Bacterial Signatures of “Red-Operculum” Disease in the Gut of Crucian Carp (Carassius auratus)


Fish gut microbiota play important roles in fish immunity, nutrition, and the adaptation to environmental changes. To date, few studies have focused on the interactions among environmental factors, fish diseases, and gut microbiota compositions. We compared the gut bacterial communities of healthy crucian carps (Carassius auratus) with those of individuals affected by “red-operculum” disease and corresponding water and sediment microbiota in four fish farm ponds. Distinct gut bacterial communities were observed in healthy and diseased fish. The bacterial communities of diseased fish were less diverse and stable than those of healthy individuals. The differences in bacterial community compositions between diseased and healthy fish were explained by the changes in the relative abundances of some specific bacterial OTUs, which belonged to the genera such as Vibrio, Aeromonas, and Shewanella, and they were prevalent in diseased fish, but rare or even absent in environmental samples. Water temperature and ammonia concentration were the two most important environmental factors that impacted gut microbiota in diseased fish. These results highlighted the surge of some potential pathogens as bacterial signatures that were associated with “red-operculum” disease in crucian carps.

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3


  1. 1.

    Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6(10):776–788

  2. 2.

    Walter J, Britton RA, Roos S (2011) Host-microbial symbiosis in the vertebrate gastrointestinal tract and the lactobacillus reuteri paradigm. Proc. Natl. Acad. Sci. U. S. A. 108(Supplement 1):4645–4652

  3. 3.

    O’Hara AM, Shanahan F (2006) The gut flora as a forgotten organ. EMBO Rep. 7(7):688–693. doi:10.1038/sj.embor.7400731

  4. 4.

    Clarke SF, Murphy EF, O’Sullivan O, Lucey AJ, Humphreys M, Hogan A, Hayes P, O’Reilly M, Jeffery IB, Wood-Martin R, Kerins DM, Quigley E, Ross RP, O’Toole PW, Molloy MG, Falvey E, Shanahan F, Cotter PD (2014) Exercise and associated dietary extremes impact on gut microbial diversity. Gut 63(12):1913–1920. doi:10.1136/gutjnl-2013-306541

  5. 5.

    Berg RD (1992) Translocation and the indigenous gut flora. In: Probiotics. Springer, Netherlands, pp 55–85

  6. 6.

    Ringø E, Birkbeck T (1999) Intestinal microflora of fish larvae and fry. Aquac. Res. 30(2):73–93

  7. 7.

    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(2):e30440. doi:10.1371/journal.pone.0030440

  8. 8.

    Ringø E, Myklebust R, Mayhew TM, Olsen RE (2007) Bacterial translocation and pathogenesis in the digestive tract of larvae and fry. Aquaculture 268(1):251–264

  9. 9.

    Ringø E, Jutfelt F, Kanapathippillai P, Bakken Y, Sundell K, Glette J, Mayhew TM, Myklebust R, Olsen RE (2004) Damaging effect of the fish pathogen Aeromonas salmonicida ssp. salmonicida on intestinal enterocytes of Atlantic salmon (Salmo salar L.) Cell Tissue Res. 318(2):305–311

  10. 10.

    Ringø E, Mikkelsen H, Kaino T, Olsen RE, Mayhew TM, Myklebust R (2006) Endocytosis of indigenous bacteria and cell damage caused by vibrio anguillarum in the foregut and hindgut of spotted wolffish (Anarhichas minor Olafsen) fry: an electron microscopical study. Aquac. Res. 37(6):647–651

  11. 11.

    Jutfelt F, Olsen RE, Glette J, Ringo E, Sundell K (2006) Translocation of viable Aeromonas salmonicida across the intestine of rainbow trout, Oncorhynchus mykiss (Walbaum). J. Fish Dis. 29(5):255–262. doi:10.1111/j.1365-2761.2006.00715.x

  12. 12.

