Skip to main content
SpringerLink
Log in

Environmental impacts of antibiotics addition to algal-bacterial-based aquaponic system

  • Environmental Biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Antibiotics usage is a double-edged sword among the production promotion and environmental aggravation of aquaculture system. In this study, the effects of sulfadiazine addition on algal-bacterial-based aquaponic (AA) system were thoroughly investigated. Results showed that sulfadiazine addition increased the nitrogen (N) and carbon (C) recovery of AA system by 1.3 times and 2.9 times, respectively. Meanwhile, the global warming potential was increased by 63% due to aggravated nitrous oxide (N2O) emission. This was mainly because sulfadiazine increased the abundance of nirS genes and decreased the abundance of nosZ genes, which subsequently led to higher N2O accumulation. Furthermore, resistance gene (sul-1, sul-2, and intI-1) abundance in the treatment group was an order higher than that of the control group, which would give rise to the environmental risk for agroecological system.

Key Points

• Sulfadiazine addition increased NUE at expense of aggravated GHG emissions.

• Sulfadiazine disrupted the balance between the abundance of nirS and nosZ genes.

• Sulfadiazine addition increased the resistance gene abundance of AA system.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article.

References

  • Anbalagan A, Schwede S, Lindberg C, Nehrenheim E (2016) Influence of hydraulic retention time on indigenous microalgae and activated sludge process. Water Res 91:277–284

    Article  CAS  Google Scholar 

  • APHA (2012) Standard methods for the examination of water and wastewater, twenty-first ed. American Public Health Association, Washington, DC

  • Baeza C, Knappe DRU (2011) Transformation kinetics of biochemically active compounds in low-pressure UV photolysis and UV/H2O2 advanced oxidation processes. Water Res 45(15):4531–4543

    Article  CAS  Google Scholar 

  • Cai T, Park SY, Li Y (2013) Nutrient recovery from wastewater streams by microalgae: status and prospects. Renew Sustain Energy Rev 19:360–369

    Article  CAS  Google Scholar 

  • Fang Y, Chen X, Hu Z, Liu D, Gao H, Nie L (2018) Effects of hydraulic retention time on the performance of algal-bacterial-based aquaponics (AA): focusing on nitrogen and oxygen distribution. Appl Microbiol Biot 102(22):9843–9855

    Article  CAS  Google Scholar 

  • Fang Y, Hu Z, Zou Y, Fan J, Wang Q, Zhu Z (2017) Increasing economic and environmental benefits of media-based aquaponics through optimizing aeration pattern. J Clean Prod 162:1111–1117

    Article  CAS  Google Scholar 

  • Fang Y, Hu Z, Zou Y, Zhang J, Zhu Z, Zhang J, Nie L (2017b) Improving nitrogen utilization efficiency of aquaponics by introducing algal-bacterial consortia. Bioresour Technol 245(A):358–364

  • Fedorova G, Grabic R, Grabicova K, Turek J, Van Nguyen T, Randak T, Brooks BW, Zlabek V (2022) Water reuse for aquaculture: comparative removal efficacy and aquatic hazard reduction of pharmaceuticals by a pond treatment system during a one year study. J Hazard Mater 421:126712

    Article  CAS  Google Scholar 

  • Ghamkhar R, Hartleb C, Wu F, Hicks A (2020) Life cycle assessment of a cold weather aquaponic food production system. J Clean Prod 244:118767

    Article  Google Scholar 

  • Gonzalez C, Marciniak J, Villaverde S, Leon C, Garcia PA, Munoz R (2008) Efficient nutrient removal from swine manure in a tubular biofilm photo-bioreactor using algae-bacteria consortia. Water Sci Technol 58(1):95–102

    Article  CAS  Google Scholar 

  • Gorito AM, Ribeiro ARL, Pereira MFR, Almeida CMR, Silva AMT (2022) Advanced oxidation technologies and constructed wetlands in aquaculture farms: what do we know so far about micropollutant removal? Environ Res 204(A):111955

  • Hamoutene D, Salvo F (2020) Biodegradation of some aquaculture chemotherapeutants weathered in flocculent samples collected at hard-bottom sites in Newfoundland (Canada). Mar Chem 224:103811

  • Han Y, Wang J, Zhao Z, Chen J, Lu H, Liu G (2017) Fishmeal application induces antibiotic resistance gene propagation in mariculture sediment. Environ Sci Technol 51(18):10850–10860

    Article  CAS  Google Scholar 

  • He Q, Zhu Y, Li G, Fan L, Ai H, Huangfu X, Li H (2017) Impact of dissolved oxygen on the production of nitrous oxide in biological aerated filters. Front Env Sci Eng 11(6):16

  • Huang X, Feng Y, Hu C, Xiao X, Yu D, Zou X (2016) Mechanistic model for interpreting the toxic effects of sulfonamides on nitrification. J Hazard Mater 305(15):123–129

