Skip to main content
SpringerLink
Log in

Fish Gut Microbiome: Current Approaches and Future Perspectives

  • Review Article
  • Published:
Indian Journal of Microbiology Aims and scope Submit manuscript

Abstract

In recent years, investigations of microbial flora associated with fish gut have deepened our knowledge of the complex interactions occurring between microbes and host fish. The gut microbiome not only reinforces the digestive and immune systems in fish but is itself shaped by several host-associated factors. Unfortunately, in the past, majority of studies have focused upon the structure of fish gut microbiome providing little knowledge of effects of these factors distinctively and the immense functional potential of the gut microbiome. In this review, we have highlighted the recently gained insights into the diversity and functions of the fish gut microbiome. We have also delved on the current approaches that are being employed to study the fish gut microbiome with an aim to collate all the knowledge gained and make accurate conclusions for their application based perspectives. The literature reviewed indicated that the future research should shift towards functional microbiomics to improve the maximum sustainable yield in aquaculture.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Hooper LV, Gordon JI (2001) Commensal host-bacterial relationships in the gut. Science 292:1115–1118. https://doi.org/10.1126/science.1058709

    Article  CAS  PubMed  Google Scholar 

  2. Nelson JS (2006) Fishes of the world, 4th edn. Wiley, Hoboken

    Google Scholar 

  3. Suyehiro Y (1942) A study on the digestive system and feeding habits of fish. Jap J Zool 10:1–303

    Google Scholar 

  4. Al-Harbi AH, Uddin MN (2004) Seasonal variation in the intestinal bacterial flora of hybrid tilapia (Oreochromis niloticus x Oreochromis aureus) cultured in earthern ponds in Saudi Arabia. Aquaculture 229:37–44. https://doi.org/10.1016/S0044-8486(03)00388-0

    Article  Google Scholar 

  5. Ringo E, Olsen RE, Mayhew TM, Myklebust R (2003) Electron microscopy of the intestinal microflora of fish. Aquaculture 227:395–415. https://doi.org/10.1016/j.aquaculture.2003.05.001

    Article  Google Scholar 

  6. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Romero J, Navarrete P (2006) 16S rDNA-based analysis of dominant bacterial populations associated with early life stages of coho salmon (Oncorhynchus kisutch). Microb Ecol 51:422–430. https://doi.org/10.1007/s00248-006-9037-9

    Article  CAS  PubMed  Google Scholar 

  8. Reveco FE, Øverland M, Romarheim OH, Mydland LT (2014) Intestinal bacterial community structure differs between healthy and inflamed intestines in Atlantic salmon (Salmo salar L.). Aquaculture 420–421:262–269. https://doi.org/10.1016/j.aquaculture.2013.11.007

    Article  CAS  Google Scholar 

  9. Navarrete P, Espejo RT, Romero J (2009) Molecular analysis of microbiota along the digestive tract of juvenile Atlantic salmon (Salmo salar L.). Microb Ecol 57:550–561. https://doi.org/10.1007/s00248-008-9448-x

    Article  CAS  PubMed  Google Scholar 

  10. Stickney RR, Shumway SE (1974) Occurrence of cellulase activity in the stomachs of fishes. J Fish Biol 6:779–790. https://doi.org/10.1111/j.1095-8649.1974.tb05120.x

    Article  CAS  Google Scholar 

  11. Sugita H, Miyajima C, Deguchi Y (1991) The vitamin B12-producing ability of the intestinal microflora of freshwater fish. Aquaculture 92:267–276. https://doi.org/10.1016/0044-8486(91)90028-6

    Article  CAS  Google Scholar 

  12. Nayak SK (2010) Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29:2–14. https://doi.org/10.1016/j.fsi.2010.02.017

    Article  CAS  PubMed  Google Scholar 

  13. Ayo-Olalusi CI, Oresegun A, Bernard E (2014) Screening of Lactic acid bacteria from the gut of Chrysichthys nigrodigitatus for use as probiotics in aquaculture production. J Fish Aquat Sci 9:478–482. https://doi.org/10.3923/jfas.2014.478.482

    Article  Google Scholar 

  14. Asaduzzaman M, Iehata S, Akter S, Kader MA, Ghosh SK, Khan MNA, Abol-Munafi AB (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. Aquac Rep 9:53–61. https://doi.org/10.1016/j.aqrep.2017.12.003

    Article  Google Scholar 

  15. Star B, Haverkamp THA, Jentoft S, Jakobsen KS (2013) Next generation sequencing shows high variation of the intestinal microbial species composition in Atlantic cod caught at a single location. BMC Microbiol 13:248. https://doi.org/10.1186/1471-2180-13-248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Xing MX, Hou ZH, Yuan JB, Liu Y, Qu Y, Liu B (2013) Taxonomic and functional metagenomic profiling of gastrointestinal tract microbiome of the farmed adult turbot (Scophthalmus maximus). FEMS Microbiol Ecol 86:432–443. https://doi.org/10.1111/1574-6941.12174

