Abstract
Antibiotics are frequently applied in aquaculture to control infectious diseases and promote aquaculture production. The long-term application of antibiotics can lead to antibiotic resistance within an ecosystem. Herein, we assessed the ecological responses to two antibiotics (oxytetracycline (OTC) and sulfadiazine (SD)) at three concentrations (0 mg/kg (control), 10 mg/kg, and 1000 mg/kg) re-entering the aquaculture sediments of shrimp ponds with an approximately long-term drug application history (5, 15, and more than 30 years) for 2 and 4 months. For the newly reclaimed aquaculture ponds (approximately 5 years), the re-entered OTC significantly promoted urease activity (UA) and peroxidase activity (POA), while inhibited dehydrogenase activity (DHA) and fluorescein diacetate esterase activity (FDA). Meanwhile, the re-entered SD showed promotional effects on POA and DHA, and inhibitory effects on UA and FDA. For ponds with 15 years of aquaculture history, re-entered OTC promoted POA, inhibited FDA, and changed the influencing effects of UA and DHA with exposure time. The re-entered SD showed promotional effects on UA, POA and DHA, and inhibitory effects on FDA. For long-term aquaculture ponds (more than 30 years of aquaculture history), re-entered OTC promoted POA, DHA, and FDA, while it inhibited UA. Meanwhile, SD promoted all four enzyme activities. Pearson correlation analysis indicated that the variances of enzyme responses to the re-entry of antibiotics in the three sediment environments were related with the type, concentration, and exposure time of antibiotics, as well as the sediment properties and aquaculture history. The enzyme activities in the sediment environment from newly reclaimed aquaculture ponds were more sensitive to the re-entered antibiotics, while the enzyme activities displayed a clear tolerance in the sediment environment with more than 30 years of aquaculture history. However, in the sediment environment with 15 years of aquaculture history, the response of the enzyme activities to re-entered antibiotics demonstrated time processes of antibiotic adaptation during antibiotic resistance selection. This study has illustrated the effects of re-entered antibiotics on enzyme activities in the aquaculture environment with long-term antibiotic resistance/tolerance profiles, and further establishes the possible effects on ecosystem functioning in continuous antibiotic selection pressure.
Similar content being viewed by others
Data availability
The data sets used and/or analyzed during the current study are available from the corresponding author on request.
References
Adam G, Duncan H (2001) Development of a sensitive and rapid method for the measurement of total microbial activity using fluorescein diacetate (FDA) in a range of soils. Soil Biol Biochem 33:943–951
Bao Y, Zhou Q, Wan Y, Yu Q, Xie X (2010) Effects of soil/solution ratios and cation types on adsorption and desorption of tetracycline in soils. Soil Sci Soc Am J 74:1553–1561
Barrena R, Vázquez F, Sánchez A (2008) Dehydrogenase activity as a method for monitoring the composting process. Bioresour Technol 99:905–908
Bernier SP, Surette MG (2013) Concentration-dependent activity of antibiotics in natural environments. Front Microbiol 4:20
Boxall ABA, Rudd MA, Brooks BW, Caldwell DJ, ChoiKHickmann S, InnesE OK, Staveley JP, Verslycke T, AnkleyGT BKF, Belanger SE, Berninger JP, Carriquiriborde P, Coors A, DeLeo PC, Dyer SD, Ericson JF, Gagné F, Giesy JP, Gouin T, Hallstrom L, Karlsson MV, Larsson DGJ, Lazorchak JM, Mastrocco F, McLaughlin A, McMaster ME, Meyerhoff RD, Moore R, Parrott JL, Snape JR, Murray-Smith R, Servos MR, Sibley PK, Straub JO, Szabo ND, Topp E, Tetreault GR, Trudeau VL, Van Der Kraak G (2012) Pharmaceuticals and personal care products in the environment: what are the big questions? Environ Health Persp 120:1221–1229
