Skip to main content
Log in

Characterization of the bacterial communities associated with biofilters in two full-scale recirculating aquaculture systems

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

Abstract

Bacteria play a major role in metabolizing ammonia and other metabolites in recirculating aquaculture systems (RASs). To characterize and compare the bacterial communities in the biofilters of two full-scale RASs for the culture of puffer fish, Takifugu rubripes, at different ages and densities were studied. In overall, 47 807 optimized reads of the 16S rRNA gene with V4–V5 region were obtained from four biofilm samples collected after biofilm maturation. At 97% cut-off level, these sequences were clustered into 500 operational taxonomic units, and were classified into 19 bacterial phyla and 138 genera. At the phylum level, Proteobacteria and Bacteroidetes were the most abundant, followed by Nitrospirae and Planctomycetes. At the genus level, Colwellia, Marinifilum, Oceanospirillum, Lutibacter, Winogradskyella, Pseudoalteromonas, Arcobacter, and Phaeobacter were the top members. Nitrosomonas and Nitrospira were main ammonia- and nitrite-oxidizing bacteria. Differences in bacterial communities at different sampling dates and similarities of both biofilters were revealed in the Venn diagram and cluster analysis. Maintaining a good water quality and health of farmed fish in RASs depended on the correct management of the bacterial communities. This study provides more accurate information on the bacterial communities associated with the bifilters of both RASs.

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.

Institutional subscriptions

Similar content being viewed by others

Data Availability Statement

All data generated and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Blancheton J P, Attramadal K L K, Michaud L, d’Orbcastel E R, Vadstein O. 2013. Insight into bacterial population in aquaculture systems and its implication. Aquacultural Engineering, 53: 30–39, https://doi.org/10.1016/j.aquaeng.2012.11.009.

    Article  Google Scholar 

  • Caporaso J G, Lauber C L, Walters W A, Berg-Lyons D, Huntley J, Fierer N, Owens S M, Betley J, Fraser L, Bauer M, Gormley N, Gilbert J A, Smith G, Knight R. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal, 6(8): 1 621–1 624, https://doi.org/10.1038/ismej.2012.8.

    Article  Google Scholar 

  • Chen Z, Liu Y, Liu L Z, Wang X J, Liu Z P, Liu Y 2013. Heterotrophic bacterial community structure of multistage biofilters in a commercial pufferfish Takifugu rubripes RAS. Advanced Materials Research, 726–731: 1 621–1 627, https://doi.org/10.4028/www.scientific.net/AMR.726-731.1621.

    Article  Google Scholar 

  • Foesel B U, Gieseke A, Schwermer C, Stief P, Koch L, Cytryn E, De La Torré J R, Van Rijn J, Minz D, Drake H L, Schramm A. 2008. Nitrosomonas Nm143-like ammonia oxidizers and Nitrospira marina-like nitrite oxidizers dominate the nitrifier community in a marine aquaculture biofilm. FEMS Microbiology Ecology, 63(2): 192–204, https://doi.org/10.1111/j.1574-6941.2007.00418.x.

    Article  Google Scholar 

  • Haaijer S C M, Ji K, Van Niftrik L, Hoischen A, Speth D, Jetten M S M, Damsté J S S, Op den Camp H J M. 2013. A novel marine nitrite-oxidizing Nitrospira species from Dutch coastal North Sea water. Frontiers in Microbiology, 4: 60, https://doi.org/10.3389/fmicb.2013.00060.

    Article  Google Scholar 

  • Huang Z T, Wan R, Song X F, Liu Y, Hallerman E, Dong D P, Zhai J M, Zhang H S, Sun L Y. 2016. Metagenomic analysis shows diverse, distinct bacterial communities in biofilters among different marine recirculating aquaculture systems. Aquaculture International, 24(5): 1 393–1 408, https://doi.org/10.1007/s10499-016-9997-9.

    Article  Google Scholar 

  • Itoi S, Niki A, Sugita H. 2006. Changes in microbial communities associated with the conditioning of filter material in recirculating aquaculture systems of the pufferfish Takifugu rubripes. Aquaculture, 256(1–4): 287–295, https://doi.org/10.1016/j.aquaculture.2006.02.037.