    Article  CAS  PubMed  Google Scholar 

  17. Xia JH, Lin G, Fu GH, Wan ZY, Lee M, Wang L, Liu XJ, Yue GH (2014) The intestinal microbiome of fish under starvation. BMC Genom 15:266. https://doi.org/10.1186/1471-2164-15-266

    Article  Google Scholar 

  18. Zarkasi KZ, Abell GC, Taylor RS, Neuman C, Hatje E, Tamplin ML, Katouli M, Bowman JP (2014) Pyrosequencing-based characterization of gastrointestinal bacteria of Atlantic salmon (Salmo salar L.) within a commercial mariculture system. J Appl Microbiol 117:18–27. https://doi.org/10.1111/jam.12514

    Article  CAS  PubMed  Google Scholar 

  19. 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. https://doi.org/10.1038/srep24340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Wu S, Wang G, Angert ER, Wang W, Li W, Zou H (2012) Composition, diversity, and origin of the bacterial community in grass carp intestine. PLoS One 7:e30440. https://doi.org/10.1371/journal.pone.0030440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Tarnecki AM, Burgos FA, Ray CL, Arias CR (2017) Fish intestinal microbiome: diversity and symbiosis unravelled by metagenomics. J Appl Microbiol 123:2–17. https://doi.org/10.1111/jam.13415

    Article  PubMed  Google Scholar 

  22. Nayak SK (2010) Role of gastrointestinal microbiota in fish. Aquac Res 41:1553–1573. https://doi.org/10.1111/j.1365-2109.2010.02546.x

    Article  Google Scholar 

  23. Rawls JF, Samuel BS, Gordon JI (2004) Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc Natl Acad Sci USA 101:4596–4601. https://doi.org/10.1073/pnas.0400706101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Sullam KE, Essinger SD, Lozupone CA, O’Connor MP, Rosen GL, Knight R, Kilham SS, Russell JA (2012) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol Ecol 21:3363–3378. https://doi.org/10.1111/j.1365-294X.2012.05552.x

    Article  PubMed  Google Scholar 

  25. Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM, Guillemin K, Rawls JF (2011) Evidence for a core gut microbiota in the zebrafish. ISME J 5:1595–1608. https://doi.org/10.1038/ismej.2011.38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ringo E, Sperstad S, Myklebust R, Refstie S, Krogdahl A (2006) Characterisation of the microbiota associated with intestine of Atlantic cod (Gadus morhua L.)—the effect of fish meal, standard soybean meal and a bioprocessed soybean meal. Aquaculture 261:829–841. https://doi.org/10.1016/j.aquaculture.2006.06.030

    Article  CAS  Google Scholar 

  27. Givens CE, Ransom B, Bano N, Hollibaugh JT (2014) A fish tale: comparison of the gut microbiomes of 12 finfish and 3 shark species. Mar Ecol Prog Ser 518:209–223. https://doi.org/10.3354/meps11034

    Article  Google Scholar 

  28. Desai AR, Links MG, Collins SA, Mansfield GS, Drew MD, Van Kessel AG, Hill JE (2012) Effects of plant-based diets on the distal gut microbiome of rainbow trout (Oncorhynchus mykiss). Aquaculture 350–353:134–142. https://doi.org/10.1016/j.aquaculture.2012.04.005

    Article  CAS  Google Scholar 

  29. Li X, Yan Q, Xie S, Hu W, Yu Y, Hu Z (2013) Gut microbiota contributes to the growth of fast-growing transgenic common carp (Cyprinus carpio L.). PLoS One 8:e64577. https://doi.org/10.1371/journal.pone.0064577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Carda-Diéguez M, Mira A, Fouz B (2013) Pyrosequencing survey of intestinal microbiota diversity in cultured sea bass (Dicentrarchus labrax) fed functional diets. FEMS Microbiol Ecol 87:451–459. https://doi.org/10.1111/1574-6941.12236

    Article  CAS  PubMed  Google Scholar 

  31. Ingerslev HC, von Gersdorff Jørgensen L, Lenz Strube M, Larsen N, Dalsgaard I, Boye M, Madsen L (2014) The development of the gut microbiota in rainbow trout (Oncorhynchus mykiss) is affected by first feeding and diet type. Aquaculture 424–425:24–34. https://doi.org/10.1016/j.aquaculture.2013.12.032

    Article  Google Scholar 

  32. Gómez GD, Balcázar JL (2008) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol Med Microbiol 52:145–154. https://doi.org/10.1111/j.1574-695X.2007.00343.x

    Article  CAS  PubMed  Google Scholar 

  33. Llewellyn MS, Boutin S, Hoseinifar SH, Derome N (2014) Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries. Front Microbiol 5:207. https://doi.org/10.3389/fmicb.2014.00207

    Article  PubMed  PubMed Central  Google Scholar 

  34. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes J, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Aßhauer KP, Wemheuer B, Daniel R, Meinicke P (2015) Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 31:2882–2884. https://doi.org/10.1093/bioinformatics/btv287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Li H, Zheng Z, Cong-xin X, Bo H, Chao-yuan W, Gang H (2009) Isolation of cellulose-producing microbes from the intestine of grass carp (Ctenopharyngodon idellus). Environ Biol Fishes 86:131–135. https://doi.org/10.1007/978-90-481-3458-8_19