    Hansen G, Olafsen J (1990) Endocytosis of bacteria in yolksac larvae of cod (Gadus morhua L.). In: Microbiology in poecilotherms. Elsevier, Amsterdam, pp 187–191

  13. 13.

    Zhang XJ, Yang WM, Zhang DF, Li TT, Gong XN, Li AH (2015) Does the gastrointestinal tract serve as the infectious route of Aeromonas hydrophila in crucian carp (Carassius carassius)? Aquac. Res. 46(1):141–154

  14. 14.

    Ling SH, Wang XH, Lim TM, Leung KY (2001) Green fluorescent protein-tagged Edwardsiella Tarda reveals portal of entry in fish. FEMS Microbiol. Lett. 194(2):239–243

  15. 15.

    Kassinen A, Krogius-Kurikka L, Mäkivuokko H, Rinttilä T, Paulin L, Corander J, Malinen E, Apajalahti J, Palva A (2007) The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterology 133(1):24–33

  16. 16.

    Qin N, Yang F, Li A, Prifti E, Chen Y, Shao L, Guo J, Le Chatelier E, Yao J, Wu L (2014) Alterations of the human gut microbiome in liver cirrhosis. Nature 513(7516):59–64

  17. 17.

    Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, Benyamin FW, Lei YM, Jabri B, Alegre ML, Chang EB, Gajewski TF (2015) Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350(6264):1084–1089. doi:10.1126/science.aac4255

  18. 18.

    Li T, Long M, Ji C, Shen Z, Gatesoupe FJ, Zhang X, Zhang Q, Zhang L, Zhao Y, Liu X, Li A (2016) Alterations of the gut microbiome of largemouth bronze gudgeon (Coreius guichenoti) suffering from furunculosis. Sci Rep 6:30606. doi:10.1038/srep30606

  19. 19.

    Perez T, Balcazar JL, Ruiz-Zarzuela I, Halaihel N, Vendrell D, de Blas I, Muzquiz JL (2010) Host-microbiota interactions within the fish intestinal ecosystem. Mucosal Immunol. 3(4):355–360. doi:10.1038/mi.2010.12

  20. 20.

    Li T, Long M, Gatesoupe FJ, Zhang Q, Li A, Gong X (2015) Comparative analysis of the intestinal bacterial communities in different species of carp by pyrosequencing. Microb. Ecol. 69(1):25–36. doi:10.1007/s00248-014-0480-8

  21. 21.

    Li J, Ni J, Li J, Wang C, Li X, Wu S, Zhang T, Yu Y, Yan Q (2014) Comparative study on gastrointestinal microbiota of eight fish species with different feeding habits. J. Appl. Microbiol. 117(6):1750–1760. doi:10.1111/jam.12663

  22. 22.

    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(13):3363–3378

  23. 23.

    Ingerslev HC, Strube ML, Jorgensen L, Dalsgaard I, Boye M, Madsen L (2014) Diet type dictates the gut microbiota and the immune response against Yersinia Ruckeri in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 40(2):624–633. doi:10.1016/j.fsi.2014.08.021

  24. 24.

    Beasley DE, Koltz AM, Lambert JE, Fierer N, Dunn RR (2015) The evolution of stomach acidity and its relevance to the human microbiome. PLoS One 10(7):e0134116. doi:10.1371/journal.pone.0134116

  25. 25.

    Schmidt VT, Smith KF, Melvin DW, Amaral-Zettler LA (2015) Community assembly of a euryhaline fish microbiome during salinity acclimation. Mol. Ecol. 24(10):2537–2550. doi:10.1111/mec.13177

  26. 26.

    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(1):18–27. doi:10.1111/jam.12514

  27. 27.

    Starliper CE (2011) Bacterial coldwater disease of fishes caused by Flavobacterium psychrophilum. J. Adv. Res. 2(2):97–108. doi:10.1016/j.jare.2010.04.001

  28. 28.

