Effects of solid-phase denitrification on the nitrate removal and bacterial community structure in recirculating aquaculture system
- 597 Downloads
- 8 Citations
Abstract
A solid-phase denitrification (SPD) reactor packed with poly (3-hydroxybutyrate-co-3-hydroxyvalerate) as a carbon source was incorporated into a recirculating aquaculture system (RAS) to remove accumulated nitrate. Bacterial community structures in different parts of the RAS, including biofilter unit, SPD reactor, and culture water, were analyzed using Illumina MiSeq sequencing technology. The data showed that nitrate levels decreased remarkably in the RAS connected with SPD reactor (RAS-DR). In contrast, nitrate levels increased continuously in the conventional RAS without SPD reactor (RAS-CK). Biofilter unit and culture water in RAS-DR developed lower species richness and higher bacterial community diversity than that in RAS-CK. The bacterial community structure of RAS was significantly affected by the SPD process and the changes included an increase in the proportion of Proteobacteria and Firmicutes and a decrease in Nitrospira abundance in RAS-DR. Firmicutes was the most abundant phylum (56.9 %) and mainly consisted of Clostridium sensu stricto (48.3 %) in SPD reactor.
Keywords
Nitrate Solid-phase denitrification Microbial community Recirculating aquaculture system Illumina MiSeq sequencingNotes
Acknowledgments
The authors are grateful for the financial support offered by the National Natural Science Foundation of China (Grant No. 21077014), Beijing Natural Science Foundation (Grant No. 8152016), and the Special Program for Creative Ability and Youth Science Foundation of Beijing Academy of Agriculture and Forestry Sciences (Grant No. KJCX 20140420, QNJJ 201417).
References
- Abou-Zeid DM, Müller RJ, Deckwer WD (2001) Degradation of natural and synthetic polyesters under anaerobic conditions. J Biotechnol 86(2):113–126. doi: 10.1016/S0168-1656(00)00406-5 CrossRefPubMedGoogle Scholar
- Attramadal KJK, Truong TMH, Bakke I, Skjermo J, Olsen Y, Vadstein O (2014) RAS and microbial maturation as tools for K-selection of microbial communities improve survival in cod larvae. Aquaculture 432:483–490. doi: 10.1016/j.aquaculture.2014.05.052 CrossRefGoogle Scholar
- Blancheton JP, Attramadal KJK, Michaud L, Roque d’Orbcastele E, Vadstein O (2013) Insight into bacterial population in aquaculture systems and its implication. Aquac Eng 53:30–39. doi: 10.1016/j.aquaeng.2012.11.009 CrossRefGoogle Scholar
- Boley A, Müller WR, Haider G (2000) Biodegradable polymers as solid substrate and biofilm carrier for denitrification in recirculated aquaculture systems. Aquac Eng 22:75–85. doi: 10.1016/S0144-8609(00)00033-9 CrossRefGoogle Scholar
- Chen L, Wang LY, Liu SY, Hu JY, He Y, Zhou HW, Zhang XH (2013) Profiling of microbial community during in situ remediation of volatile sulfide compounds in river sediment with nitrate by high throughput sequencing. Int Biodeter Biodegr 85:429–437. doi: 10.1016/j.ibiod.2013.08.015 CrossRefGoogle Scholar
- Chu LB, Wang JL (2013) Denitrification performance and biofilm characteristics using biodegradable polymers PCL as carriers and carbon source. Chemosphere 91(9):1310–1316. doi: 10.1016/j.chemosphere.2013.02.064 CrossRefPubMedGoogle Scholar
- Cochlan WP, Herndon J, Kudelan RM (2008) Inorganic and organic nitrogen uptake by the toxigenic diatom Pseudo-nitzschia australis (Bacillariophyceae). Harmful Algae 8(1):111–118. doi: 10.1016/j.hal.2008.08.008 CrossRefGoogle Scholar
- Colwell RK, Chao A, Gotelli NJ, Lin SY, Mao CX, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5(1):3–21. doi: 10.1093/jpe/rtr044 CrossRefGoogle Scholar
