1932

Abstract

Aquaculture is the fastest-growing sector in food production worldwide. For decades, research on animal physiology, nutrition, and behavior established the foundations of best practices in land-based fish rearing and disease control. Current DNA sequencing, bioinformatics, and data science technologies now allow deep investigations of host-associated microbiomes in a tractable fashion. Adequate use of these technologies can illuminate microbiome dynamics and aid the engineering of microbiome-based solutions to disease prevention in an unprecedented manner. This review examines molecular studies of bacterial diversity, function, and host immunitymodulation at early stages of fish development, where microbial infections cause important economic losses. We uncover host colonization and virulence factors within a synthetic assemblage of fish pathogens using high-end comparative genomics and address the use of probiotics and paraprobiotics as applicable disease-prevention strategies in fish larval and juvenile rearing. We finally propose guidelines for future microbiome research of presumed relevance to fish larviculture.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-062920-113114
2021-02-15
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/animal/9/1/annurev-animal-062920-113114.html?itemId=/content/journals/10.1146/annurev-animal-062920-113114&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T et al. 2013. Animals in a bacterial world, a new imperative for the life sciences. PNAS 110:3229–36
    [Google Scholar]
  2. 2. 
    Ley RE. 2010. Obesity and the human microbiome. Curr. Opin. Gastroenterol. 26:5–11
    [Google Scholar]
  3. 3. 
    Evrensel A, Ceylan ME. 2015. The gut-brain axis: the missing link in depression. Clin. Psychopharmacol. Neurosci. 13:239–44
    [Google Scholar]
  4. 4. 
    Grice EA. 2014. The skin microbiome: potential for novel diagnostic and therapeutic approaches to cutaneous disease. Semin. Cutan. Med. Surg. 33:98–103
    [Google Scholar]
  5. 5. 
    Peixoto RS, Rosado PM, Leite DCA, Rosado AS, Bourne DG 2017. Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front. Microbiol. 8:341
    [Google Scholar]
  6. 6. 
    van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG et al. 2013. Duodenal infusion of donor feces for recurrent Clostridium difficile. N. Engl. J. Med 368:407–15
    [Google Scholar]
  7. 7. 
    Gopal M, Gupta A, Thomas G 2013. Bespoke microbiome therapy to manage plant diseases. Front. Microbiol. 4:355
    [Google Scholar]
  8. 8. 
    Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M et al. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–100
    [Google Scholar]
  9. 9. 
    Rosado PM, Leite DCA, Duarte GA, Chaloub RM, Jospin G et al. 2019. Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation. ISME J 13:921–36
    [Google Scholar]
  10. 10. 
    Gomes NC, Flocco CG, Costa R, Junca H, Vilchez R et al. 2010. Mangrove microniches determine the structural and functional diversity of enriched petroleum hydrocarbon-degrading consortia. FEMS Microbiol. Ecol. 74:276–90
    [Google Scholar]
  11. 11. 
    Oliveira V, Gomes NCM, Almeida A, Silva AMS, Simões MMQ et al. 2014. Hydrocarbon contamination and plant species determine the phylogenetic and functional diversity of endophytic degrading bacteria. Mol. Ecol. 23:1392–404
    [Google Scholar]
  12. 12. 
    Food Agric. Organ. 2014. The State of World Fisheries and Aquaculture: Opportunities and Challenges Rome: Food Agric. Organ.
  13. 13. 
    Skjermo J, Bergh Ø 2004. High-M alginate immunostimulation of Atlantic halibut (Hippoglossus hippoglossus L.) larvae using Artemia for delivery, increases resistance against vibriosis. Aquaculture 238:107–13
    [Google Scholar]
  14. 14. 
    Makridis P, Fjellheim AJ, Skjermo J, Vadstein O 2000. Control of the bacterial flora of Brachionus plicatilis and Artemia franciscana by incubation in bacterial suspensions. Aquaculture 185:207–18
    [Google Scholar]
  15. 15. 
    Vivekanandhan G, Savithamani K, Hatha AAM, Lakshmanaperumalsamy P 2002. Antibiotic resistance of Aeromonas hydrophila isolated from marketed fish and prawn of South India. Int. J. Food Microbiol. 76:165–68
    [Google Scholar]
  16. 16. 
    De Schryver P, Vadstein O 2014. Ecological theory as a foundation to control pathogenic invasion in aquaculture. ISME J 8:2360–68
    [Google Scholar]
  17. 17. 
    Verschuere L, Rombaut G, Sorgeloos P, Verstraete W 2000. Probiotic bacteria as biological control agents in aquaculture. Microbiol. Mol. Biol. Rev. 64:655–71
    [Google Scholar]
  18. 18. 
    Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA et al. 2017. Expert consensus document: the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat. Rev. Gastroenterol. Hepatol. 14:491–502
    [Google Scholar]
  19. 19. 
    Heppell J, Davis HL. 2000. Application of DNA vaccine technology to aquaculture. Adv. Drug Deliv. Rev. 43:29–43
    [Google Scholar]
  20. 20. 
