Skip to main content
Log in

Intestinal microbiota of healthy and unhealthy Atlantic salmon Salmo salar L. in a recirculating aquaculture system

  • Biology
  • Published:
Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

The present study sampled the intestinal content of healthy and unhealthy Atlantic salmon (Salmo salar L.), the ambient water of unhealthy fish, and the biofilter material in the recirculating aquaculture system (RAS) to understand differences in the intestinal microbiota. The V4–V5 regions of the prokaryotic 16S rRNA genes in the samples were analyzed by MiSeq high-throughput sequencing. The fish were adults with no differences in body length or weight. Representative members of the intestinal microbiota were identified. The intestinal microbiota of the healthy fish included Proteobacteria (44.33%), Actinobacteria (17.89%), Bacteroidetes (15.25%), and Firmicutes (9.11%), among which the families Micrococcaceae and Oxalobacteraceae and genera Sphingomonas, Streptomyces, Pedobacter, Janthinobacterium, Burkholderia, and Balneimonas were most abundant. Proteobacteria (70.46%), Bacteroidetes (7.59%), and Firmicutes (7.55%) dominated the microbiota of unhealthy fish, and Chloroflexi (2.71%), and Aliivibrio and Vibrio as well as genera in the family Aeromonadaceae were most strongly represented. Overall, the intestinal hindgut microbiota differed between healthy and unhealthy fish. This study offers a useful tool for monitoring the health status of fish and for screening the utility of probiotics by studying the intestinal microbiota.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Backhed F, Ding H, Wang T, Hooper L V, Koh G Y, Nagy A, Semenkovich C F, Gordon J I. 2004. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. U. S. A., 101 (44): 15718–15723.

    Article  Google Scholar 

  • Bakke-McKellep A M, Penn M H, Salas P M, Refstie S, Sperstad S, Landsverk T, Ringø E, Krogdahl Å. 2007. Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). Brit. J. Nutr., 97 (4): 699–713.

    Article  Google Scholar 

  • Balcázar J L, Vendrell D, de Blas I, Ruiz-Zarzuela I, Muzquiz J L, Girones O. 2008. Characterization of probiotic properties of lactic acid bacteria isolated from intestinal microbiota of fish. Aquaculture, 278 (1-4): 188–191.

    Article  Google Scholar 

  • Bik E M, Eckburg P B, Gill S R, Nelson K E, Purdom E A, Francois F, Perez-Perez G, Blaser M J, Relman D A. 2006. Molecular analysis of the bacterial microbiota in the human stomach. Proc. Natl. Acad. Sci. U. S. A., 103 (3): 732–737.

    Article  Google Scholar 

  • Blumberg R, Powrie F. 2012. Microbiota, disease, and back to health: a metastable journey. Sci. Transl. Med., 4 (137): 137rv7.

    Article  Google Scholar 

  • Caporaso J G, Kuczynski J, Stombaugh J, Bittinger K, Bushman F D, Costello E K, Fierer N, Peña A G, Goodrich J K, Gordon J I, Huttley G A, Kelley S T, Knights D, Koenig J E, Ley R E, Lozupone C A, McDonald D, McDonald B D, Pirrung M, Reeder J, Sevinsky J R, Turnbaugh P J, Walters W A, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods., 7 (5): 335–336.

    Article  Google Scholar 

  • Claesson M J, Jeffery I B, Conde S, Power S E, O’Connor E M, Cusack S, Harris H M B, Coakley M, Lakshminarayanan B, O’Sullivan O, Fitzgerald G F, Deane J, O’Connor M, Harnedy N, O’Connor K, O’Mahony D, van Sinderen D, Wallace M, Brennan L, Stanton C, Marchesi J R, Fitzgerald A P, Shanahan F, Hill C, Ross R P, O’Toole P W. 2012. Gut microbiota composition correlates with diet and health in the elderly. Nature, 488 (7410): 178–184.

    Article  Google Scholar 

  • Cole J R. 2003. The ribosomal database project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic. Acids. Res., 31 (1): 442–443.

    Article  Google Scholar 

  • Das S, Ward L R, Burke C. 2010. Screening of marine Streptomyces spp. for potential use as probiotics in aquaculture. Aquaculture, 305 (1-4): 32–41.