    Article  Google Scholar 

  • Kersters K, De Vos P, Gillis M, Swings J, Vandamme P, Stackebrandt E. 2006. Introduction to the Proteobacteria. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K H, Stackebrandt E eds. The Prokaryotes: A Handbook on the Biology of Bacteria. Springer, New York. p.3–37.

    Chapter  Google Scholar 

  • Keuter S, Beth S, Quantz G, Schulz C, Spieck E. 2017. Longterm monitoring of nitrification and nitrifying communities during biofilter activation of two marine recirculation aquaculture systems (RAS). International Journal of Aquaculture and Fishery Sciences, 3(3): 51–61, https://doi.org/10.17352/2455-8400.000029.

    Google Scholar 

  • Kirchman D L. 2002. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiology Ecology, 39(2): 91–100, https://doi.org/10.1111/j.1574-6941.2002.tb00910.x.

    Google Scholar 

  • Léonard N, Guiraud J P, Gasset E, Cailleres J P, Blancheton J P. 2002. Bacteria and nutrients—nitrogen and carbon—in a recirculating system for sea bass production. Aquacultural Engineering, 26(2): 111–127.

    Article  Google Scholar 

  • Li Y Y, Zhang T, Zhang C Y, Zhu Y, Ding J F, Ma Y X. 2015. Bacterial diversity in the intestine of young farmed puffer fish Takifugu rubripes. Chinese Journal of Oceanology and Limnology, 33(4): 913–918, https://doi.org/10.1007/s00343-015-4219-2.

    Article  Google Scholar 

  • Lin Z L, Wang H, Yu C Y, Lv F H, Liu H M, Zhang T. 2017. Commercial production of tiger puffer (Takifugu rubripes) in winter using a recirculating aquaculture system. Journal of Ocean University of China, 16(1): 107–113, https://doi.org/10.1007/s11802-017-2802-1.

    Article  Google Scholar 

  • Ma Y X, Li M, Sun J X, Hao Z L, Liang J, Zhao X W. 2019. Characterization of bacterial community associated with four organs of the Yesso scallop (Patinopecten yessoensis) by high-throughput sequencing. Journal of Ocean University of China, 18(2): 493–500, https://doi.org/10.1007/s11802-019-3791-z.

    Article  Google Scholar 

  • Martins C I M, Eding E H, Verdegem M C J, Heinsbroek L T N, Schneider O, Blancheton J P, d’Orbcastel E R, Verreth J A J. 2010. New developments in recirculating aquaculture systems in Europe: a perspective on environmental sustainability. Aquacultural Engineering, 43(3): 83–93, https://doi.org/10.1016/j.aquaeng.2010.09.002.

    Article  Google Scholar 

  • Metzker M L. 2010. Sequencing technologies—the next generation. Nature Reviews Genetics, 11(1): 31–46, https://doi.org/10.1038/nrg2626.

    Article  Google Scholar 

  • Michaud L, Blancheton J P, Bruni V, Piedrahita R. 2006. Effect of particulate organic carbon on heterotrophic bacterial populations and nitrification efficiency in biological filters. Aquacultural Engineering, 34(3): 224–233, https://doi.org/10.1016/j.aquaeng.2005.07.005.

    Article  Google Scholar 

  • Michaud L, Lo Giudice A, Troussellier M, Smedile F, Bruni V, Blancheton J P. 2009. Phylogenetic characterization of the heterotrophic bacterial communities inhabiting a marine recirculating aquaculture system. Journal of Applied Microbiology, 107(6): 1 935–1 946, https://doi.org/10.1111/j.1365-2672.2009.04378.x.

    Article  Google Scholar 

  • Pot B, Gillis M. 2015. Oceanospirillum. John Wiley and Sons, Inc., New York, https://doi.org/10.1002/9781118960608.gbm01196.

    Book  Google Scholar 

  • Ruan Y J, Guo X S, Ye Z Y, Liu Y, Zhu S M. 2015. Bacterial community analysis of different sections of a biofilter in a full-scale marine recirculating aquaculture system. North American Journal of Aquaculture, 77(3): 318–326, https://doi.org/10.1080/15222055.2015.1017128.