    Beveridge MCM, Brummett RE (2015) Aquaculture and the environment. In: Freshwater fisheries ecology. Wiley, pp 794–803. doi:10.1002/9781118394380.ch55

  29. 29.

    Hrubec TC, Robertson JL, Smith SA, Tinker MK (1996) The effect of temperature and water quality on antibody response to Aeromonas salmonicida in sunshine bass (Morone Chrysops× Morone saxatilis). Vet Immunol Immunop 50(1):157–166

  30. 30.

    Rice CD, Arkoosh MR, Adams S (2002) Immunological indicators of environmental stress and disease susceptibility in fishes. In: Biological indicators of aquatic ecosystem stress. American Fisheries Society, Symposium 8, Bethesda, MD, pp 187–220

  31. 31.

    Zhang H, Sparks JB, Karyala SV, Settlage R, Luo XM (2015) Host adaptive immunity alters gut microbiota. ISME J 9(3):770–781. doi:10.1038/ismej.2014.165

  32. 32.

    Kroupova H, Machova J, Piackova V, Blahova J, Dobsikova R, Novotny L, Svobodova Z (2008) Effects of subchronic nitrite exposure on rainbow trout (Oncorhynchus mykiss). Ecotoxicol. Environ. Saf. 71(3):813–820. doi:10.1016/j.ecoenv.2008.01.015

  33. 33.

    Boutin S, Bernatchez L, Audet C, Derome N (2013) Network analysis highlights complex interactions between pathogen, host and commensal microbiota. PLoS One 8(12):e84772. doi:10.1371/journal.pone.0084772

  34. 34.

    Carballo M, Munoz M, Cuellar M, Tarazona J (1995) Effects of waterborne copper, cyanide, ammonia, and nitrite on stress parameters and changes in susceptibility to saprolegniosis in rainbow trout (Oncorhynchus mykiss). Appl. Environ. Microbiol. 61(6):2108–2112

  35. 35.

    Yearbook CFS (2014) China fishery statistics yearbook 2014. Bureau of Fisheries, China Agriculture Press, Beijing

  36. 36.

    Ziyu D, Huida C, Haoxiang Y, Dinghe J, Mingyao G, Xuancai Z (1993) Studies on hemorrhagic septicemia of blunt snout bream (Megalobrama amblycephala) and crucian carp (Carassius auratus). Fish Sci Technol Inf 3:001

  37. 37.

    Chen H, Lu C (1991) Study on the pathogen of epidemic septicemia occurred in cultured cyprinoid fishes in southeastern China. J Nanjing Agric Univ 14(4):87–91

  38. 38.

    Humphrey JD, Ashburner LD (1993) Spread of the bacterial fish pathogen Aeromonas salmonicida after importation of infected goldfish, Carassius auratus, into Australia. Aust. Vet. J. 70(12):452

  39. 39.

    Li A, Yang W, Hu J, Wang W, Cai T, Wang J (2006) Optimization by orthogonal array design and humoral immunity of the bivalent vaccine against Aeromonas hydrophila and Vibrio Fluvialis infection in crucian carp (Carassius auratus L.) Aquac. Res. 37(8):813–820

  40. 40.

    Jin L, Li X, Zou D, Li S, Song W, Xu Y (2013) Protection of crucian carp (Carassius auratus Gibelio) against septicaemia caused by Aeromonas hydrophila using specific egg yolk immunoglobulins. Aquac. Res. 44(6):928–936

  41. 41.

    Getchell RG, Erkinharju T, Johnson AO, Davis BW, Hatch EE, Cornwell ER, Bowser PR (2015) Goldfish Carassius auratus susceptibility to viral hemorrhagic septicemia virus genotype IVb depends on exposure route. Dis. Aquat. Org. 115(1):25–36. doi:10.3354/dao02872

  42. 42.

    Liu H, Fu F, Huang J, He J, Shi X, Gao L, Yang J, Jiang Y (2004) Amino acid sequence of a Chinese isolate of spring viraemia virus of carp and preliminary analysis of the glycoprotein gene. Virol. Sin. 20(6):647–651

  43. 43.