    Article  Google Scholar 

  • Defoirdt T, Boon N, Sorgeloos P, Verstraete W, Bossier P. 2007. Alternatives to antibiotics to control bacterial infections: luminescent vibriosis in aquaculture as an example. Trends. Biotechnol., 25 (10): 472–479.

    Article  Google Scholar 

  • Desai A R, Links M G, Collins S A, Mansfield G S, Drew M D, Van Kessel A G, Hill J E. 2012. Effects of plant-based diets on the distal gut microbiome of rainbow trout (Oncorhynchus mykiss). Aquaculture, 350-353: 134–142.

    Article  Google Scholar 

  • DeSantis T Z, Hugenholtz P, Larsen N, Rojas M, Brodie E L, Keller K, Huber T, Dalevi D, Hu P, Andersen G L. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol., 72 (7): 5069–5072.

    Article  Google Scholar 

  • Dharmaraj S. 2011. Antagonistic potential of marine actinobacteria against fish and shellfish pathogens. Turk. J. Bio l., 35 (3): 303–311.

    Google Scholar 

  • Donskey C J. 2004. The role of the intestinal tract as a reservoir and source for transmission of nosocomial pathogens. Clin. Infect. Dis., 39 (2): 219–226.

    Article  Google Scholar 

  • Du Y S, Yi M M, Xiao P, Meng L J, Li X, Sun G X, Liu Y. 2015. The impact of Aeromonas salmonicida infection on innate immune parameters of Atlantic salmon (Salmo salar L). Fish. Shellfish. Immun., 44 (1): 307–315.

    Article  Google Scholar 

  • Edgar R C, Haas B J, Clemente J C, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27 (16): 2194–2200.

    Article  Google Scholar 

  • Ewart K V, Belanger J C, Williams J, Karakach T, Penny S, Tsoi S C M, Richards R C, Douglas S E. 2005. Identification of genes differentially expressed in Atlantic salmon (Salmo salar) in response to infection by Aeromonas salmonicida using cDNA microarray technology. Dev. Comp. Immunol., 29 (4): 333–347.

    Article  Google Scholar 

  • Gill N, Wlodarska M, Finlay B. 2011. Roadblocks in the gut: barriers to enteric infection. Cell. Microbiol., 13 (5): 660–669.

    Article  Google Scholar 

  • Gill S R, Pop M, DeBoy R T, Eckburg P B, Turnbaugh P J, Samuel B S, Gordon J I, Relman D A, Fraser-Liggett C M, Nelson K E. 2006. Metagenomic analysis of the human distal gut microbiome. Science, 312 (5778): 1355–1359.

    Article  Google Scholar 

  • Giongo A, Gano K A, Crabb D B, Mukherjee N, Novelo L L, Casella G, Drew J C, Ilonen J, Knip M, Hyöty H, Veijola R, Simell T, Simell O, Neu J, Wasserfall C H, Schatz D, Atkinson M A, Triplett E W. 2011. Toward defining the autoimmune microbiome for type 1 diabetes. ISME J, 5 (1): 82–91.

    Article  Google Scholar 

  • Gómez G D, Balcázar J L. 2008. A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol. Med. Microbiol., 52 (2): 145–154.

    Article  Google Scholar 

  • Goodfellow M, Williams S T. 1983. Ecology of actinomycetes. Annu. Rev. Microbiol., 37: 189–216.

    Article  Google Scholar 

  • Gustafson C E, Thomas C J, Trust T J. 1992. Detection of Aeromonas salmonicida from fish by using polymerase chain reaction amplification of the virulence surface array protein gene. Appl. Environ. Microb iol., 58 (12): 3816–3825.

    Google Scholar 

  • Han S F, Liu Y C, Zhou Z G, He S X, Cao Y N, Shi P, Yao B, Ring Ö E. 2010. Analysis of bacterial diversity in the intestine of grass carp (Ctenopharyngodon idellus) based on 16S rDNA gene sequences. Aquac. Res., 42 (1): 47–56.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hooper L V, Littman D R, Macpherson A J. 2012. Interactions between the microbiota and the immune system. Science, 336 (6086): 1268–1273.

    Article  Google Scholar 

  • Hughes J B, Hellmann J J, Ricketts T H, Bohannan B J M. 2001. Counting the uncountable: statistical approaches to estimating microbial diversity. Appl. Environ. Microb iol., 67 (10): 4399–4406.