    Embregts CWE, Forlenza M. 2016. Oral vaccination of fish: lessons from humans and veterinary species. Dev. Comp. Immunol. 64:118–37
    [Google Scholar]
  21. 21. 
    Soliman WS, Shaapan RM, Mohamed LA, Gayed SSR 2019. Recent biocontrol measures for fish bacterial diseases, in particular to probiotics, bio-encapsulated vaccines, and phage therapy. Open Vet. J. 9:190–95
    [Google Scholar]
  22. 22. 
    Reitan KI, Rainuzzo JR, Øie G, Olsen Y 1997. A review of the nutritional effects of algae in marine fish larvae. Aquaculture 155:207–21
    [Google Scholar]
  23. 23. 
    Sheth RU, Cabral V, Chen SP, Wang HH 2016. Manipulating bacterial communities by in situ microbiome engineering. Trends Genet 32:189–200
    [Google Scholar]
  24. 24. 
    Gratacap RL, Wargelius A, Edvardsen RB, Houston RD 2019. Potential of genome editing to improve aquaculture breeding and production. Trends Genet 35:672–84
    [Google Scholar]
  25. 25. 
    Vine NG, Leukes WD, Kaiser H 2006. Probiotics in marine larviculture. FEMS Microbiol. Rev. 30:404–27
    [Google Scholar]
  26. 26. 
    Hoseinifar SH, Sun Y-Z, Wang A, Zhou Z 2018. Probiotics as means of diseases control in aquaculture, a review of current knowledge and future perspectives. Front. Microbiol. 9:2429
    [Google Scholar]
  27. 27. 
    Duarte LN, Coelho FJRC, Cleary DFR, Bonifácio D, Martins P, Gomes NCM 2019. Bacterial and microeukaryotic plankton communities in a semi-intensive aquaculture system of sea bass (Dicentrarchus labrax): a seasonal survey. Aquaculture 503:59–69
    [Google Scholar]
  28. 28. 
    Choudhury TG, Kamilya D. 2019. Paraprobiotics: an aquaculture perspective. Rev. Aquacult. 11:1258–70
    [Google Scholar]
  29. 29. 
    Song SK, Beck BR, Kim D, Park J, Kim J et al. 2014. Prebiotics as immunostimulants in aquaculture: a review. Fish Shellfish Immunol 40:40–48
    [Google Scholar]
  30. 30. 
    Vonaesch P, Anderson M, Sansonetti PJ 2018. Pathogens, microbiome and the host: emergence of the ecological Koch's postulates. FEMS Microbiol. Rev. 42:273–92
    [Google Scholar]
  31. 31. 
    Wilkins LJ, Monga M, Miller AW 2019. Defining dysbiosis for a cluster of chronic diseases. Sci. Rep. 9:12918
    [Google Scholar]
  32. 32. 
    Bass D, Stentiford GD, Wang H-C, Koskella B, Tyler CR 2019. The pathobiome in animal and plant diseases. Trends Ecol. Evol. 34:996–1008
    [Google Scholar]
  33. 33. 
    Merrifield DL, Rodiles A. 2015. The fish microbiome and its interactions with mucosal tissues. Mucosal Health in Aquaculture BH Beck, E Peatman 273–95 San Diego, CA: Academic
    [Google Scholar]
  34. 34. 
    de Bruijn I, Liu Y, Wiegertjes GF, Raaijmakers JM 2018. Exploring fish microbial communities to mitigate emerging diseases in aquaculture. FEMS Microbiol. Ecol. 94:fix161
    [Google Scholar]
  35. 35. 
    Tarnecki AM, Burgos FA, Ray CL, Arias CR 2017. Fish intestinal microbiome: diversity and symbiosis unravelled by metagenomics. J. Appl. Microbiol. 123:2–17
    [Google Scholar]
  36. 36. 
    Vadstein O, Bergh Ø, Gatesoupe F-J, Galindo-Villegas J, Mulero V et al. 2013. Microbiology and immunology of fish larvae. Rev. Aquacult. 5:S1–S25
    [Google Scholar]
  37. 37. 
    Nikouli E, Meziti A, Antonopoulou E, Mente E, Kormas KA 2019. Host-associated bacterial succession during the early embryonic stages and first feeding in farmed gilthead sea bream (Sparus aurata). Genes 10:7483
    [Google Scholar]
  38. 38. 
    Califano G, Castanho S, Soares F, Ribeiro L, Cox CJ et al. 2017. Molecular taxonomic profiling of bacterial communities in a gilthead seabream (Sparus aurata) hatchery. Front. Microbiol. 8:204
    [Google Scholar]
  39. 39. 
    Le D, Nguyen P, Nguyen D, Dierckens K, Boon N et al. 2020. Gut microbiota of migrating wild rabbit fish (Siganus guttatus) larvae have low spatial and temporal variability. Microb. Ecol. 79:539–51
    [Google Scholar]
  40. 40. 
    Wilkes Walburn J, Wemheuer B, Thomas T, Copeland E, O'Connor W et al. 2019. Diet and diet-associated bacteria shape early microbiome development in yellowtail kingfish (Seriola lalandi). Microb. Biotechnol. 12:275–88
    [Google Scholar]
  41. 41. 