    Article  Google Scholar 

  37. Li H, Wu S, Wirth S, Hao Y, Wang W, Zou H, Li W, Wang G (2016) Diversity and activity of cellulolytic bacteria, isolated from the gut contents of grass carp (Ctenopharyngodon idellus) (Valenciennes) fed on Sudan grass (Sorghum sudanense) or artificial feedstuffs. Aquac Res 47:153–164. https://doi.org/10.1111/are.12478

    Article  CAS  Google Scholar 

  38. McDonald R, Schreier HJ, Watts JE (2012) Phylogenetic analysis of microbial communities in different regions of the gastrointestinal tract in Panaque nigrolineatus, a wood-eating fish. PLoS One 7:e48018. https://doi.org/10.1371/journal.pone.0048018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Watts JEM, McDonald R, Daniel R, Schreier HJ (2013) Examination of a culturable microbial population from the gastrointestinal tract of the wood-eating loricariid catfish Panaque nigrolineatus. Diversity 5:641–656. https://doi.org/10.3390/d5030641

    Article  CAS  Google Scholar 

  40. Clements KD, Pasch IBY, Moran D, Turner SJ (2007) Clostridia dominate 16S rRNA gene libraries prepared from the hindgut of temperate marine herbivorous fishes. Mar Biol 150:1431–1440. https://doi.org/10.1007/s00227-006-0443-9

    Article  CAS  Google Scholar 

  41. Catalan N, Villasante A, Wacyk J, Ramírez C, Romero J (2017) Fermented soybean meal increases lactic acid bacteria in gut microbiota of Atlantic Salmon (Salmo salar). Probiot Antimicrob Proteins. https://doi.org/10.1007/s12602-017-9366-7

    Article  Google Scholar 

  42. Montalban-Arques A, De Schryver P, Bossier P, Gorkiewicz G, Mulero V, Gatlin DM, Galindo-Villegas J (2015) Selective manipulation of the gut microbiota improves immune status in vertebrates. Front Immunol 6:512. https://doi.org/10.3389/fimmu.2015.00512

    Article  PubMed  PubMed Central  Google Scholar 

  43. Maji A, Misra R, Dhakan DB, Gupta V, Mahato NK, Saxena R, Mittal P, Thukral N, Sharma E, Singh A, Virmani R, Gaur M, Singh H, Hasija Y, Arora G, Agrawal A, Chaudhry A, Khurana JP, Sharma VK, Lal R, Singh Y (2018) Gut microbiome contributes to impairment of immunity in pulmonary tuberculosis patients by alteration of butyrate and propionate producers. Environ Microbiol 20:402–419. https://doi.org/10.1111/1462-2920.14015

    Article  CAS  PubMed  Google Scholar 

  44. Yan Q, Li J, Yu Y, Wang J, He Z, Van Nostrand JD, Kempher ML, Wu L, Wang Y, Liao L, Li X, Wu S, Ni J, Wang C, Zhou J (2016) Environmental filtering decreases with fish development for the assembly of gut microbiota. Environ Microbiol 18:4739–4754. https://doi.org/10.1111/1462-2920.13365

    Article  CAS  PubMed  Google Scholar 

  45. Burns AR, Stephens WZ, Stagaman K, Wong S, Rawls JF, Guillemin K, Bohannan BJ (2016) Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J 10:655–664. https://doi.org/10.1038/ismej.2015.142

    Article  CAS  PubMed  Google Scholar 

  46. Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848. https://doi.org/10.1016/j.cell.2006.02.017

    Article  CAS  PubMed  Google Scholar 

  47. Rieu A, Aoudia N, Jego G, Chluba J, Yousfi N, Briandet R, Deschamps J, Gasquet B, Monedero V, Garrido C, Guzzo J (2014) The biofilm mode of life boosts the anti-inflammatory properties of Lactobacillus. Cell Microbiol 16:1836–1853. https://doi.org/10.1111/cmi.12331

    Article  CAS  PubMed  Google Scholar 

  48. de Vos WM (2015) Microbial biofilms and the human intestinal microbiome. NPJ Biofilms Microbiomes 1:15005. https://doi.org/10.1038/npjbiofilms.2015.5

    Article  PubMed  PubMed Central  Google Scholar 

  49. Kalia VC, Prakash J, Koul S, Ray S (2017) Simple and rapid method for detecting biofilm forming bacteria. Indian J Microbiol 57:109–111. https://doi.org/10.1007/s12088-016-0616-2