    Article  Google Scholar 

  • Janda J M, Abbott S L. 2010. The genus aeromonas: taxonomy, pathogenicity, and infection. Clin. Microbiol. Rev., 23 (1): 35–73.

    Article  Google Scholar 

  • Kim D H, Brunt J, Austin B. 2007. Microbial diversity of intestinal contents and mucus in rainbow trout (Oncorhynchus mykiss). J. Appl. Microbiol., 102 (6): 1654–1664.

    Article  Google Scholar 

  • Koskinen R, Ali-Vehmas T, Kämpfer P, Laurikkala M, Tsitko I, Kostyal E, Atroshi F, Salkinoja-Salonen M. 2000. Characterization of Sphingomonas isolates from Finnish and Swedish drinking water distribution systems. J. Appl. Microbiol., 89 (4): 687–696.

    Article  Google Scholar 

  • Levine J M, D'Antonio C M. 1999. Elton revisited: a review of evidence linking diversity and invasibility. Oikos, 87 (1): 15–26.

    Article  Google Scholar 

  • Li X M, Yu Y H, Feng W S, Yan Q Y, Gong Y C. 2012. Host species as a strong determinant of the intestinal microbiota of fish larvae. J. Microbiol., 50 (1): 29–37.

    Article  Google Scholar 

  • Li X M, Zhu Y J, Yan Q Y, Ringø E, Yang D G. 2014. Do the intestinal microbiotas differ between paddlefish (Polyodon spathala) and bighead carp (Aristichthys nobilis) reared in the same pond?. J. Appl. Microbiol., 117 (5): 1245–1252.

    Article  Google Scholar 

  • Llewellyn M S, McGinnity P, Dionne M, Letourneau J, Thonier F, Carvalho G R, Creer S, Derome N. 2015. The biogeography of the atlantic salmon (Salmo salar) gut microbiome. ISME J., 10 (5): 1280–1284.

    Article  Google Scholar 

  • Manichanh C, Borruel N, Casellas F, Guarner F. 2012. The gut microbiota in IBD. Nat. Rev. Gastroenterol. Hepatol., 9 (10): 599–608.

    Article  Google Scholar 

  • Navarrete P, Magne F, Mardones P, Riveros M, Opazo R, Suau A, Pochart P, Romero J. 2010. Molecular analysis of intestinal microbiota of rainbow trout (Oncorhynchus mykiss). FEMS Microbiol. Ecol., 71 (1): 148–156.

    Article  Google Scholar 

  • Nelson A M, Walk S T, Taube S, Taniuchi M, Houpt E R, Wobus C E, Young V B. 2012. Disruption of the human gut microbiota following Norovirus infection. PLoS One, 7 (10): e48224.

    Article  Google Scholar 

  • Ni J J, Yan Q Y, Yu Y H, Zhang T L. 2014. Factors influencing the grass carp gut microbiome and its effect on metabolism. FEMS Microbiol. Ecol., 87 (3): 704–714.

    Article  Google Scholar 

  • Ni J J, Yu Y H, Zhang T L, Gao L. 2012. Comparison of intestinal bacterial communities in grass carp, Ctenopharyngodon idellus, from two different habitats. Chin. J. Oceanol. Limn ol., 30 (5): 757–765.

    Article  Google Scholar 

  • Nicholson J K, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. 2012. Host-gut microbiota metabolic interactions. Science, 336 (6086): 1262–1267.

    Article  Google Scholar 

  • O'Hara A M, Shanahan F. 2006. The gut flora as a forgotten organ. EMBO Rep., 7 (7): 688–693.

    Article  Google Scholar 

  • Penn K, Jenkins C, Nett M, Udwary D W, Gontang E A, McGlinchey R P, Foster B, Lapidus A, Podell S, Allen E E, Moore B S, Jensen P R. 2009. Genomic islands link secondary metabolism to functional adaptation in marine Actinobacteria. ISME J., 3 (10): 1193–1203.

    Article  Google Scholar 

  • Peter H, Beier S, Bertilsson S, Lindström E S, Langenheder S, Tranvik L J. 2011. Function-specific response to depletion of microbial diversity. ISME J., 5 (2): 351–361.

    Article  Google Scholar 

  • Rawls J F, Samuel B S, Gordon J I. 2004. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc. Natl. Acad. Sci. U. S. A., 101 (13): 4596–4601.