    Ingerslev HC, von Gersdorff Jørgensen L, Lenz Strube M, Larsen N, Dalsgaard I et al. 2014. The development of the gut microbiota in rainbow trout (Oncorhynchus mykiss) is affected by first feeding and diet type. Aquaculture 424–25:24–34
    [Google Scholar]
  42. 42. 
    Giatsis C, Sipkema D, Smidt H, Heilig H, Benvenuti G et al. 2015. The impact of rearing environment on the development of gut microbiota in tilapia larvae. Sci. Rep. 5:18206
    [Google Scholar]
  43. 43. 
    Bakke I, Coward E, Andersen T, Vadstein O 2015. Selection in the host structures the microbiota associated with developing cod larvae (Gadus morhua). Environ. Microbiol. 17:3914–24
    [Google Scholar]
  44. 44. 
    Bledsoe JW, Peterson BC, Swanson KS, Small BC 2016. Ontogenetic characterization of the intestinal microbiota of channel catfish through 16S rRNA gene sequencing reveals insights on temporal shifts and the influence of environmental microbes. PLOS ONE 11:e0166379
    [Google Scholar]
  45. 45. 
    Lokesh J, Kiron V, Sipkema D, Fernandes JMO, Moum T 2019. Succession of embryonic and the intestinal bacterial communities of Atlantic salmon (Salmo salar) reveals stage-specific microbial signatures. Microbiol. Open 8:e00672
    [Google Scholar]
  46. 46. 
    Kjørsvik E, van der Meeren T, Kryvi H, Arnfinnson J, Kvenseth PG 1991. Early development of the digestive tract of cod larvae, Gadus morhua L., during start-feeding and starvation. J. Fish Biol. 38:1–15
    [Google Scholar]
  47. 47. 
    Vadstein O, Attramadal KJK, Bakke I, Forberg T, Olsen Y et al. 2018. Managing the microbial community of marine fish larvae: a holistic perspective for larviculture. Front. Microbiol. 9:1820
    [Google Scholar]
  48. 48. 
    Li X, Zhou L, Yu Y, Ni J, Xu W, Yan Q 2017. Composition of gut microbiota in the gibel carp (Carassius auratus gibelio) varies with host development. Microb. Ecol. 74:239–49
    [Google Scholar]
  49. 49. 
    Duarte LN, Coelho FJRC, Oliveira V, Cleary DFR, Martins P, Gomes NCM 2019. Characterization of bacterioplankton communities from a hatchery recirculating aquaculture system (RAS) for juvenile sole (Solea senegalensis) production. PLOS ONE 14:e0211209
    [Google Scholar]
  50. 50. 
    Li X, Yu Y, Feng W, Yan Q, Gong Y 2012. Host species as a strong determinant of the intestinal microbiota of fish larvae. J. Microbiol. 50:29–37
    [Google Scholar]
  51. 51. 
    Hansen GH, Olafsen JA. 1989. Bacterial colonization of cod (Gadus morhua L.) and halibut (Hippoglossus hippoglossus) eggs in marine aquaculture. Appl. Environ. Microbiol. 55:1435–46
    [Google Scholar]
  52. 52. 
    Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI 2007. The human microbiome project. Nature 449:804–10
    [Google Scholar]
  53. 53. 
    Flint HJ, Scott KP, Louis P, Duncan SH 2012. The role of the gut microbiota in nutrition and health. Nat. Rev. Gastroenterol. Hepatol. 9:577–89
    [Google Scholar]
  54. 54. 
    Vestrum RI, Attramadal KJK, Winge P, Li K, Olsen Y et al. 2018. Rearing water treatment induces microbial selection influencing the microbiota and pathogen associated transcripts of cod (Gadus morhua) larvae. Front. Microbiol. 9:851
    [Google Scholar]
  55. 55. 
    Xiao Joe JT, Chiou PP, Kuo CY, Jia Lin JH, Wu JL, Lu MW 2019. The microbiota profile and transcriptome analysis of immune response during metamorphosis stages in orange spotted grouper (Epinephelus coioides). Fish Shellfish Immunol 90:141–49
    [Google Scholar]
  56. 56. 
    Wei J, Guo X, Liu H, Chen Y, Wang W 2018. The variation profile of intestinal microbiota in blunt snout bream (Megalobrama amblycephala) during feeding habit transition. BMC Microbiol 18:99
    [Google Scholar]
  57. 57. 
    Lescak EA, Milligan-Myhre KC. 2017. Teleosts as model organisms to understand host-microbe interactions. J. Bacteriol. 199:e00868–16
    [Google Scholar]
  58. 58. 
    Rawls JF, Samuel BS, Gordon JI 2004. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. PNAS 101:4596–601
    [Google Scholar]
  59. 59. 
    Bates JM, Mittge E, Kuhlman J, Baden KN, Cheesman SE, Guillemin K 2006. Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev. Biol. 297:374–86
    [Google Scholar]
  60. 60. 
    Bates JM, Akerlund J, Mittge E, Guillemin K 2007. Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe 2:371–82
    [Google Scholar]
  61. 61. 