- Davidson J, Good C, Welsh C, Summerfelt ST (2014) Comparing the effects of high vs. low nitrate on the health, performance, and welfare of juvenile rainbow trout Oncorhynchus mykiss within water recirculating aquaculture systems. Aquac Eng 59:30–40. doi: 10.1016/j.aquaeng.2014.01.003 CrossRefGoogle Scholar
- Eding EH, Kamstra A, Verreth JAJ, Huisman EA, Klapwijk A (2006) Design and operation of nitrifying trickling filters in recirculating aquaculture: a review. Aquac Eng 34(3):234–260. doi: 10.1016/j.aquaeng.2005.09.007 CrossRefGoogle Scholar
- FAO, The State of World Fisheries and Aquaculture. (2014) Food and agriculture organization of the United Nations, Rome. http://www.fao.org/3/a-i3720e/index.html
- Gauger E, Smolowitz R, Uhlinger K, Casey J, Gómez-Chiarri M (2006) Vibrio harveyi and other bacterial pathogens in cultured summer flounder, Paralichthys dentatus. Aquaculture 260(1–4):10–20. doi: 10.1016/j.aquaculture.2006.06.012 CrossRefGoogle Scholar
- Gutierrez-Wing MT, Malone RF, Rusch KA (2012) Evaluation of polyhydroxybutyrate as a carbon source for recirculating aquaculture water denitrification. Aquac Eng 51:36–43. doi: 10.1016/j.aquaeng.2012.07.002 CrossRefGoogle Scholar
- Hamlin HJ, Michaels JT, Beaulaton CM, Graham WF, Dutt W, Steinbach P, Losordo TM, Schrader KK, Main KL (2008) Comparing denitrification rates and carbon sources in commercial scale upflow denitrification biological filters in aquaculture. Aquac Eng 38(2):79–92. doi: 10.1016/j.aquaeng.2007.11.003 CrossRefGoogle Scholar
- Hovanec TA, Taylor LT, Blakis A, Delong EF (1998) Nitrospira-Like bacteria associated with nitrite oxidation in freshwater aquaria. Appl Environ Microbiol 64(1):258–264PubMedPubMedCentralGoogle Scholar
- Itoi S, Ebihara N, Washio S, Sugita H (2007) Nitrite-oxidizing bacteria, Nitrospira, distribution in the outer layer of the biofilm from filter materials of a recirculating water system for the goldfish Carassius auratus. Aquaculture 264(1–4):297–308. doi: 10.1016/j.aquaculture.2007.01.007 CrossRefGoogle Scholar
- Kamstra A, van der Heul JW (1998) Aquaculture and water: fish culture, shellfish culture and water usage. European Aquaculture Society Special Publication, Oostende, pp 128–129Google Scholar
- Kaviraj A, Bhunia F, Saha NC (2004) Toxicity of methanol to fish, crustacean, oligochaete worm, and aquatic ecosystem. Int J Toxicol 23(1):55–63CrossRefPubMedGoogle Scholar
- Khan ST, Horiba Y, Yamamoto M, Hiraishi A (2002) Members of the Family Comamonadaceae as primary poly(3-Hydroxybutyrate-co-3-Hydroxyvalerate)-degrading denitrifiers in activated sludge as revealed by a polyphasic approach. Appl Environ Microbiol 68(7):3206–3214CrossRefPubMedPubMedCentralGoogle Scholar
- Khan ST, Horiba Y, Takahashi N, Hiraishi A (2007) Activity and community composition of denitrifying bacteria in poly(3-hydroxybutyrate-co-3-hdroxyvalerate)-using solid-phase denitrification processes. Microbes Environ 22(1):20–31CrossRefGoogle Scholar
- Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-Index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79(17):5112–5120CrossRefPubMedPubMedCentralGoogle Scholar
- Lee PG, Lea RN, Dohmann E, Prebilsky W, Turk PE, Ying H, Whitson JL (2000) Denitrification in aquaculture systems: an example of a fuzzy logic control problem. Aquac Eng 23(1–3):37–59. doi: 10.1016/S0144-8609(00)00046-7 CrossRefGoogle Scholar
- Lee HW, Lee SY, Lee JW, Park JB, Choi ES, Park YK (2002) Molecular characterization of microbial community in nitrate-removing activated sludge. FEMS Microbiol Ecol 41:85–94. doi: 10.1016/S0168-6496(02)00289-1 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- Martins P, Cleary DFR, Pires ACC, Rodrigues AM, Quintino V, Calado R, Gomes NCM (2013) Molecular analysis of bacterial communities and detection of potential pathogens in a recirculating aquaculture system for Scophthalmus maximus and Solea senegalensis. PLoS ONE 8(11):e80847. doi: 10.1371/journal.pone.0080847 CrossRefPubMedPubMedCentralGoogle Scholar