    Yue Z, Teng Y, Liang C, Xie X, Xu B, Zhu L, Lei Z, He J, Liu Z, Jiang Y, Liu H, Qin Q (2008) Development of a sensitive and quantitative assay for spring viremia of carp virus based on real-time RT-PCR. J. Virol. Methods 152(1–2):43–48. doi:10.1016/j.jviromet.2008.05.031

  44. 44.

    Boyd CE, Tucker CS (1992) Water quality and pond soil analyses for aquaculture. Water quality and pond soil analyses for aquaculture. Auburn University, Auburn

  45. 45.

    Tamaki H, Wright CL, Li X, Lin Q, Hwang C, Wang S, Thimmapuram J, Kamagata Y, Liu WT (2011) Analysis of 16S rRNA Amplicon Sequencing Options on the Roche/454 Next-Generation Titanium Sequencing Platform. PLoS ONE 6(9): e25263

  46. 46.

    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7(5):335–336. doi:10.1038/nmeth.f.303

  47. 47.

    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. doi:10.1093/bioinformatics/btr381

  48. 48.

    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75(23):7537–7541

  49. 49.

    Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. doi:10.1093/bioinformatics/btr507

  50. 50.

    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73(16):5261–5267

  51. 51.

    Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22(13):1658–1659. doi:10.1093/bioinformatics/btl158

  52. 52.

    Core TR (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  53. 53.

    Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5(10):R80

  54. 54.

    Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol. 12(6):R60. doi:10.1186/gb-2011-12-6-r60

  55. 55.

    Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31(9):814–821. doi:10.1038/nbt.2676

  56. 56.

    Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40(Database issue):D109–D114. doi:10.1093/nar/gkr988

  57. 57.

    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(7):5069–5072. doi:10.1128/aem.03006-05

  58. 58.

    Wang S, Loreau M (2014) Ecosystem stability in space: alpha, beta and gamma variability. Ecol. Lett. 17(8):891–901. doi:10.1111/ele.12292

  59. 59.

    Nayak SK (2010) Role of gastrointestinal microbiota in fish. Aquac. Res. 41(11):1553–1573

  60. 60.

    Kozinska A, Pekala A (2004) First isolation of Shewanella putrefaciens from freshwater fish-a potential new pathogen of fish. Bull Eur Ass Fish Pathol 24:189–193

  61. 61.

    Xing M, Hou Z, Yuan J, 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(3):432–443. doi:10.1111/1574-6941.12174

  62. 62.

    Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA (2008) Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6(2):121–131

  63. 63.

    Sugita H, Miyajima C, Deguchi Y (1991) The vitamin B12-producing ability of the intestinal microflora of freshwater fish. Aquaculture 92:267–276

  64. 64.

    Ahne W, Bjorklund HV, Essbauer S, Fijan N, Kurath G, Winton JR (2002) Spring viremia of carp (SVC). Dis. Aquat. Org. 52(3):261–272. doi:10.3354/dao052261

  65. 65.

    Nelson J, Rohovec J, Fryer J (1985) Tissue location of vibrio bacterin delivered by intraperitoneal injection, immersion and oral routes to Salmo gairdneri [rainbow trout]. Fish Pathol (Jpn) 19(4):263–269

  66. 66.

    Yardimci B, Aydin Y (2011) Pathological findings of experimental Aeromonas hydrophila infection in Nile tilapia (Oreochromis niloticus). Ankara Univ Vet Fak Derg 58:47–54

  67. 67.

    Schonherz AA, Hansen MH, Jorgensen HB, Berg P, Lorenzen N, Einer-Jensen K (2012) Oral transmission as a route of infection for viral haemorrhagic septicaemia virus in rainbow trout, Oncorhynchus mykiss (Walbaum). J. Fish Dis. 35(6):395–406. doi:10.1111/j.1365-2761.2012.01358.x

  68. 68.