    Article  Google Scholar 

  • Ray A K, Ghosh K, Ringø E. 2012. Enzyme-producing bacteria isolated from fish gut: a review. Aquacult. Nutr., 18 (5): 465–492.

    Article  Google Scholar 

  • Reveco F E, Øverland M, Romarheim O H, Mydland L T. 2014. Intestinal bacterial community structure differs between healthy and inflamed intestines in Atlantic salmon (Salmo salar L.). Aquaculture, 420-421: 262–269.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 (4): 422–430.

    Article  Google Scholar 

  • Round J L, Mazmanian S K. 2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol., 9 (5): 313–323.

    Article  Google Scholar 

  • Shin N R, Whon T W, Bae J W. 2015. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol., 33 (9): 496–503.

    Article  Google Scholar 

  • Sommer F, Bäckhed F. 2013. The gut microbiota—masters of host development and physiology. Nat. Rev. Microbiol., 11 (4): 227–238.

    Article  Google Scholar 

  • Sullam K E, Essinger S D, Lozupone C A, O'Connor M P, Rosen G L, Knight R, Kilham S, Russell J A. 2012. Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol. Ecol., 21 (13): 3363–3378.

    Article  Google Scholar 

  • Velmurugan S, John S T, Nagaraj D S, Ashine T A, Kumaran S, Pugazhvendan S. 2015. Isolation of actinomycetes from shrimp culture pond and antagonistic to pathogenic Vibrio spp. and WSSV. Int. J. Curr. Microbiol. App. Sci., 4 (7): 82–92.

    Google Scholar 

  • Verschuere L, Rombaut G, Sorgeloos P, Verstraete W. 2000. Probiotic bacteria as biological control agents in aquaculture. Microbiol. Mol. Biol. R., 64 (4): 655–671.

    Article  Google Scholar 

  • Wang L M, Zhao B, Li F S, Xu K, Ma C Q, Tao F, Li Q G, Xu P. 2011. Highly efficient production of D-lactate by Sporolactobacillus sp. CASD with simultaneous enzymatic hydrolysis of peanut meal. Appl. Microbiol. Biot., 89 (4): 1009–1017.

    Article  Google Scholar 

  • Wang T T, Cai G X, Qiu Y P, Fei N, Zhang M H, Pang X Y, Jia W, Cai S J, Zhao L P. 2012. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J., 6 (2): 320–329.

    Article  Google Scholar 

  • Willing B P, Russell S L, Finlay B. 2011. Shifting the balance: antibiotic effects on host-microbiota mutualism. Nat. Rev. Microbiol., 9 (4): 233–243.

    Article  Google Scholar 

  • Wolfensohn S, Lloyd M. 2008. Handbook of Laboratory Animal Management and Welfare. 3 rd edn. John Wiley & Sons, United Kingdom.

    Google Scholar 

  • Wu S G, Wang G T, Angert E R, Wang W W, Li W X, Zou H. 2012. Composition, diversity, and origin of the bacterial community in grass carp intestine. PLoS One, 7 (2): e30440.

    Article  Google Scholar 

  • Yan Q Y, van der Gast C J, Yu Y H. 2012. Bacterial community assembly and turnover within the intestines of developing zebrafish. PLoS One, 7 (1): e30603.

    Article  Google Scholar 

  • Zheng Y F, Yu M, Liu Y, Su Y, Xu T, Yu M C, Zhang X H. 2016. Comparison of cultivable bacterial communities associated with Pacific white shrimp (Litopenaeus vannamei) larvae at different health statuses and growth stages. Aquaculture, 451: 163–169.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ying Liu  (刘鹰).

Additional information

Supported by the National Natural Science Foundation of China (Nos. 31472312, 41306152, 31402283), the Qingdao Innovation Talents Program (No. 13-CX-16), the National Key Technology Research and Development Program of China (No. 2014BAD08B09), the Earmarked Fund for Modern Agroindustry Technology Research System (No. CARS-48), and the Project for International S&T Cooperation Program of China (No. 2014DFA31030)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, C., Sun, G., Li, S. et al. Intestinal microbiota of healthy and unhealthy Atlantic salmon Salmo salar L. in a recirculating aquaculture system. J. Ocean. Limnol. 36, 414–426 (2018). https://doi.org/10.1007/s00343-017-6203-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-017-6203-5

Keyword

Navigation