeon (Coreius guichenoti) suffering from furunculosis
Li, T., Long, M., Ji, C., Shen, Z., Gatesoupe, F.-J., Zhang, X., Zhang, Q., Zhang, L., Zhao, Y., Liu, X., et al. (2016) · Scientific Reports · doi:10.1038/srep30606 · Cited by 145
The use of probiotic bacteria against Aeromonas infections in salmonid aquaculture
Fečkaninová, A., Koščová, J., Mudroňová, D., Popelka, P., & Toropilová, J. (2016) · Aquaculture · doi:10.1016/j.aquaculture.2016.11.042 · Cited by 140
Phylogenetic and functional characterization of the distal intestinal microbiome of rainbow troutOncorhynchus mykissfrom both farm and aquarium settings
Lyons, P. P., Turnbull, J. F., Dawson, K. A., & Crumlish, M. (2016) · Journal of Applied Microbiology · doi:10.1111/jam.13347 · Cited by 138
“Some studies of the intestinal microbiota of rainbow trout have hypothesized that the composition could mirror that of the surrounding aquatic environment (Trust and Sparrow 1974; Yoshimizu and Kimura 1976; Sugita et al. 1982; Ringø and Strom 1994; Nayak 2010; Semova et al. 2012; Xing et al. 2013; Sullam et al. 2015).”
BackgroundInfluential
Composition of Gut Microbiota in the Gibel Carp (Carassius auratus gibelio) Varies with Host Development
Li, X., Zhou, L., Yu, Y., Ni, J., Xu, W., & Yan, Q. (2017) · Microbial Ecology · doi:10.1007/s00248-016-0924-4 · Cited by 139
“munity, in contrast to previous suggestions for other fish species [12, 54].”
Result
Effects of cadmium on intestinal histology and microbiota in freshwater crayfish (Procambarus clarkii)
Zhang, Y., Li, Z., Kholodkevich, S. V., Sharov, A. N., Chen, C., Feng, Y., Ren, N., & Sun, K. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.125105 · Cited by 137
Effects of dietary probiotic on the growth performance, non-specific immunity and disease resistance of cobia, Rachycentron canadum
Geng, X., Dong, X., Tan, B., Yang, Q., CHI, S.-Y., Liu, H., & Liu, X. M. (2011) · Aquaculture Nutrition · doi:10.1111/j.1365-2095.2011.00875.x · Cited by 133
Alternative dietary protein sources for Atlantic salmon ( Salmo salar L.) effect on intestinal microbiota, intestinal and liver histology and growth
Hartviksen, M. A. B., Vecino, J. L. G., Ringø, E., Bakke, A. M., Wadsworth, S., Krogdahl, Å., Ruohonen, K., & Kettunen, A. (2014) · Aquaculture Nutrition · doi:10.1111/anu.12087 · Cited by 132
Effects of dietary mixed probiotics on growth, non-specific immunity, intestinal morphology and microbiota of juvenile pacific white shrimp, Litopenaeus vannamei
Xie, J.-J., Liu, Q.-Q., Liao, S., Fang, H., Yin, P., Xie, S., Tian, L., Liu, Y., & Niu, J. (2019) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2019.04.301 · Cited by 131
Effect of fish meal substitution with fermented soy pulp on growth performance, digestive enzyme, amino acid profile, and immune-related gene expression of African catfish (Clarias gariepinus)
Kari, Z. A., Kabir, M. A., Dawood, M. A. O., Razab, M. K. A. A., Ariff, N. S. N. A., Sarkar, T., Pati, S., Edinur, H. A., Mat, K. B., Ismail, T. A., et al. (2021) · Aquaculture · doi:10.1016/j.aquaculture.2021.737418 · Cited by 131
Impact of Polypropylene Microplastics and Chemical Pollutants on European Sea Bass (Dicentrarchus labrax) Gut Microbiota and Health
Montero, D., Rimoldi, S., Torrecillas, S., Rapp, J., Moroni, F., Herrera, A., Gómez, M., Fernández-Montero, Á., & Terova, G. (2022) · Science of The Total Environment · doi:10.1016/j.scitotenv.2021.150402 · Cited by 127
Selection in the host structures the microbiota associated with developing cod larvae ( G adus morhua )
Bakke, I., Coward, E., Andersen, T., & Vadstein, Ô. (2015) · Environmental Microbiology · doi:10.1111/1462-2920.12888 · Cited by 124
Effects of low‐level dietary microalgae supplementation on the distal intestinal microbiome of farmed rainbow trout Oncorhynchus mykiss (Walbaum)
Lyons, P. P., Turnbull, J. F., Dawson, K. A., & Crumlish, M. (2016) · Aquaculture Research · doi:10.1111/are.13080 · Cited by 124
Microplastics as an aquatic pollutant affect gut microbiota within aquatic animals
Li, W., Chen, X., Li, M., Cai, Z., Gong, H., & Yan, M. (2021) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2021.127094 · Cited by 126
Molecular Analysis of Bacterial Microbiota Associated with Oysters (Crassostrea gigas and Crassostrea corteziensis) in Different Growth Phases at Two Cultivation Sites
Trabal, N., Mazón‐Suástegui, J. M., Vázquez‐Juárez, R., Ascencio‐Valle, F., Morales‐Bojórquez, E., & Romero, J. (2012) · Microbial Ecology · doi:10.1007/s00248-012-0039-5 · Cited by 122
Soybean meal-induced enteritis in Atlantic salmon ( Salmo salar) and Chinook salmon ( Oncorhynchus tshawytscha ) but not in pink salmon ( O . gorbuscha )
Booman, M., Forster, I. P., Vederas, J. C., Groman, D. B., & Jones, S. R. M. (2017) · Aquaculture · doi:10.1016/j.aquaculture.2017.10.025 · Cited by 122
Aquatic animals promote antibiotic resistance gene dissemination in water via conjugation: Role of different regions within the zebra fish intestinal tract, and impact on fish intestinal microbiota
Fu, J., Yang, D., Jin, M., Liu, W., Zhao, X. H., Li, C., Zhao, T., Wang, J., Gao, Z., Shen, Z., et al. (2017) · Molecular Ecology · doi:10.1111/mec.14255 · Cited by 118
“In addition to this, Aeromonas that has obtained plasmids might be regarded as an intestinal pathogen by intestinal immune systems and could be competitively excluded and eliminated from the intestinal mucosa by gut microbiota (Nayak, 2010).”