    Article  CAS  Google Scholar 

  • Hu Z, Lee JW, Chandran K, Kim S, Brotto AC, Khanal SK (2015) Effect of plant species on nitrogen recovery in aquaponics. Bioresour Technol 188:92–98

    Article  CAS  Google Scholar 

  • Hu Z, Lee JW, Chandran K, Kim S, Sharma K, Khanal SK (2014) Influence of carbohydrate addition on nitrogen transformations and greenhouse gas emissions of intensive aquaculture system. Sci Total Environ 470:193–200

    Article  Google Scholar 

  • IPCC (2013) In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (Eds.), Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

  • Ji M, Hu Z, Hou C, Liu H, Ngo HH, GuoW LuS, Zhang J (2020) New insights for enhancing the performance of constructed wetlands at low temperatures. Bioresour Technol 301:122722

    Article  CAS  Google Scholar 

  • Ji M, Zhang J, Wang S, Liang S, Hu Z (2021) Enhanced phosphorus removal of constructed wetland through plant growth-promoting rhizobacteria (PGPR) addition. Environ Sci Pollut Res 28(37):52124–52132

    Article  CAS  Google Scholar 

  • Kampschreur MJ, Temmink H, Kleerebezem R, Jetten MSM, van Loosdrecht MCM (2009) Nitrous oxide emission during wastewater treatment. Water Res 43(17):4093–4103

    Article  CAS  Google Scholar 

  • Karya NGAI, van der Steen NP, Lens PNL (2013) Photo-oxygenation to support nitrification in an algal-bacterial consortium treating artificial wastewater. Bioresour Technol 134:244–250

    Article  CAS  Google Scholar 

  • Klinger D, Naylor R (2012) Searching for solutions in aquaculture: charting a sustainable course. Annu Rev Environ Resour 37:247

    Article  Google Scholar 

  • Kong AYY, Hristova K, Scow KM, Six J (2010) Impacts of different N management regimes on nitrifier and denitrifier communities and N cycling in soil microenvironments. Soil Biol Biochem 42(9):1523–1533

    Article  CAS  Google Scholar 

  • Lee CS, Lee S, Ko S, Oh H, Ahn C (2015) Effects of photoperiod on nutrient removal, biomass production, and algal-bacterial population dynamics in lab-scale photobioreactors treating municipal wastewater. Water Res 68:680–691

    Article  CAS  Google Scholar 

  • Lou X, Liu Z, Fang C, Tang Y, Guan J, Guo Y, Zhang X, Shi Y, Huang D, Cai Y (2022) Fate of sul.famethoxazole and potential formation of haloacetic acids during chlorine disinfection process in aquaculture water. Environ Res 204(A):111958

  • Love DC, Fry JP, Li X, Hill ES, Genello L, Semmens K, Thompson RE (2015) Commercial aquaponics production and profitability: findings from an international survey. Aquaculture 435:67–74

    Article  Google Scholar 

  • Migliorati MDA, Scheer C, Grace PR, Rowlings DW, Bell M, McGree J (2014) Influence of different nitrogen rates and DMPP nitrification inhibitor on annual N2O emissions from a subtropical wheat-maize cropping system. Agric Ecosyst Environ 186:33–43

    Article  Google Scholar 

  • Mujtaba G, Lee K (2017) Treatment of real wastewater using co-culture of immobilized Chlorella vulgaris and suspended activated sludge. Water Res 120:174–184

    Article  CAS  Google Scholar 

  • Munoz R, Guieysse B (2006) Algal-bacterial processes for the treatment of hazardous contaminants: a review. Water Res 40(15):2799–2815

    Article  CAS  Google Scholar 

  • Osada T, Shiraishi M, Hasegawa T, Kawahara H (2017) Methane, nitrous oxide and ammonia generation in full-scale swine wastewater purification facilities. Front Env Sci Eng 11(3):10

    Article  Google Scholar 

  • Patil HJ, Gatica J, Zolti A, Benet-Perelberg A, Naor A, Dror B, Al Ashhab A, Marman S, Hasan NA, Colwell RR, Sher D, Minz D, Cytryn E (2020) Temporal resistome and microbial community dynamics in an intensive aquaculture facility with prophylactic antimicrobial treatment. Microorganisms 8(12):1984

  • Qing Y, Li H, Zhang M, Lu S, Wu J, Liu F (2021) Effects of sulfadiazine in swine wastewater on microorganisms and nitrogen transformation processes in wetland sediment. Res Environ Sci 34(9):2191–2199

    CAS  Google Scholar 

  • Reay DS, Davidson EA, Smith KA, Smith P, Melillo JM, Dentener F, Crutzen PJ (2012) Global agriculture and nitrous oxide emissions. Nat Clim Change 2(6):410–416

    Article  CAS  Google Scholar 

  • Romero Gonzalez R, Fernandez Fernandez R, Martinez Vidal JL, Sanchez Muros MJ, GarridoFrenich A (2010) Depletion of veterinary drugs used in aquaculture after administration in feed to Gilthead Seabream (Sparus aurata). J Food Protect 73(9):1664–1670

    Article  Google Scholar 

  • Silva CR, Gomes LC, Brandao FR (2007) Effect of feeding rate and frequency on tarnbaqui (Colossoma macropomum) growth, production and feeding costs during the first growth phase in cages. Aquaculture 264(1–4):135–139

    Article  Google Scholar 

  • MAPRC (2007) Specification for the Application of Sulfanilamides in Aquaculture. In: SC/T 1084–2006 (ed Ministry of Agriculture C).