    Cheesman SE, Neal JT, Mittge E, Seredick BM, Guillemin K 2011. Epithelial cell proliferation in the developing zebrafish intestine is regulated by the Wnt pathway and microbial signaling via Myd88. PNAS 108:Suppl. 14570–77
    [Google Scholar]
  62. 62. 
    Faro A, Boj SF, Clevers H 2009. Fishing for intestinal cancer models: unraveling gastrointestinal homeostasis and tumorigenesis in zebrafish. Zebrafish 6:361–76
    [Google Scholar]
  63. 63. 
    Crosnier C, Vargesson N, Gschmeissner S, Ariza-McNaughton L, Morrison A, Lewis J 2005. Delta-Notch signalling controls commitment to a secretory fate in the zebrafish intestine. Development 132:1093–104
    [Google Scholar]
  64. 64. 
    Troll JV, Hamilton MK, Abel ML, Ganz J, Bates JM et al. 2018. Microbiota promote secretory cell determination in the intestinal epithelium by modulating host Notch signaling. Development 145:dev155317
    [Google Scholar]
  65. 65. 
    Ray AK, Ghosh K, Ringø E 2012. Enzyme-producing bacteria isolated from fish gut: a review. Aquacult. Nutr. 18:465–92
    [Google Scholar]
  66. 66. 
    Semova I, Carten JD, Stombaugh J, Mackey LC, Knight R et al. 2012. Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish. Cell Host Microbe 12:277–88
    [Google Scholar]
  67. 67. 
    Rolig AS, Sweeney EG, Kaye LE, DeSantis MD, Perkins A et al. 2018. A bacterial immunomodulatory protein with lipocalin-like domains facilitates host-bacteria mutualism in larval zebrafish. eLife 7:e37172
    [Google Scholar]
  68. 68. 
    Galindo-Villegas J, García-Moreno D, de Oliveira S, Meseguer J, Mulero V 2012. Regulation of immunity and disease resistance by commensal microbes and chromatin modifications during zebrafish development. PNAS 109:E2605–14
    [Google Scholar]
  69. 69. 
    Liu T, Zhang L, Joo D, Sun S-C 2017. NF-κB signaling in inflammation. Signal Transduct. Targeted Ther. 2:17023
    [Google Scholar]
  70. 70. 
    Kanther M, Sun X, Mühlbauer M, Mackey LC, Flynn EJ3rd et al. 2011. Microbial colonization induces dynamic temporal and spatial patterns of NF-κB activation in the zebrafish digestive tract. Gastroenterology 141:197–207
    [Google Scholar]
  71. 71. 
    Murdoch CC, Espenschied ST, Matty MA, Mueller O, Tobin DM, Rawls JF 2019. Intestinal serum amyloid A suppresses systemic neutrophil activation and bactericidal activity in response to microbiota colonization. PLOS Pathogens 15:e1007381
    [Google Scholar]
  72. 72. 
    Oidtmann B, Peeler E, Lyngstad T, Brun E, Bang Jensen B, Stärk KDC 2013. Risk-based methods for fish and terrestrial animal disease surveillance. Prev. Vet. Med. 112:13–26
    [Google Scholar]
  73. 73. 
    Karimi E, Slaby BM, Soares AR, Blom J, Hentschel U, Costa R 2018. Metagenomic binning reveals versatile nutrient cycling and distinct adaptive features in alphaproteobacterial symbionts of marine sponges. FEMS Microbiol. Ecol. 94:fiy074
    [Google Scholar]
  74. 74. 
    Stentiford GD, Sritunyalucksana K, Flegel TW, Williams BAP, Withyachumnarnkul B et al. 2017. New paradigms to help solve the global aquaculture disease crisis. PLOS Pathogens 13:e1006160
    [Google Scholar]
  75. 75. 
    Chen IA, Chu K, Palaniappan K, Pillay M, Ratner A et al. 2019. IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes. Nucleic Acids Res 8:D666–D77
    [Google Scholar]
  76. 76. 
    Silva SG, Keller-Costa T, Bloom J, Costa R 2019. Comparative genomics reveals complex natural product biosynthesis potential and carbon metabolism across host-associated and free-living Aquimarina (Bacteroidetes) species. Environ. Microbiol. 21:4002–19
    [Google Scholar]
  77. 77. 
    Blin K, Shaw S, Steinke K, Villebro R, Ziemert N et al. 2019. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 47:W81–W87
    [Google Scholar]
  78. 78. 
    Reglinski M, Sriskandan S. 2015. Staphylococcus aureus. Molecular Medical Microbiology Y-W Tang, M Sussman, D Liu, I Poxton, J Schwartzman 675–716 Boston: Academic. , 2nd. ed.
    [Google Scholar]
  79. 79. 
    Anthoni U, Christophersen C, Nielsen PH, Gram L, Petersen BO 1995. Pseudomonine, an isoxazolidone with siderophoric activity from Pseudomonas fluorescens AH2 isolated from Lake Victorian Nile perch. J. Nat. Products 58:1786–89
    [Google Scholar]
  80. 80. 