    Article  CAS  PubMed  Google Scholar 

  50. Sanchez LM, Cheng AT, Warner CJ, Townsley L, Peach KC, Navarro G, Shikuma NJ, Bray WM, Riener RM, Yildiz FH, Linington RG (2016) Biofilm formation and detachment in gram-negative pathogens is modulated by select bile acids. PLoS One 11:e0149603. https://doi.org/10.1371/journal.pone.0149603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Larsen AM, Mohammed HH, Arias CR (2014) Comparison of DNA extraction protocols for the analysis of gut microbiota in fishes. FEMS Microbiol Lett 362:fnu031. https://doi.org/10.1093/femsle/fnu031

    Article  PubMed  CAS  Google Scholar 

  52. Gajardo K, Rodiles A, Kortner TM, Krogdahl Å, Bakke AM, Merrifield DL, Sørum H (2016) A high-resolution map of the gut microbiota in Atlantic salmon (Salmo salar): a basis for comparative gut microbial research. Sci Rep 6:30893. https://doi.org/10.1038/srep30893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Ye L, Amberg J, Chapman D, Gaikowski M, Liu WT (2014) Fish gut microbiota analysis differentiates physiology and behavior of invasive Asian carp and indigenous American fish. ISME J 8:541–551. https://doi.org/10.1038/ismej.2013.181

    Article  CAS  PubMed  Google Scholar 

  54. Wong S, Rawls JF (2012) Intestinal microbiota composition in fishes is influenced by host ecology and environment. Mol Ecol 21:3100–3102. https://doi.org/10.1111/j.1365-294X.2012.05646.x

    Article  PubMed  PubMed Central  Google Scholar 

  55. Rawls JF, Mahowald MA, Ley RE, Gordon JI (2006) Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 127:423–433. https://doi.org/10.1016/j.cell.2006.08.043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Hennersdorf P, Kleinertz S, Theisen S, Abdul-Aziz MA, Mrotzek G, Palm HW, Saluz HP (2016) Microbial diversity and parasitic load in tropical fish of different environmental conditions. PLoS One 11:e0151594. https://doi.org/10.1371/journal.pone.0151594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Miyake S, Ngugi DK, Stingl U (2015) Diet strongly influences the gut microbiota of surgeonfishes. Mol Ecol 24:656–672. https://doi.org/10.1111/mec.13050

    Article  PubMed  Google Scholar 

  58. Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH (2013) The influence of diet on the gut microbiota. Pharmacol Res 69:52–60. https://doi.org/10.1016/j.phrs.2012.10.020

    Article  CAS  PubMed  Google Scholar 

  59. Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Knight R, Caporaso JG, Svanback R (2014) Individuals’ diet diversity influences gut microbial diversity in two freshwater fish (threespine stickleback and Eurasian perch). Ecol Lett 17:979–987. https://doi.org/10.1111/ele.12301

    Article  PubMed  PubMed Central  Google Scholar 

  60. Saha S, Roy RN, Sen SK, Ray AK (2006) Characterization of cellulase-producing bacteria from the digestive tract of tilapia, Oreochromis mossambica (Peters) and grass carp, Ctenopharyngodon idella (Valenciennes). Aquac Res 37:380–388. https://doi.org/10.1111/j.1365-2109.2006.01442.x

    Article  CAS  Google Scholar 

  61. Dehler CE, Secombes CJ, Martin SA (2017) Environmental and physiological factors shape the gut microbiota of Atlantic salmon parr (Salmo salar L.). Aquaculture 467:149–157. https://doi.org/10.1016/j.aquaculture.2016.07.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. 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 74:239–249. https://doi.org/10.1007/s00248-016-0924-4

    Article  PubMed  Google Scholar 

  63. Giatsis C, Sipkema D, Smidt H, Heilig H, Benvenuti G, Verreth J, Verdegem M (2015) The impact of rearing environment on the development of gut microbiota in tilapia larvae. Sci Rep 5:18206. https://doi.org/10.1038/srep18206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Eichmiller JJ, Hamilton MJ, Staley C, Sadowsky MJ, Sorensen PW (2016) Environment shapes the fecal microbiome of invasive carp species. Microbiome 4:44. https://doi.org/10.1186/s40168-016-0190-1

    Article  PubMed  PubMed Central  Google Scholar 

  65. Schmidt VT, Smith KF, Melvin DW, Amaral-Zettler LA (2015) Community assembly of a euryhaline fish microbiome during salinity acclimation. Mol Ecol 24:2537–2550. https://doi.org/10.1111/mec.13177

    Article  PubMed  Google Scholar 

  66. Sylvain FÉ, Cheaib B, Llewellyn M, Correia TG, Fagundes DB, Val AL, Derome N (2016) pH drop impacts differentially skin and gut microbiota of the Amazonian fish tambaqui (Colossoma macropomum). Sci Rep 6:32032. https://doi.org/10.1038/srep32032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. 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. https://doi.org/10.1007/s12275-012-1340-1

    Article  CAS  PubMed  Google Scholar 

  68. Li XM, Zhu YJ, Yan QY, Ringø E, Yang DG (2014) Do the intestinal microbiotas differ between paddlefish (Polyodon spathala) and bighead carp (Aristichthys nobilis) reared in the same pond? J Appl Microbiol 117:1245–1252. https://doi.org/10.1111/jam.12626