- Mergaert J, Boley A, Cnockaert MC, Muller WR, Swings J (2001) Identity and potential functions of heterotrophic bacterial isolates from a continuous-upflow fixed-bed reactor for denitrification of drinking water with bacterial polyester as source of carbon and electron donor. Syst Appl Microbiol 24(2):303–310. doi: 10.1078/0723-2020-00037 CrossRefPubMedGoogle Scholar
- Meske C (1976) Fish culture in a recirculating system with water treatment by activated sludge. In: Pillay TVR, Dill WA (eds) Advances in Aquaculture. Fishing News Ltd, Farnham, pp 527–531Google Scholar
- Michaud L, Blancheton JP, Bruni V, Piedrahita R (2006) Effect of particulate organic carbon on heterotrophic bacterial populations and nitrification efficiency in biological filters. Aquac Eng 34(3):224–233. doi: 10.1016/j.aquaeng.2005.07.005 CrossRefGoogle Scholar
- Michaud L, Giudice AL, Interdonato F, Triplet S, Ying L, Blancheton JP (2014) C/N ratio-induced structural shift of bacterial communities inside lab-scale aquaculture biofilters. Aquac Eng 58:77–87. doi: 10.1016/j.aquaeng.2013.11.002 CrossRefGoogle Scholar
- Oh J, Silverstein J (1999) Acetate limitation and nitrite accumulation during denitrification. J Environ Eng 125(3):234–242CrossRefGoogle Scholar
- Ovez B, Ozgen S, Yuksel M (2006) Biological denitrification in drinking water using Glycyrrhiza glabra and Arunda donax as the carbon source. Process Biochem 41(7):1539–1544. doi: 10.1016/j.procbio.2006.02.015 CrossRefGoogle Scholar
- Rurangwa E, Verdegem MCJ (2014) Microorganisms in recirculating aquaculture systems and their management. Rev Aquacult 5:1–14. doi: 10.1111/raq.12057 Google Scholar
- Saito T, Saegusa H, Miyata Y, Fukui T (1992) Intracellular degradation of poly(3-hydroxybutyrate) granules of Zoogloea ramigera I-16-M. FEMS Microbiol Rev 103:333–338. doi: 10.1016/0378-1097(92)90327-K CrossRefGoogle Scholar
- Schloe K, Gillis M, Hoste B, Pot B, Vancanneyt M, Mergaert J, Swings J, Biedermann J, Süssmuth R (2000) Polyphasic characterization of poly-3-hydroxybutyrate-co-3-hydroxyvalerate (P(HB-co-HV)) metabolizing and denitrifying Acidovorax sp. strains. Syst Appl Microbiol 23(3):364–372. doi: 10.1016/S0723-2020(00)80066-1 CrossRefPubMedGoogle Scholar
- Schneider O, Chabrillon-Popelka M, Smidt H, Haenen O, Sereti V, Eding EH, Verreth JAJ (2007) HRT and nutrients affect bacterial communities grown on recirculation aquaculture system effluents. FEMS Microbiol Ecol 60(2):207–219. doi: 10.1111/j.1574-6941.2007.00282.x CrossRefPubMedGoogle Scholar
- Schreier HJ, Mirzoyan N, Saito K (2010) Microbial diversity of biological filters in recirculating aquaculture systems. Curr Opin Biotech 21(3):318–325. doi: 10.1016/j.copbio.2010.03.011 CrossRefPubMedGoogle Scholar
- SEPAC (State Environmental Protection Administration of China), (2002) Monitoring and analysis methods of water and wastewater, 4th edn. China Environmental Science Press, BeijingGoogle Scholar
- Shao MF, Zhang T, Fang HHP, Li X (2011) The effect of nitrate concentration on sulfide-driven autotrophic denitrification in marine sediment. Chemosphere 83(1):1–6. doi: 10.1016/j.chemosphere.2011.01.042 CrossRefPubMedGoogle Scholar
- Shen Z, Zhou Y, Hu J, Wang J (2013a) Denitrification performance and microbial diversity in a packed-bed bioreactor using biodegradable polymer as carbon source and biofilm support. J Hazard Mater 250–251:431–438. doi: 10.1016/j.jhazmat.2013.02.026 CrossRefPubMedGoogle Scholar