    Barghouthi S, Young R, Olson MO, Arceneaux JE, Clem LW, Byers BR 1989. Amonabactin, a novel tryptophan- or phenylalanine-containing phenolate siderophore in Aeromonas hydrophila. J. Bacteriol 171:1811–16
    [Google Scholar]
  81. 81. 
    Soengas RG, Anta C, Espada A, Paz V, Ares IR et al. 2006. Structural characterization of vanchrobactin, a new catechol siderophore produced by the fish pathogen Vibrio anguillarum serotype O2. Tetrahedron Lett 47:7113–16
    [Google Scholar]
  82. 82. 
    Moran MA, Belas R, Schell MA, González JM, Sun F et al. 2007. Ecological genomics of marine roseobacters. Appl. Environ. Microbiol. 73:4559–69
    [Google Scholar]
  83. 83. 
    Bentzon-Tilia M, Sonnenschein EC, Gram L 2016. Monitoring and managing microbes in aquaculture—towards a sustainable industry. Microb. Biotechnol. 9:576–84
    [Google Scholar]
  84. 84. 
    Martins P, Coelho FJRC, Cleary DFR, Pires ACC, Marques B et al. 2018. Seasonal patterns of bacterioplankton composition in a semi-intensive European seabass (Dicentrarchus labrax) aquaculture system. Aquaculture 490:240–50
    [Google Scholar]
  85. 85. 
    Seyedsayamdost MR, Case RJ, Kolter R, Clardy J 2011. The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat. Chem 3:331–35
    [Google Scholar]
  86. 86. 
    Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT et al. 2015. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522:98–101
    [Google Scholar]
  87. 87. 
    D'Alvise PW, Melchiorsen J, Porsby CH, Nielsen KF, Gram L 2010. Inactivation of Vibrio anguillarum by attached and planktonic Roseobacter cells. Appl. Environ. Microbiol. 76:2366–70
    [Google Scholar]
  88. 88. 
    D'Alvise PW, Lillebø S, Prol-Garcia MJ, Wergeland HI, Nielsen KF et al. 2012. Phaeobacter gallaeciensis reduces Vibrio anguillarum in cultures of microalgae and rotifers, and prevents vibriosis in cod larvae. PLOS ONE 7:e43996
    [Google Scholar]
  89. 89. 
    Martins P, Cleary DFR, Pires ACC, Rodrigues AM, Quintino V et al. 2013. Molecular analysis of bacterial communities and detection of potential pathogens in a recirculating aquaculture system for Scophthalmus maximus and Solea senegalensis. PLOS ONE 8:e80847
    [Google Scholar]
  90. 90. 
    Carrión VJ, Perez-Jaramillo J, Cordovez V, Tracanna V, de Hollander M et al. 2019. Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science 366:606–12
    [Google Scholar]
  91. 91. 
    Hai NV. 2015. The use of probiotics in aquaculture. J. Appl. Microbiol. 119:917–35
    [Google Scholar]
  92. 92. 
    Tarkhani R, Imani A, Hoseinifar SH, Ashayerizadeh O, Sarvi Moghanlou K et al. 2020. 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 Shellfish Immunol 98:661–69
    [Google Scholar]
  93. 93. 
    Han B, Long W-Q, He J-Y, Liu Y-J, Si Y-Q, Tian L-X 2015. Effects of dietary Bacillus licheniformis on growth performance, immunological parameters, intestinal morphology and resistance of juvenile Nile tilapia (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol 46:225–31
    [Google Scholar]
  94. 94. 
    Hamdan AM, El-Sayed AF, Mahmoud MM 2016. Effects of a novel marine probiotic, Lactobacillus plantarum AH 78, on growth performance and immune response of Nile tilapia (Oreochromis niloticus). J. Appl. Microbiol. 120:1061–73
    [Google Scholar]
  95. 95. 
    Pourgholam MA, Khara H, Safari R, Sadati MAY, Aramli MS 2016. Dietary administration of Lactobacillus plantarum enhanced growth performance and innate immune response of Siberian sturgeon. Acipenser baerii. Probiotics Antimicrob. Proteins 8:1–7
    [Google Scholar]
  96. 96. 
    Yu Y, Wang C, Wang A, Yang W, Lv F et al. 2018. Effects of various feeding patterns of Bacillus coagulans on growth performance, antioxidant response and Nrf2-Keap1 signaling pathway in juvenile gibel carp (Carassius auratus gibelio). Fish Shellfish Immunol 73:75–83
    [Google Scholar]
  97. 97. 
    Makled SO, Hamdan AM, El-Sayed AM 2020. Growth promotion and immune stimulation in Nile tilapia, Oreochromis niloticus, fingerlings following dietary administration of a novel marine probiotic, Psychrobacter maritimus S. Probiotics Antimicrob. Proteins 12:365–74
    [Google Scholar]
  98. 98. 
    Amir I, Zuberi A, Kamran M, Imran M, MuH Murtaza 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 Shellfish Immunol 95:464–72
    [Google Scholar]
  99. 99. 
    Bunnoy A, Na-Nakorn U, Srisapoome P 2019. Probiotic effects of a novel strain, Acinetobacter KU011TH, on the growth performance, immune responses, and resistance against Aeromonas hydrophila of bighead catfish (Clarias macrocephalus Günther, 1864). Microorganisms 7:613
    [Google Scholar]
  100. 100. 