    Article  CAS  PubMed  Google Scholar 

  69. Wong S, Waldrop T, Summerfelt S, Davidson J, Barrows F, Kenney PB, Welch T, Wiens GD, Snekvik K, Rawls JF, Good C (2013) Aquacultured rainbow trout (Oncorhynchus mykiss) possess a large core intestinal microbiota that is resistant to variation in diet and rearing density. Appl Environ Microbiol 79:4974–4984. https://doi.org/10.1128/AEM.00924-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Sullam KE, Rubin BE, Dalton CM, Kilham SS, Flecker AS, Russell JA (2015) Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies. ISME J 9:1508–1522. https://doi.org/10.1038/ismej.2014.231

    Article  PubMed  PubMed Central  Google Scholar 

  71. Li T, Long M, Li H, Gatesoupe FJ, 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. https://doi.org/10.3389/fmicb.2017.00454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Michl SC, Ratten JM, 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. https://doi.org/10.1371/journal.pone.0177735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Mansfield GS, Desai AR, Nilson SA, Van Kessel AG, Drew MD, Hill JE (2010) Characterization of rainbow trout (Oncorhynchus mykiss) intestinal microbiota and inflammatory marker gene expression in a recirculating aquaculture system. Aquaculture 307:95–104. https://doi.org/10.1016/j.aquaculture.2010.07.014

    Article  CAS  Google Scholar 

  74. Ringø E, Zhou Z, Vecino JLG, Wadsworth S, Romero J, Krogdahl Å, Olsen RE, Dimitroglou A, Foey A, Davies S, Owen M, Lauzon HL, Martinsen LL, De Schryver P, Bossier P, Sperstad S, Merrifield DL (2016) Effect of dietary components on the gut microbiota of aquatic animals. A never-ending story? Aquac Nutr 22:219–282. https://doi.org/10.1111/anu.12346

    Article  CAS  Google Scholar 

  75. Rajendhran J, Gunasekaran P (2010) Human microbiomics. Indian J Microbiol 50:109–112. https://doi.org/10.1007/s12088-010-0034-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Sangwan N, Lambert C, Sharma A, Gupta V, Khurana P, Khurana JP, Sockett RE, Gilbert JA, Lal R (2015) Arsenic rich Himalayan hot spring metagenomics reveal genetically novel predator-prey genotypes. Environ Microbiol Rep 7:812–823. https://doi.org/10.1111/1758-2229.12297

    Article  CAS  PubMed  Google Scholar 

  77. Sangwan N, Lata P, Dwivedi V, Singh A, Niharika N, Kaur J (2012) Comparative metagenomic analysis of soil microbial communities across three hexachlorocyclohexane contamination levels. PLoS One 7:e46219. https://doi.org/10.1371/journal.pone.0046219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Dwivedi V, Sangwan N, Nigam A, Garg N, Niharika N, Khurana P, Khurana JP, Lal R (2012) Draft genome sequence of Thermus sp. RL isolated from hot water spring located atop the Himalayan ranges at Manikaran, India. J Bacteriol 194:3534–3535. https://doi.org/10.1128/JB.00604-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Singh AK, Sangwan N, Sharma A, Gupta V, Khurana JP, Lal R (2013) Draft genome sequence of Sphingobium quisquiliarum P25T, a novel Hexachlorocylohexane (HCH) degrading bacterium isolated from the HCH dumpsite. Genome Announc 1:e00717-12. https://doi.org/10.1128/genomeA.00717-13

    Article  Google Scholar 

  80. Mukherjee U, Kumar R, Mahato NK, Khurana JP, Lal R (2013) Draft genome sequence of Sphingobium sp. HDIPO4, an avid degrader of Hexachlorocyclohexane. Genome Announc 1:e00749-13. https://doi.org/10.1128/genomeA.00749-13

    Article  PubMed  PubMed Central  Google Scholar 

  81. Kaur J, Verma H, Tripathi C, Khurana JP, Lal R (2013) Draft genome sequence of a Hexachlorocyclohexane-degrading bacterium, Sphingobium baderi strain LL03T. Genome Announc 1:e00751-13. https://doi.org/10.1128/genomeA.00751-13

    Article  PubMed  PubMed Central  Google Scholar 

  82. Dua A, Malhotra J, Saxena A, Khan F, Lal R (2013) Devosia lucknowensis sp. nov., a bacterium isolated from Hexachlorocyclohexane (HCH) contaminated pond soil. J Microbiol 51:689–694. https://doi.org/10.1007/s12275-013-2705-9

    Article  CAS  PubMed  Google Scholar 

  83. Dua A, Sangwan N, Kaur J, Saxena A, Kohli P, Gupta AK, Lal R (2013) Draft genome sequence of Agrobacterium sp. Strain UHFBA-218, isolated from rhizosphere soil of crown gall-infected cherry rootstock colt. Genome Announc 1:e00302–e00313. https://doi.org/10.1128/genomeA.00302-13