    Article  Google Scholar 

  • Rud I, Kolarevic J, Holan A B, Berget I, Calabrese S, Terjesen B F. 2017. Deep-sequencing of the bacterial microbiota in commercial-scale recirculating and semi-closed aquaculture systems for Atlantic salmon post-smolt production. Aquacultural Engineering, 78: 50–62, https://doi.org/10.1016/j.aquaeng.2016.10.003.

    Article  Google Scholar 

  • Rurangwa E, Verdegem M C J. 2015. Microorganisms in recirculating aquaculture systems and their management. Reviews in Aquaculture, 7(2): 117–130, https://doi.org/10.1111/raq.12057.

    Article  Google Scholar 

  • Sakami T, Andoh T, Morita T, Yamamoto Y. 2012. Phylogenetic diversity of ammonia-oxidizing archaea and bacteria in biofilters of recirculating aquaculture systems. Marine Genomics, 7(9): 27–31, https://doi.org/10.1016/j.margen.2012.04.006.

    Article  Google Scholar 

  • Satomi M, Kimura B, Hamada T, Harayama S, Fujii T. 2002. Phylogenetic study of the genus Oceanospirillum based on 16S rRNA and gyrB genes: emended description of the genus Oceanospirillum, description of Pseudospirillum gen. nov., Oceanobacter gen. nov. and Terasakiella gen. nov. and transfer of Oceanospirillum jannaschii and Pseudomonas stanieri to Marinobacterium as Marinobacterium jannaschii comb. nov. and Marinobacterium stanieri comb. no. International Journal of Systematic and Evolutionary Microbiology, 52(3): 739–747, https://doi.org/10.1099/ijs.0.01427-0.

    Google Scholar 

  • Schreier H J, Mirzoyan N, Saito K. 2010. Microbial diversity of biological filters in recirculating aquaculture systems. Current Opinion in Biotechnology, 21(3): 318–325, https://doi.org/10.1016/jxopbio.2010.03.011.

    Article  Google Scholar 

  • Sun X Y, Liu J C, Li M, Zhao X W, Liang J, Sun P H, Ma Y X. 2016. Characterization of bacterial communities associating with larval development of Yesso scallop (Patinopecten yessoensis Jay, 1857) by high-throughput sequencing. Journal of Ocean University of China, 15(6): 1 067–1 072, https://doi.org/10.1007/s11802-016-3092-8.

    Article  Google Scholar 

  • Tal Y, Watts J E M, Schreier H J. 2006. Anaerobic ammonium-oxidizing (anammox) bacteria and associated activity in fixed-film biofilters of a marine recirculating aquaculture system. Applied and Environmental Microbiology, 72(4): 2 896–2 904, https://doi.org/10.1128/AEM.72.4.2896-2904.2006.

    Article  Google Scholar 

  • Tal Y, Watts J E M, Schreier S B, Sowers K R, Schreier H J. 2003. Characterization of the microbial community and nitrogen transformation processes associated with moving bed bioreactors in a closed recirculated mariculture system. Aquaculture, 215(1–4): 187–202, https://doi.org/10.1016/S0044-8486(02)00372-1.

    Article  Google Scholar 

  • Turner S N, Pryer K M, Miao V P W, Palmer J D. 1999. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. The Journal of Eukaryotic Microbiology, 46(4): 327–338, https://doi.org/10.1111/j.1550-7408.1999.tb04612.x.

    Article  Google Scholar 

  • van de Graaf AA, Mulder A, de Bruijn P, Jetten M S, Robertson L A, Kuenen J G. 1995. Anaerobic oxidation of ammonium is a biologically mediated process. Applied and Environmental Microbiology, 61(4): 1 246–1 251.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yuexin Ma.

Additional information

Supported by the National Key R&D Program of China (No. 2017YFD0701700) and National Natural Science Foundation of China (Nos. 31472312, 31672673)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, Y., Du, X., Liu, Y. et al. Characterization of the bacterial communities associated with biofilters in two full-scale recirculating aquaculture systems. J. Ocean. Limnol. 39, 1143–1150 (2021). https://doi.org/10.1007/s00343-020-0120-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-020-0120-8

Keyword

Navigation