    Mohammadian T, Nasirpour M, Tabandeh MR, Heidary AA, Ghanei-Motlagh R, Hosseini SS 2019. Administrations of autochthonous probiotics altered juvenile rainbow trout Oncorhynchus mykiss health status, growth performance and resistance to Lactococcus garvieae, an experimental infection. Fish Shellfish Immunol 86:269–79
    [Google Scholar]
  101. 101. 
    Hoseinifar SH, Dadar M, Ringø E 2017. Modulation of nutrient digestibility and digestive enzyme activities in aquatic animals: the functional feed additives scenario. Aquacult. Res. 48:3987–4000
    [Google Scholar]
  102. 102. 
    Ringø E, Hoseinifar SH, Ghosh K, Doan HV, Beck BR, Song SK 2018. Lactic acid bacteria in finfish—an update. Front. Microbiol. 9:1818
    [Google Scholar]
  103. 103. 
    Xia Y, Lu M, Chen G, Cao J, Gao F et al. 2018. Effects of dietary Lactobacillus rhamnosus JCM1136 and Lactococcus lactis subsp. lactis JCM5805 on the growth, intestinal microbiota, morphology, immune response and disease resistance of juvenile Nile tilapia, Oreochromis niloticus. Fish Shellfish Immunol. 76:368–79
    [Google Scholar]
  104. 104. 
    Xia Y, Cao J, Wang M, Lu M, Chen G et al. 2019. Effects of Lactococcus lactis subsp. lactis JCM5805 on colonization dynamics of gut microbiota and regulation of immunity in early ontogenetic stages of tilapia. Fish Shellfish Immunol 86:53–63
    [Google Scholar]
  105. 105. 
    Xia Y, Wang M, Gao F, Lu M, Chen G 2020. Effects of dietary probiotic supplementation on the growth, gut health and disease resistance of juvenile Nile tilapia (Oreochromis niloticus). Anim. Nutr. 6:69–79
    [Google Scholar]
  106. 106. 
    Guo G, Li C, Xia B, Jiang S, Zhou S et al. 2020. The efficacy of lactic acid bacteria usage in turbot Scophthalmus maximus on intestinal microbiota and expression of the immune related genes. Fish Shellfish Immunol 100:90–97
    [Google Scholar]
  107. 107. 
    Dittmann KK, Rasmussen BB, Melchiorsen J, Sonnenschein EC, Gram L, Bentzon-Tilia M 2020. Changes in the microbiome of mariculture feed organisms after treatment with a potentially probiotic strain of Phaeobacter inhibens. Appl. Environ. Microbiol 86:e00499–20
    [Google Scholar]
  108. 108. 
    Niu KM, Khosravi S, Kothari D, Lee WD, Lim JM et al. 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 Shellfish Immunol 93:258–68
    [Google Scholar]
  109. 109. 
    Li Z, Bao N, Ren T, Han Y, Jiang Z et al. 2019. The effect of a multi-strain probiotic on growth performance, non-specific immune response, and intestinal health of juvenile turbot, Scophthalmus maximus L. Fish Physiol. Biochem. 45:1393–407
    [Google Scholar]
  110. 110. 
    Adorian TJ, Jamali H, Farsani HG, Darvishi P, Hasanpour S et al. 2019. Effects of probiotic bacteria Bacillus on growth performance, digestive enzyme activity, and hematological parameters of Asian sea bass, Lates calcarifer (Bloch). Probiotics Antimicrob. Proteins 11:248–55
    [Google Scholar]
  111. 111. 
    Lin HL, Shiu YL, Chiu CS, Huang SL, Liu CH 2017. Screening probiotic candidates for a mixture of probiotics to enhance the growth performance, immunity, and disease resistance of Asian seabass, Lates calcarifer (Bloch), against Aeromonas hydrophila. Fish Shellfish Immunol 60:474–82
    [Google Scholar]
  112. 112. 
    Dawood MAO, Koshio S, Ishikawa M, Yokoyama S, El Basuini MF et al. 2016. Effects of dietary supplementation of Lactobacillus rhamnosus or/and Lactococcus lactis on the growth, gut microbiota and immune responses of red sea bream, Pagrus major. Fish Shellfish Immunol. 49:275–85
    [Google Scholar]
  113. 113. 
    Mohapatra S, Chakraborty T, Prusty AK, Das P, Paniprasad K, Mohanta KN 2012. Use of different microbial probiotics in the diet of rohu, Labeo rohita fingerlings: effects on growth, nutrient digestibility and retention, digestive enzyme activities and intestinal microflora. Aquacult. Nutr. 18:1–11
    [Google Scholar]
  114. 114. 
    Adams CA. 2010. The probiotic paradox: Live and dead cells are biological response modifiers. Nutr. Res. Rev. 23:37–46
    [Google Scholar]
  115. 115. 
    Canani RB, De Filippis F, Nocerino R, Laiola M, Paparo L et al. 2017. Specific signatures of the gut microbiota and increased levels of butyrate in children treated with fermented cow's milk containing heat-killed Lactobacillus paracasei CBA L74. Appl. Environ. Microbiol. 83:e01206–17
    [Google Scholar]
  116. 116. 