    Article  PubMed  PubMed Central  Google Scholar 

  84. Negi V, Lata P, Sangwan N, Gupta S, Das S, Rao DLN, Lal R (2014) Draft genome sequence of Hexachlorocyclohexane (HCH)-degrading Sphingobium lucknowense strain F2, isolated from the HCH dumpsite. Genome Announc 2:e00788-14. https://doi.org/10.1128/genomeA.00788-14

    Article  PubMed  PubMed Central  Google Scholar 

  85. Sharma A, Hira P, Shakarad M, Lal R (2014) Draft genome sequence of Cellulosimicrobium sp. MM, isolated from arsenic rich microbial mats of a Himalayan hot spring. Genome Announc 5:e01020-14. https://doi.org/10.1128/genomeA.01020-14

    Article  Google Scholar 

  86. Schrader C, Schielke A, Ellerbroek L, Johne R (2012) PCR inhibitors—occurrence, properties and removal. J Appl Microbiol 113:1014–1026. https://doi.org/10.1111/j.1365-2672.2012.05384.x

    Article  CAS  PubMed  Google Scholar 

  87. Kashinskaya EN, Andree KB, Simonov EP, Solovyev MM (2017) DNA extraction protocols may influence biodiversity detected in the intestinal microbiome: a case study from wild Prussian carp. Carassius gibelio. FEMS Microbiol Ecol 93:fiw240. https://doi.org/10.1093/femsec/fiw240

    Article  CAS  PubMed  Google Scholar 

  88. Hart ML, Meyer A, Johnson PJ, Ericsson AC (2015) Comparative evaluation of DNA extraction methods from feces of multiple host species for downstream next-generation sequencing. PLoS One 10:e0143334. https://doi.org/10.1371/journal.pone.0143334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Henderson G, Cox F, Kittelmann S, Miri VH, Zethof M, Noel SJ, Waghorn GC, Janssen PH (2013) Effect of DNA extraction methods and sampling techniques on the apparent structure of cow and sheep rumen microbial communities. PLoS One 8:e74787. https://doi.org/10.1371/journal.pone.0074787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Mirsepasi H, Persson S, Struve C, Andersen LOB, Petersen AM, Krogfelt KA (2014) Microbial diversity in fecal samples depends on DNA extraction method: easyMag DNA extraction compared to QIAamp DNA stool mini kit extraction. BMC Res Notes 7:50. https://doi.org/10.1186/1756-0500-7-50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Kanther M, Rawls JF (2010) Host-microbe interactions in the developing zebrafish. Curr Opin Immunol 22:10–19. https://doi.org/10.1016/j.coi.2010.01.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Cheesman SE, Guillemin K (2007) We know you are in there: conversing with the indigenous gut microbiota. Res Microbiol 158:2–9. https://doi.org/10.1016/j.resmic.2006.10.005

    Article  PubMed  Google Scholar 

  93. Kalia VC (2014) Microbes, antimicrobials and resistance: the battle goes on. Indian J Microbiol 54:1–2. https://doi.org/10.1007/s12088-013-0443-7

    Article  CAS  PubMed  Google Scholar 

  94. Austin B (2011) Taxonomy of bacterial fish pathogens. Vet Res 42:20. https://doi.org/10.1186/1297-9716-42-20

    Article  PubMed  PubMed Central  Google Scholar 

  95. Kalia VC (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31:224–245. https://doi.org/10.1016/j.biotechadv.2012.10.004

    Article  CAS  PubMed  Google Scholar 

  96. Koul S, Kalia VC (2017) Multiplicity of quorum quenching enzymes: a potential mechanism to limit quorum sensing bacterial population. Indian J Microbiol 57:100–108. https://doi.org/10.1007/s12088-016-0633-1

    Article  CAS  PubMed  Google Scholar 

  97. Kalia VC, Purohit HJ (2011) Quenching the quorum sensing system: potential antibacterial drug targets. Crit Rev Microbiol 37:121–140. https://doi.org/10.3109/1040841X.2010.532479

    Article  CAS  PubMed  Google Scholar 

  98. Chu W, Lu F, Zhu W, Kang C (2011) Isolation and characterization of new potential probiotic bacteria based on quorum-sensing system. J Appl Microbiol 110:202–208. https://doi.org/10.1111/j.1365-2672.2010.04872.x

    Article  CAS  PubMed  Google Scholar 

  99. Willis AR, Moore C, Mazon-Moya M, Krokowski S, Lambert C, Till R, Mostowy S, Sockett RE (2016) Injections of predatory bacteria work alongside host immune cells to treat Shigella infection in Zebrafish larvae. Curr Biol 26:3343–3351. https://doi.org/10.1016/j.cub.2016.09.067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Cao H, He S, Wang H, Hou S, Lu L, Yang X (2012) Bdellovibrios, potential biocontrol bacteria against pathogenic Aeromonas hydrophila. Vet Microbiol 154:413–418. https://doi.org/10.1016/j.vetmic.2011.07.032