- Shen Z, Zhou Y, Wang J (2013b) Comparison of denitrification performance and microbial diversity using starch/polylactic acid blends and ethanol as electron donor for nitrate removal. Bioresour Technol 131:33–39. doi: 10.1016/j.biortech.2012.12.169 CrossRefPubMedGoogle Scholar
- Singer A, Parnes S, Gross A, Sagi A, Brenner A (2008) A novel approach to denitrification processes in a zero-discharge recirculating system for small-scale urban aquaculture. Aquac Eng 39(2–3):72–77CrossRefGoogle Scholar
- Sugita H, Nakamura H, Shimada T (2005) Microbial communities associated with filter materials in recirculating aquaculture systems of freshwater fish. Aquaculture 243(1–4):403–409. doi: 10.1016/j.aquaeng.2008.07.001 CrossRefGoogle Scholar
- Süssmuth R (2000) Polyphasic characterization of poly-3-hydroxybutyrate-co-3-hydroxyvalerate (P(HB-co-HV)) metabolizing and denitrifying Acidovorax sp. strains. Syst Appl Microbiol 23(3):364–372. doi: 10.1016/S0723-2020(00)80066-1 CrossRefPubMedGoogle Scholar
- Takahashi M, Yamada T, Tanno M, Tsuji H, Hiraishi A (2011) Nitrate removal efficiency and bacterial community dynamics in denitrification processes using poly (L-lactic acid) as the solid substrate. Microbes Environ 26(3):212–219CrossRefPubMedGoogle Scholar
- Takeda M, Matsuoka H, Hamana H, Hikuma M (1995) Biosynthesis of poly-3-hydroxybutyrate by Sphaerotilus natans. Appl Microbiol Biotechnol 43(1):31–34. doi: 10.1007/BF00170618 CrossRefGoogle Scholar
- Talaat AM, Reimschuessel R, Wasserman SS, Trucksis M (1998) Goldfish, Carassius auratus, a novel animal model for the study of Mycobacterium marinum pathogenesis. Infect Immun 66(6):2938–2942PubMedPubMedCentralGoogle Scholar
- Trois C, Pisano G, Oxarango L (2010) Alternative solutions for the bio-denitrification of landfill leachates using pine bark and compost. J Hazard Mater 178(1–3):1100–1105. doi: 10.1016/j.jhazmat.2010.01.054 CrossRefPubMedGoogle Scholar
- Van Kessel M, Dutilh BE, Neveling K, Kwint MP, Veltman JA, Flik G, Jetten MS, Klaren PH, den Camp HJO (2011) Pyrosequencing of 16S rRNA gene amplicons to study the microbiota in the gastrointestinal tract of carp (Cyprinus carpio L.). AMB Express 1(1):41. doi: 10.1186/2191-0855-1-41 CrossRefPubMedPubMedCentralGoogle Scholar
- Van Rijn J, Tal Y, Schreier HJ (2006) Denitrification in recirculating systems: theory and applications. Aquac Eng 34(3):364–376. doi: 10.1016/j.aquaeng.2005.04.004 CrossRefGoogle Scholar
- Wang XM, Wang JL (2013) Nitrate removal from groundwater using solid-phase denitrification process without inoculating with external microorganisms. Int J Environ Sci Technol 10:955–960. doi: 10.1007/s13762-013-0236-x CrossRefGoogle Scholar
- Wang XM, Xing LJ, Qiu TL, Han ML (2013) Simultaneous removal of nitrate and pentachlorophenol from simulated groundwater using a biodenitrification reactor packed with corncob. Environ Sci Pollut R 20(4):2236–2244. doi: 10.1007/s11356-012-1092-9 CrossRefGoogle Scholar
- Wrighton KC, Virdis B, Clauwaert P, Read ST, Daly RA, Boon N, Piceno Y, Andersen GL, Coates JD, Rabaey K (2010) Bacterial community structure corresponds to performance during cathodic nitrate reduction. ISME J 4(11):1443–1455. doi: 10.1038/ismej.2010.66 CrossRefPubMedGoogle Scholar
- Wu SG, Tian JY, Gatesoupe FJ, Li WX, Zou H, Yang BJ, Wang GT (2013a) Intestinal microbiota of gibel carp (Carassius auratus gibelio) and its origin as revealed by 454 pyrosequencing. World J Microbiol Biotechnol 29(9):1585–1595. doi: 10.1007/s11274-013-1322-4 CrossRefPubMedGoogle Scholar
- Wu WZ, Yang LH, Wang JL (2013b) Denitrification performance and microbial diversity in a packed-bed bioreactor using PCL as carbon source and biofilm carrier. Appl Microbiol Biot 97(6):2725–2733. doi: 10.1007/s00253-012-4110-4 CrossRefGoogle Scholar