Intestinal microbiota of healthy and unhealthy Atlantic salmon <i>Salmo salar</i> L. in a recirculating aquaculture system -- Journal of Oceanology and Limnology,2018,36(2):414-426

	Cite this paper:
	WANG Chun, SUN Guoxiang, LI Shuangshuang, LI Xian, LIU Ying. Intestinal microbiota of healthy and unhealthy Atlantic salmon Salmo salar L. in a recirculating aquaculture system[J]. Journal of Oceanology and Limnology, 2018, 36(2): 414-426

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

WANG Chun^1,2, SUN Guoxiang¹, LI Shuangshuang³, LI Xian¹, LIU Ying¹

1 Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 University of Chinese Academy of Sciences, Beijing 100049, China;
3 College of Energy and Environmental Engineering, Hebei University of Engineering, Handan 056038, China

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.

Key words: intestinal microbiota|health status|Atlantic salmon (Salmo salar L.)|recirculating aquaculture system|high-throughput pyrosequencing

Received: 2016-08-01 Revised:

Tools

PDF (589 KB) Free

Print this page

Add to favorites

Email this article to others

Authors

Articles by WANG Chun

Articles by SUN Guoxiang

Articles by LI Shuangshuang

Articles by LI Xian

Articles by LIU Ying

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):15 718-15 723.
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.
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.
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.
Blumberg R, Powrie F. 2012. Microbiota, disease, and back to health:a metastable journey. Sci. Transl. Med., 4(137):137rv7.
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.
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.
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.
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.
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.
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.
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):5 069-5 072.
Dharmaraj S. 2011. Antagonistic potential of marine actinobacteria against fish and shellfish pathogens. Turk.J. Biol., 35(3):303-311.
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.
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.
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):2 194-2 200.
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.
Gill N, Wlodarska M, Finlay B. 2011. Roadblocks in the gut:barriers to enteric infection. Cell. Microbiol., 13(5):660-669.
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):1 355-1 359.
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.
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.
Goodfellow M, Williams S T. 1983. Ecology of actinomycetes.Annu. Rev. Microbiol., 37:189-216.
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. Microbiol., 58(12):3 816-3 825.
Han S F, Liu Y C, Zhou Z G, He S X, Cao Y N, Shi P, Yao B, RingÖ 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.
Hansen G H, Olafsen J A. 1999. Bacterial interactions in early life stages of marine cold water fish. Microb. Ecol., 38(1):1-26.
Hooper L V, Littman D R, Macpherson A J. 2012. Interactions between the microbiota and the immune system. Science, 336(6086):1 268-1 273.
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. Microbiol., 67(10):4 399-4 406.
Janda J M, Abbott S L. 2010. The genus aeromonas:taxonomy, pathogenicity, and infection. Clin. Microbiol. Rev., 23(1):35-73.
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):1 654-1 664.
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.
Levine J M, D'Antonio C M. 1999. Elton revisited:a review of evidence linking diversity and invasibility. Oikos, 87(1):15-26.
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.
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):1 245-1 252.
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):1 280-1 284.
Manichanh C, Borruel N, Casellas F, Guarner F. 2012. The gut microbiota in IBD. Nat. Rev. Gastroenterol. Hepatol., 9(10):599-608.
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.
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.
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.
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. Limnol., 30(5):757-765.
Nicholson J K, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. 2012. Host-gut microbiota metabolic interactions. Science, 336(6086):1 262-1 267.
O'Hara A M, Shanahan F. 2006. The gut flora as a forgotten organ. EMBO Rep., 7(7):688-693.
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):1 193-1 203.
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.
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):4 596-4 601.
Ray A K, Ghosh K, Ringø E. 2012. Enzyme-producing bacteria isolated from fish gut:a review. Aquacult. Nutr., 18(5):465-492.
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.
Ringø E, Birkbeck T H. 1999. Intestinal microflora of fish larvae and fry. Aquac. Res., 30(2):73-93.
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.
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.
Shin N R, Whon T W, Bae J W. 2015. Proteobacteria:microbial signature of dysbiosis in gut microbiota. Trends Biotechnol., 33(9):496-503.
Sommer F, Bäckhed F. 2013. The gut microbiota-masters of host development and physiology. Nat. Rev. Microbiol., 11(4):227-238.
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):3 363-3 378.
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.
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.
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):1 009-1 017.
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.
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.
Wolfensohn S, Lloyd M. 2008. Handbook of Laboratory Animal Management and Welfare. 3rd edn. John Wiley & Sons, United Kingdom.
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.
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.
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.