    Article  PubMed  Google Scholar 

  101. Chu WH, Zhu W (2010) Isolation of Bdellovibrio as biological therapeutic agents used for the treatment of Aeromonas hydrophila infection in fish. Zoonoses Public Health 57:258–264. https://doi.org/10.1111/j.1863-2378.2008.01224.x

    Article  CAS  PubMed  Google Scholar 

  102. Feng S, Tan CH, Cohen Y, Rice SA (2016) Isolation of Bdellovibrio bacteriovorus from a tropical wastewater treatment plant and predation of mixed species biofilms assembled by the native community members. Environ Microbiol 18:3923–3931. https://doi.org/10.1111/1462-2920.13384

    Article  CAS  PubMed  Google Scholar 

  103. Oyedara OO, De Luna-Santillana EJ, Olguin-Rodriguez O, Guo X, Mendoza-Villa MA et al (2016) Isolation of Bdellovibrio sp. from soil samples in Mexico and their potential applications in control of pathogens. Microbiologyopen 5:992–1002. https://doi.org/10.1002/mbo3.382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Iebba V, Santangelo F, Totino V, Nicoletti M, Gagliardi A et al (2013) Higher prevalence and abundance of Bdellovibrio bacteriovorus in the human gut of healthy subjects. PLoS One 8:e61608. https://doi.org/10.1371/journal.pone.0061608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. He S, Ran C, Qin C, Li S, Zhang H, de Vos WM, Ringø E, Zhou Z (2017) Anti-infective effect of adhesive probiotic Lactobacillus in fish is correlated with their spatial distribution in the intestinal tissue. Sci Rep 7:13195. https://doi.org/10.1038/s41598-017-13466-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Koul S, Kalia VC (2016) Comparative genomics reveals biomarkers to identify Lactobacillus species. Indian J Microbiol 56:265–276. https://doi.org/10.1007/s12088-016-0605-5

    Article  PubMed  PubMed Central  Google Scholar 

  107. Zhang Z, Li D, Refaey MM, Xu W, Tang R, Li L (2018) Host age affects the development of southern catfish gut bacterial community divergent from that in the food and rearing water. Front Microbiol 9:495. https://doi.org/10.3389/fmicb.2018.00495

    Article  PubMed  PubMed Central  Google Scholar 

  108. Zhang Z, Li D, Refaey MM, Xu W (2017) High spatial and temporal variations of microbial community along the southern catfish gastrointestinal tract: insights into dynamic food digestion. Front Microbiol 8:1531. https://doi.org/10.3389/fmicb.2017.01531

    Article  PubMed  PubMed Central  Google Scholar 

  109. Koo H, Hakim JA, Powell ML, Kumar R, Eipers PG, Morrow CD, Crowley M, Lefkowitz EJ, Watts SA, Bej AK (2017) Metagenomics approach to the study of the gut microbiome structure and function in zebrafish Danio rerio fed with gluten formulated diet. J Microbiol Methods 135:69–76. https://doi.org/10.1016/j.mimet.2017.01.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Nielsen S, Walburn JW, Vergés A, Thomas T, Egan S (2017) Microbiome patterns across the gastrointestinal tract of the rabbitfish Siganus fuscescens. PeerJ 5:e3317. https://doi.org/10.7717/peerj.3317

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  111. Carlson JM, Leonard AB, Hyde ER, Petrosino JF, Primm TP (2017) Microbiome disruption and recovery in the fish Gambusia affinis following exposure to broad-spectrum antibiotic. Infect Drug Resist 10:143–154. https://doi.org/10.2147/IDR.S129055

    Article  PubMed  PubMed Central  Google Scholar 

  112. Li T, Li H, Gatesoupe FJ, She R, Lin Q, Yan X, Li J, Li X (2017) Bacterial signatures of “Red-Operculum” disease in the gut of crucian carp (Carassius auratus). Microb Ecol 74:510–521. https://doi.org/10.1007/s00248-017-0967-1

    Article  PubMed  Google Scholar 

  113. Stagaman K, Burns AR, Guillemin K, Bohannan BJ (2017) The role of adaptive immunity as an ecological filter on the gut microbiota in zebrafish. ISME J 11:1630–1639. https://doi.org/10.1038/ismej.2017.28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Gajardo K, Jaramillo-Torres A, Kortner TM, Merrifield DL, Tinsley J, Bakke AM, Krogdahl Å (2017) Alternative protein sources in the diet modulate microbiota and functionality in the distal intestine of Atlantic salmon (Salmo salar). Appl Environ Microbiol 83:e02615–e02616. https://doi.org/10.1128/AEM.02615-16

    Article  PubMed  PubMed Central  Google Scholar 

  115. Zhai Q, Yu L, Li T, Zhu J, Zhang C, Zhao J, Zhang H, Chen W (2017) Effect of dietary probiotic supplementation on intestinal microbiota and physiological conditions of Nile tilapia (Oreochromis niloticus) under waterborne cadmium exposure. Antonie Van Leeuwenhoek 110:501–513. https://doi.org/10.1007/s10482-016-0819-x