  • Wang G, Zhang Q, Kuang S, Li J (2019) The joint toxicity of mixed antibiotics on Chlorella vulgaris at normal environmental concentration. Asian J Ecotoxicol 14(2):122–128

    Google Scholar 

  • Wang L, Min M, Li Y, Chen P, Chen Y, Liu Y, Wang Y, Ruan R (2010) Cultivation of green algae Chlorella sp. in different wastewaters from municipal wastewater treatment plant. Appl Biochem Biotech 162(4):1174–1186

  • Wongkiew S, Hu Z, Chandran K, Lee JW, Khanal SK (2017) Nitrogen transformations in aquaponic systems: a review. Aqric Eng 76:9–19

    Google Scholar 

  • Wu X, Wu H, Zhang A, Sekou K, Li Z, Ye J (2022) Influence of polystyrene microplastics on levofloxacin removal by microalgae from freshwater aquaculture wastewater. J Environ Manage 301:113865

  • Yan C, Liu X, Zhang R, Song Z (2011) Effects of different kinds of disinfectant and antibiotics on the activity of Nitrifying Bacteria preparation. Hebei Fisheries 12:13-16+23

  • Ying G, He L, Ying A, Zhang Q, Liu Y, Zhao J (2017) China must reduce its antibiotic use. Environ Sci Technol 51(3):1072–1073

    Article  CAS  Google Scholar 

  • Zhi W, Ji G (2014) Quantitative response relationships between nitrogen transformation rates and nitrogen functional genes in a tidal flow constructed wetland under C/N ratio constraints. Water Res 64:32–41

    Article  CAS  Google Scholar 

  • Zhou L, Han P, Yu Y, Wang B, Men Y, Wagner M, Wu Q (2019) Cometabolic biotransformation and microbial-mediated abiotic transformation of sulfonamides by three ammonia oxidizers. Water Res 159:444–453

    Article  CAS  Google Scholar 

  • Zou Y, Hu Z, Zhang J, Xie H, Guimbaud C, Fang Y (2016a) Effects of pH on nitrogen transformations in media-based aquaponics. Bioresour Technol 210(SI):81–87

  • Zou Y, Hu Z, Zhang J, Xie H, Liang S, Wang J, Yan R (2016) Attempts to improve nitrogen utilization efficiency of aquaponics through nitrifies addition and filler gradation. Environ Sci Pollut Res 23(7):6671–6679

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We sincerely thanks for the assistance in elemental analysis from Analysis and Test Center of School of Environmental Science and Engineering, Shandong University.

Funding

This work was supported by National Key Research and Development Program of China (No. 2021YFC3200602), National Science Foundation of China (No. 51878388 and No. 51925803), Shandong Provincial Key Research and Development Program (Major Scientific and Technological Innovation Project) (No. 2020CXGC011406), Natural Science Foundation of Shandong Province (No. ZR2020YQ42), and Future Plan for Young Scholar of Shandong University.

Author information

Authors and Affiliations

  1. Shandong Key Laboratory of Environmental Processes and Health, School of Environmental Science and Engineering, Shandong University, Qingdao, 266237, People’s Republic of China

    Mingde Ji, Hang Gao, Jian Zhang, Shuang Liang & Zhen Hu

  2. Chengyang Branch of Qingdao Ecological Environment Bureau, Qingdao, 266109, People’s Republic of China

    Lingling Diao

  3. College of Safety and Environmental Engineering, Shandong University of Science and Technology, Qingdao, 266590, People’s Republic of China

    Jian Zhang

Authors
  1. Mingde Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hang Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lingling Diao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jian Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shuang Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhen Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.M. designed research, performed research, analyzed data, and wrote the manuscript; G.H. contributed in data collection and visualization; D.L. helped in checking the visualized results and revising the manuscript; Z.J. and L.S. contributed in proofreading and giving valuable comments. This study was done under the supervision by H.Z.

Corresponding author

Correspondence to Zhen Hu.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical approval

This article used fish (Cyprinus carpio) as an experimental object. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. And all the authors have checked and agreed to submit this manuscript into Applied Microbiology and Biotechnology.

Consent to publish

Authors are well aware and sure that the used data in this manuscript is not previously published.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ji, M., Gao, H., Diao, L. et al. Environmental impacts of antibiotics addition to algal-bacterial-based aquaponic system. Appl Microbiol Biotechnol 106, 3777–3786 (2022). https://doi.org/10.1007/s00253-022-11944-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-022-11944-9

Keywords

Search

Navigation