    Salinas I, Abelli L, Bertoni F, Picchietti S, Roque A et al. 2008. Monospecies and multispecies probiotic formulations produce different systemic and local immunostimulatory effects in the gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 25:114–23
    [Google Scholar]
  117. 117. 
    de Almada CN, Almada CN, Martinez RCR, Sant'Ana AS 2016. Paraprobiotics: evidences on their ability to modify biological responses, inactivation methods and perspectives on their application in foods. Trends Food Sci. Technol. 58:96–114
    [Google Scholar]
  118. 118. 
    Taverniti V, Guglielmetti S. 2011. The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of paraprobiotic concept). Genes Nutr 6:261–74
    [Google Scholar]
  119. 119. 
    Nayak SK. 2010. Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29:2–14
    [Google Scholar]
  120. 120. 
    Pan X, Wu T, Song Z, Tang H, Zhao Z 2008. Immune responses and enhanced disease resistance in Chinese drum, Miichthys miiuy (Basilewsky), after oral administration of live or dead cells of Clostridium butyrium CB2. J. Fish Dis. 31:679–86
    [Google Scholar]
  121. 121. 
    Taoka Y, Maeda H, Jo J-Y, Kim S-M, Park S-I et al. 2006. Use of live and dead probiotic cells in tilapia Oreochromis niloticus. Fish. Sci 72:755–66
    [Google Scholar]
  122. 122. 
    Gueimonde M, Kalliomäki M, Isolauri E, Salminen S 2006. Probiotic intervention in neonates—Will permanent colonization ensue. J. Pediatr. Gastroenterol. Nutr. 42:604–6
    [Google Scholar]
  123. 123. 
    Li X, Ringø E, Hoseinifar SH, Lauzon HL, Birkbeck H, Yang D 2019. The adherence and colonization of microorganisms in fish gastrointestinal tract. Rev. Aquacult. 11:603–18
    [Google Scholar]
  124. 124. 
    Thanh Tung H, Koshio S, Ferdinand Traifalgar R, Ishikawa M, Yokoyama S 2010. Effects of dietary heat-killed Lactobacillus plantarum on larval and post-larval Kuruma shrimp, Marsupenaeus japonicus Bate. J. World Aquacult. Soc. 41:16–27
    [Google Scholar]
  125. 125. 
    Dawood MAO, Koshio S, Ishikawa M, Yokoyama S 2015. Interaction effects of dietary supplementation of heat-killed Lactobacillus plantarum and β-glucan on growth performance, digestibility and immune response of juvenile red sea bream, Pagrus major. Fish Shellfish Immunol. 45:33–42
    [Google Scholar]
  126. 126. 
    Rodriguez-Estrada U, Satoh S, Haga Y, Fushimi H, Sweetman J 2013. Effects of inactivated Enterococcus faecalis and mannan oligosaccharide and their combination on growth, immunity, and disease protection in rainbow trout. N. Am. J. Aquacult. 75:416–28
    [Google Scholar]
  127. 127. 
    Cerezuela R, Cuesta A, Meseguer J, Esteban M 2012. Effects of dietary inulin and heat-inactivated Bacillus subtilis on gilthead seabream (Sparus aurata L.) innate immune parameters. Benef. Microbes 3:77–81
    [Google Scholar]
  128. 128. 
    Irianto A, Austin B. 2003. Use of dead probiotic cells to control furunculosis in rainbow trout, Oncorhynchus mykiss (Walbaum). J. Fish Dis. 26:59–62
    [Google Scholar]
  129. 129. 
    Kotani T, Kitamoto E, Kurata O, Hirayama N, Fushimi H et al. 2008. Improvement of vaccination effect on ocellate puffer and Japanese flounder by the feeding of artificial feed with heat-killed Enterococcus faecalis FK-23. Aquacult. Sci. 56:375–82
    [Google Scholar]
  130. 130. 
    Chandler CE, Ernst RK. 2017. Bacterial lipids: powerful modifiers of the innate immune response. F1000Research 6:F1000 Faculty Rev–334
    [Google Scholar]
  131. 131. 
    Zheng X, Duan Y, Dong H, Zhang J 2020. The effect of Lactobacillus plantarum administration on the intestinal microbiota of whiteleg shrimp Penaeus vannamei. Aquaculture 526:735331
    [Google Scholar]
  132. 132. 
    Hoseinifar SH, Mirvaghefi A, Merrifield DL 2011. 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). Aquaculture 318:90–94
    [Google Scholar]
  133. 133. 
    Zheng X, Duan Y, Dong H, Zhang J 2017. Effects of dietary Lactobacillus plantarum in different treatments on growth performance and immune gene expression of white shrimp Litopenaeus vannamei under normal condition and stress of acute low salinity. Fish Shellfish Immunol 62:195–201
    [Google Scholar]
  134. 134. 
    Sugawara T, Sawada D, Ishida Y, Aihara K, Aoki Y et al. 2016. Regulatory effect of paraprobiotic Lactobacillus gasseri CP2305 on gut environment and function. Microb. Ecol. Health Dis. 27:30259
    [Google Scholar]
  135. 135. 