    Article  CAS  PubMed  Google Scholar 

  116. Lyons PP, Turnbull JF, Dawson KA, Crumlish M (2017) Phylogenetic and functional characterization of the distal intestinal microbiome of rainbow trout Oncorhynchus mykiss from both farm and aquarium settings. J Appl Microbiol 122:347–363. https://doi.org/10.1111/jam.13347

    Article  CAS  PubMed  Google Scholar 

  117. Song W, Li L, Huang H, Jiang K, Zhang F, Chen X, Zhao M, Ma L (2016) The gut microbial community of Antarctic fish detected by 16S rRNA gene sequence analysis. Biomed Res Int 2016:3241529. https://doi.org/10.1155/2016/3241529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. 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. https://doi.org/10.1371/journal.pone.0166379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Giatsis C, Sipkema D, Ramiro-Garcia J, Bacanu GM, Abernathy J, Verreth J, Smidt H, Verdegem M (2016) Probiotic legacy effects on gut microbial assembly in tilapia larvae. Sci Rep 6:33965. https://doi.org/10.1038/srep33965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Gatesoupe FJ, Huelvan C, Le Bayon N, Le Delliou H, Madec L, Mouchel O, Quazuguel P, Mazurais D, Zambonino-Infante JL (2016) The highly variable microbiota associated to intestinal mucosa correlates with growth and hypoxia resistance of sea bass, Dicentrarchus labrax, submitted to different nutritional histories. BMC Microbiol 16:266. https://doi.org/10.1186/s12866-016-0885-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Stephens WZ, Burns AR, Stagaman K, Wong S, Rawls JF, Guillemin K, Bohannan BJM (2016) The composition of the zebrafish intestinal microbial community varies across development. ISME J 10:644–654. https://doi.org/10.1038/ismej.2015.140

    Article  CAS  PubMed  Google Scholar 

  122. Schmidt V, Amaral-Zettler L, Davidson J, Summerfelt S, Good C (2016) Influence of fishmeal-free diets on microbial communities in Atlantic Salmon (Salmo salar) recirculation aquaculture systems. Appl Environ Microbiol 82:4470–4481. https://doi.org/10.1128/AEM.00902-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Zarkasi KZ, Taylor RS, Abell GC, Tamplin ML, Glencross BD, Bowman JP (2016) Atlantic Salmon (Salmo salar L.) gastrointestinal microbial community dynamics in relation to digesta properties and diet. Microb Ecol 71:589–603. https://doi.org/10.1007/s00248-015-0728-y

    Article  CAS  PubMed  Google Scholar 

  124. Llewellyn MS, McGinnity P, Dionne M, Letourneau J, Thonier F, Carvalho GR, Creer S, Derome N (2016) The biogeography of the atlantic salmon (Salmo salar) gut microbiome. ISME J 10:1280–1284. https://doi.org/10.1038/ismej.2015.189

    Article  PubMed  Google Scholar 

  125. Narrowe AB, Albuthi-Lantz M, Smith EP, Bower KJ, Roane TM, Vajda AM, Miller CS (2015) Perturbation and restoration of the fathead minnow gut microbiome after low-level triclosan exposure. Microbiome 3:6. https://doi.org/10.1186/s40168-015-0069-6

    Article  PubMed  PubMed Central  Google Scholar 

  126. NCBI Resource Coordinators (2016) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 44:D7–D19. https://doi.org/10.1093/nar/gkv1290

    Article  CAS  Google Scholar 

  127. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604

    Article  CAS  PubMed  Google Scholar 

  129. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196. https://doi.org/10.1093/nar/gkm864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072. https://doi.org/10.1128/AEM.03006-05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145. https://doi.org/10.1093/nar/gkn879

    Article  CAS  PubMed  Google Scholar 

  132. Rosen GL, Reichenberger ER, Rosenfeld AM (2011) NBC: the Naive Bayes classification tool webserver for taxonomic classification of metagenomic reads. Bioinformatics 27:127–129. https://doi.org/10.1093/bioinformatics/btq619

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors acknowledge funds from ICAR-National Bureau of Agriculturally Important Microorganisms NBAIM. CT and SN gratefully acknowledge Council of Scientific & Industrial Research (CSIR) and Department of Biotechnology (DBT), Govt. of India respectively, for providing doctoral fellowships.

Author information

Authors and Affiliations

  1. Department of Zoology, University of Delhi, Delhi, 110007, India

    Chandni Talwar, Shekhar Nagar, Rup Lal & Ram Krishan Negi

Authors
  1. Chandni Talwar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shekhar Nagar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rup Lal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ram Krishan Negi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

RL and RKN conceived the idea. CT wrote the manuscript and SN helped shape the manuscript. RL and RKN critically reviewed the manuscript.

Corresponding authors

Correspondence to Rup Lal or Ram Krishan Negi.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Talwar, C., Nagar, S., Lal, R. et al. Fish Gut Microbiome: Current Approaches and Future Perspectives. Indian J Microbiol 58, 397–414 (2018). https://doi.org/10.1007/s12088-018-0760-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12088-018-0760-y

Keywords

Search

Navigation