    Zhang M, Sun Y, Liu Y, Qiao F, Chen L, Liu W-T, Du Z, Li E (2016) Response of gut microbiota to salinity change in two euryhaline aquatic animals with reverse salinity preference. Aquaculture 454:72–80

  69. 69.

    Elliott J (1981) Some aspects of thermal stress on freshwater teleosts. In: Stress and fish

  70. 70.

    Smith S, Bernatchez L, Beheregaray LB (2013) RNA-seq analysis reveals extensive transcriptional plasticity to temperature stress in a freshwater fish species. BMC Genomics 14:375. doi:10.1186/1471-2164-14-375

  71. 71.

    Yin F, Sun P, Peng S, Tang B, Zhang D, Wang C, Mu C, Shi Z (2013) The respiration, excretion and biochemical response of the juvenile common Chinese cuttlefish, Sepiella maindroni at different temperatures. Aquaculture 402:127–132

  72. 72.

    Wedemeyer GA (1996) Physiology of fish in intensive culture systems. Springer US, New York

  73. 73.

    Hargreaves JA, Tucker CS (2004) Managing ammonia in fish ponds, vol 4603. Southern Regional Aquaculture Center Stoneville, Stoneville

  74. 74.

    Durborow RM, Crosby DM, Brunson MW (1997) Ammonia in fish ponds. J. Fish. Res. Board Can. 32:2379–2383

  75. 75.

    Hansen G, Olafsen J (1999) Bacterial interactions in early life stages of marine cold water fish. Microb. Ecol. 38(1):1–26

  76. 76.

    Berg RD (1999) Bacterial translocation from the gastrointestinal tract. Adv. Exp. Med. Biol. 473:11–30

  77. 77.

    Olsen RE, Sundell K, Mayhew TM, Myklebust R, Ringø E (2005) Acute stress alters intestinal function of rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture 250(1):480–495

  78. 78.

    Ye L, Amberg J, Chapman D, Gaikowski M, Liu W-T (2013) Fish gut microbiota analysis differentiates physiology and behavior of invasive Asian carp and indigenous American fish. ISME J 8(3):541–551

  79. 79.

    De Brabandere L, Catalano MJ, Frazer TK, Allen MS (2009) Stable isotope evidence of ontogenetic changes in the diet of gizzard shad Dorosoma cepedianum. J. Fish Biol. 74(1):105–119. doi:10.1111/j.1095-8649.2008.02114.x

  80. 80.

    Harke MJ, Gobler CJ (2013) Global transcriptional responses of the toxic cyanobacterium, Microcystis aeruginosa, to nitrogen stress, phosphorus stress, and growth on organic matter. PLoS ONE 8(7):e69834

  81. 81.

    Skvortsov T, de Leeuwe C, Quinn JP, McGrath JW, Allen CCR, McElarney Y, Watson C, Arkhipova K, Lavigne R, Kulakov LA (2016) Metagenomic Characterisation of the Viral Community of Lough Neagh, the Largest Freshwater Lake in Ireland. PLoS ONE 11(2):e0150361

  82. 82.

    Ferrão-Filho AS, Kozlowsky-Suzuki B (2011) Cyanotoxins: bioaccumulation and effects on aquatic animals. Mar Drugs 9(12):2729–2772

  83. 83.

    Mou X, Lu X, Jacob J, Sun S, Heath R (2013) Metagenomic identification of bacterioplankton taxa and pathways involved in microcystin degradation in lake erie. PLoS One 8(4):e61890. doi:10.1371/journal.pone.0061890

  84. 84.

    Finegold SM, Vaisanen M-L, Molitoris DR, Tomzynski TJ, Song Y, Liu C, Collins MD, Lawson PA (2003) Cetobacterium somerae sp. nov. from human feces and emended description of the genus Cetobacterium. Syst. Appl. Microbiol. 26(2):177–181

  85. 85.