    Rossi O, van Berkel LA, Chain F, Tanweer Khan M, Taverne N et al. 2016. Faecalibacterium prausnitzii A2–165 has a high capacity to induce IL-10 in human and murine dendritic cells and modulates T cell responses. Sci. Rep. 6:18507
    [Google Scholar]
  136. 136. 
    Perdigón G, Maldonado Galdeano C, Valdez JC, Medici M 2002. Interaction of lactic acid bacteria with the gut immune system. Eur. J. Clin. Nutr. 56:S21–S26
    [Google Scholar]
  137. 137. 
    Jurado J, Villasanta-González A, Tapia-Paniagua ST, Balebona MC, García de la Banda I et al. 2018. Dietary administration of the probiotic Shewanella putrefaciens Pdp11 promotes transcriptional changes of genes involved in growth and immunity in Solea senegalensis larvae. Fish Shellfish Immunol 77:350–63
    [Google Scholar]
  138. 138. 
    Soltani M, Abdy E, Alishahi M, Mirghaed AT, Hosseini-Shekarabi P 2017. Growth performance, immune-physiological variables and disease resistance of common carp (Cyprinus carpio) orally subjected to different concentrations of Lactobacillus plantarum. Aquacult. Int 25:1913–33
    [Google Scholar]
  139. 139. 
    Pourgholam MA, Khara H, Safari R, Sadati MA, Aramli MS 2017. Hemato-immunological responses and disease resistance in Siberian sturgeon Acipenser baerii fed on a supplemented diet of Lactobacillus plantarum. Probiotics Antimicrob. Proteins 9:32–40
    [Google Scholar]
  140. 140. 
    Safari R, Adel M, Lazado CC, Caipang CM, Dadar M 2016. Host-derived probiotics Enterococcus casseliflavus improves resistance against Streptococcus iniae infection in rainbow trout (Oncorhynchus mykiss) via immunomodulation. Fish Shellfish Immunol 52:198–205
    [Google Scholar]
  141. 141. 
    Selim KM, Reda RM. 2015. Improvement of immunity and disease resistance in the Nile tilapia, Oreochromis niloticus, by dietary supplementation with Bacillus amyloliquefaciens. Fish Shellfish Immunol 44:496–503
    [Google Scholar]
  142. 142. 
    Reda RM, Selim KM. 2015. Evaluation of Bacillus amyloliquefaciens on the growth performance, intestinal morphology, hematology and body composition of Nile tilapia. Oreochromis niloticus. Aquacult. Int. 23:203–17
    [Google Scholar]
  143. 143. 
    Peixoto MJ, Domingues A, Batista S, Gonçalves JFM, Gomes AM et al. 2018. Physiopathological responses of sole (Solea senegalensis) subjected to bacterial infection and handling stress after probiotic treatment with autochthonous bacteria. Fish Shellfish Immunol 83:348–58
    [Google Scholar]
  144. 144. 
    Park Y, Lee S, Hong J, Kim D, Moniruzzaman M, Bai SC 2017. Use of probiotics to enhance growth, stimulate immunity and confer disease resistance to Aeromonas salmonicida in rainbow trout (Oncorhynchus mykiss). Aquacult. Res. 48:2672–82
    [Google Scholar]
  145. 145. 
    Allameh SK, Yusoff FM, Ringø E, Daud HM, Saad CR, Ideris A 2016. Effects of dietary mono- and multiprobiotic strains on growth performance, gut bacteria and body composition of Javanese carp (Puntius gonionotus, Bleeker 1850). Aquacult. Nutr. 22:367–73
    [Google Scholar]
  146. 146. 
    Hamza A, Fdhila K, Zouiten D, Masmoudi AS 2016. Virgibacillus proomii and Bacillus mojavensis as probiotics in sea bass (Dicentrarchus labrax) larvae: effects on growth performance and digestive enzyme activities. Fish Physiol. Biochem. 42:495–507
    [Google Scholar]
  147. 147. 
    Park Y, Moniruzzaman M, Lee S, Hong J, Won S et al. 2016. Comparison of the effects of dietary single and multi-probiotics on growth, non-specific immune responses and disease resistance in starry flounder. Platichthys stellatus. Fish Shellfish Immunol. 59:351–57
    [Google Scholar]
  148. 148. 
    Beck BR, Kim D, Jeon J, Lee SM, Kim HK et al. 2015. The effects of combined dietary probiotics Lactococcus lactis BFE920 and Lactobacillus plantarum FGL0001 on innate immunity and disease resistance in olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol 42:177–83
    [Google Scholar]
  149. 149. 
    Aly SM, Abdel-Galil Ahmed Y, Abdel-Aziz Ghareeb A, Mohamed MF 2008. Studies on Bacillus subtilis and Lactobacillus acidophilus, as potential probiotics, on the immune response and resistance of Tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol 25:128–36
    [Google Scholar]
/content/journals/10.1146/annurev-animal-062920-113114
Loading
/content/journals/10.1146/annurev-animal-062920-113114
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error