Background
Evaluation of paraprobiotic applicability of Lactobacillus plantarum in improving the immune response and disease protection in giant freshwater prawn, Macrobrachium rosenbergii (de Man, 1879)
Dash, G., Raman, R. P., Prasad, K. P., Makesh, M., Pradeep, M. A., & Sen, S. (2014) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2014.12.007 · Cited by 118
“Especially, probiotic bacteria belonging to the genus Lactobacillus are difficult to maintain at desired viability during storage as they do not form spores to cope with adverse conditions [4].”
Background
The Feasibility of Using Yellow Mealworms (Tenebrio molitor): Towards a Sustainable Aquafeed Industry
Shafique, L., Abdel‐Latif, H. M. R., Hassan, F., Alagawany, M. M., Naiel, M. A. E., Dawood, M. A. O., Yılmaz, S., & Liu, Q. (2021) · Animals · doi:10.3390/ani11030811 · Cited by 116
Culturable Gut Microbiota Diversity in Zebrafish
Cantas, L., Sørby, J. R. T., Aleström, P., & Sørum, H. R. (2012) · Zebrafish · doi:10.1089/zeb.2011.0712 · Cited by 115
Diet and diet‐associated bacteria shape early microbiome development in Yellowtail Kingfish ( Seriola lalandi )
Walburn, J. W., Wemheuer, B., Thomas, T., Copeland, E., O’Connor, W. A., Booth, M. A., Fielder, D. S., & Egan, S. (2018) · Microbial Biotechnology · doi:10.1111/1751-7915.13323 · Cited by 116
“Species of Streptococcus, Enterococcus and Lactobacillus, known to be components of the microbiome in healthy fish (Nayak, 2010; Sullam et al., 2012; Llewellyn et al., 2014) were identified as part of the core microbiome.”
BackgroundResultInfluential
Intestinal morphology, immunity and microbiota response to dietary fibers in largemouth bass, Micropterus salmoide
Lin, S., Zhou, X., Zhou, Y.-L., Kuang, W.-M., Chen, Y., Luo, L., & Dai, F. (2020) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2020.04.070 · Cited by 116

Authors: Nayak, S. K.
Affiliations: Nihon University (JP)
Corresponding author: Nayak, Sukanta K
ORCID: Nayak, Sukanta K
Venue: Aquaculture Research
Publisher: Hindawi Limited
Published: 2010-06-16
Volume: 41
Issue: 11
Pages: 1553-1573
ISSN: 1355-557X (ISSN-L)
DOI: 10.1111/j.1365-2109.2010.02546.x
OpenAlex: W1912394394
Cited by: 1,073
References: 240
Citations by year: 2026: 74 · 2025: 97 · 2024: 85 · 2023: 104 · 2022: 111 · 2021: 109 · 2020: 94 · 2019: 80 · 2018: 82 · 2017: 58 · 2016: 36 · 2015: 30 · 2014: 40 · 2013: 30 · 2012: 22
FWCI: 9.65
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: doi.wiley.com/10.1002/tdm_license_1.1 (tdm, 1903 d)
Locations: Aquaculture Research (publishedVersion)
Funders: Nihon University
Directorate for Biological Sciences
Topics: Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
Life Sciences › Agricultural and Biological Sciences › Aquatic Science › Aquaculture Nutrition and Growth
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Keywords: gut microbiota, fish gut bacteria, fish nutrition, fish immunity, fish disease, probiotics, prebiotics, synbiotics, gut microbiota modulation, fish health management, culture-independent identification

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