    Tsuchiya C, Sakata T, Sugita H (2008) Novel ecological niche of Cetobacterium somerae, an anaerobic bacterium in the intestinal tracts of freshwater fish. Lett. Appl. Microbiol. 46(1):43–48. doi:10.1111/j.1472-765X.2007.02258.x

  86. 86.

    Sugita H, Shibuya K, Shimooka H, Deguchi Y (1996) Antibacterial abilities of intestinal bacteria in freshwater cultured fish. Aquaculture 145(1):195–203

  87. 87.

    Merrifield DL, Shaw BJ, Harper GM, Saoud IP, Davies SJ, Handy RD, Henry TB (2013) Ingestion of metal-nanoparticle contaminated food disrupts endogenous microbiota in zebrafish (Danio rerio). Environ. Pollut. 174:157–163. doi:10.1016/j.envpol.2012.11.017

  88. 88.

    Wu S, Gao T, Zheng Y, Wang W, Cheng Y, Wang G (2010) Microbial diversity of intestinal contents and mucus in yellow catfish (Pelteobagrus fulvidraco). Aquaculture 303(1):1–7

  89. 89.

    Namba A, Mano N, Hirose H (2007) Phylogenetic analysis of intestinal bacteria and their adhesive capability in relation to the intestinal mucus of carp. J. Appl. Microbiol. 102(5):1307–1317

  90. 90.

    Russell NJ, Nichols DS (1999) Polyunsaturated fatty acids in marine bacteria--a dogma rewritten. Microbiology 145:767–779

  91. 91.

    Hau HH, Gralnick JA (2007) Ecology and biotechnology of the genus Shewanella. Annu. Rev. Microbiol. 61:237–258. doi:10.1146/annurev.micro.61.080706.093257

  92. 92.

    Dailey FE, McGraw JE, Jensen BJ, Bishop SS, Lokken JP, Dorff KJ, Ripley MP, Munro JB (2015) The microbiota of freshwater fish and freshwater niches contain omega-3 fatty acid-producing Shewanella species. Appl. Environ. Microbiol. 82(1):218–231. doi:10.1128/aem.02266-15

  93. 93.

    Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored "rare biosphere". Proc. Natl. Acad. Sci. U. S. A. 103(32):12115–12120. doi:10.1073/pnas.0605127103

  94. 94.

    Wadhams GH, Armitage JP (2004) Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5(12):1024–1037. doi:10.1038/nrm1524

Download references


This work was supported by Sichuan Province Science and Technology Project (2017SZ0004, 2017JY0231), Tongwei Co., Ltd., China, and China Biodiversity Observation Networks (Sino BON).

Author’s Contributions

Xiangzhen Li, Tongtong Li, and Huan Li conceived the research. Tongtong Li, Huan Li, and Xuefeng Yan performed the experiments. Tongtong Li wrote the manuscript. Tongtong Li, Xiangzhen Li, Huan Li, and François-Joël Gatesoupe edited the manuscript. She Rong, Qiang Lin, Xuefeng Yan, and Jiabao Li contributed sampling, reagents, or data analysis pipeline. All authors reviewed and accepted the manuscript.

Author information

Correspondence to Xiangzhen Li.

Ethics declarations

Ethical Approval

Compliance with the ethics committee of the Chengdu Institute of Biology, Chinese Academy of Sciences, and the methods used in this study were carried out in accordance with the approved guidelines.

Conflict of Interest

The authors declare that they have no conflicts of interest.

Electronic supplementary material


(PDF 1245 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Li, T., Li, H., Gatesoupe, F. et al. Bacterial Signatures of “Red-Operculum” Disease in the Gut of Crucian Carp (Carassius auratus). Microb Ecol 74, 510–521 (2017).

Download citation


  • Gut microbiota
  • Crucian carp
  • “Red-operculum” disease
  • Water temperature
  • Ammonia concentration