Brandt KK, Amézquita A, Backhaus T, Boxall A, Coors A, Heberer T, Lawrence JR, Lazorchak J, Schönfeld J, Snape JR, Zhu YG, Topp E (2015) Ecotoxicological assessment of antibiotics: a call for improvedconsideration of microorganisms. Environ Int 85:189–205
Cairns J, Ruokolainen L, Hultman J, Tamminen M, Virta M, Hiltunen T (2018) Ecology determines how low antibiotic concentration impacts community composition and horizontal transfer of resistance genes. Commun Biol 1:35
Chaperon S, Sauvé S (2007) Toxicity interaction of metals (Ag, Cu, Hg, Zn) to urease and dehydrogenase activities in soils. Soil Biol Biochem 39:2329–2338
Chen W, Liu W, Pan N, Jiao W, Wang M (2013) Oxytetracycline on functions and structure of soil microbial community. J Soil Sci Plant Nutr 13(4):967–975
Córdova-Kreylos AL, Scow KM (2007) Effects of ciprofloxacin on salt marsh sediment microbial communities. ISME J 1:585–595
Ding C, He J (2010) Effect of antibiotics in the environment on microbial populations. Appl Microbiol Biot 87:925–941
Fang H, Han YL, Yin YM, Pan X, Yu YL (2014) Variations in dissipation rate, microbial function, and antibiotic resistance due to repeated introductions of manure containing sulfadiazine and chlortetracycline to soil. Chemosphere 96:51–56
Friman VP, GuzmanL M, Reuman DC, Bell T (2015) Bacterial adaptation to sublethal antibiotic gradients can change the ecological properties of multitrophic microbial communities. Proc Biol Sci 282:20142920
Gu C, Karthikeyan KG (2008) Sorption of the antibiotic tetracycline to humic mineral complexes. J Environ Qual 37:704–711
Gutiérrez IR, Watanabe N, Harter T, Glaser B, Radke M (2010) Effect of sulfonamide antibiotics on microbial diversity and activity in a Californian MollicHaploxeralf. J Soil Sediment 10:537–544
Grenni P, Ancona V, BarraCaracciolo A (2018) Ecological effects of antibiotics on natural ecosystems: a review. Microchem J 136:25–39
Han JC, Zhang CG, Cheng J, Wang F, Qiu L (2019) Effects of biogas residues containing antibiotics on soil enzyme activity and lettuce growth. Environ Sci Pollut R 26:6116–6122
Hakulinen R, Kähkönen MA, Salkinoja-Salonen M (2005) Vertical distribution of sediment enzyme activities involved in the cycling of carbon, nitrogen, phosphorus, and sulfur in three boreal rural lakes. Water Res 39:2319–2326
Hou L, Yin G, Liu M, Zhou JL, Zheng YL, Gao J, Zong HB, Yang Y, Gao L, Tong CF (2015) Effects of sulfamethazine on denitrification and the associated N2O release in estuarine and coastal sediments. Environ Sci Tech 49:326–333
Holmström K, Gräslund S, Wahlström A, Poungshompoo S, Bengtsson BE, Kautsky N (2003) Antibiotic use in shrimp farming and implications for environmental impacts and human health. Int J Food Sci Tec 38:255–266
Hossain A, Nakamichi S, Habibullah-Al-Mamun M, Tani K, Masunaga S, Matsuda H (2017) Occurrence, distribution, ecological and resistance risks of antibiotics in surface water of finfish and shellfish aquaculture in Bangladesh. Chemsphere 188:329–336
Jechalke S, Heuer H, Siemens J, Amdlung W, Smalla K (2014) Fate and effects of veterinary antibiotics in soil. Trends Microbiol 22:536–545
Kizilkaya R (2008) Dehydrogenase activity in Lumbricusterrestris casts and surrounding soil affected by the addition of different organic wastes and Zn. Bioresour Technol 99:946–953
Kotzerke A, Sharma S, Schauss K, Heuer H, Thiele-Bruhn S, Smalla K, Wilke BM, Schloter M (2008) Alterations in soil microbial activity and N-transformation processes due to sulfadiazine loads in pig-manure. Environ Pollut 153:315–322
Kümmerer K (2004) Resistance in the environment. J Antimicrob Chemother 54:311–320
Kümmerer K (2009) Antibiotics in the aquatic environment - a review - Part I. Chemos 75:417–434
Li C, Chen JY, Wang JH, Ma ZH, Han P, Luan YX, Lu AX (2015) Occurrence of antibiotics in soils and manure from greenhouse vegetable production bases in Beijing, China, and an associated risk assessment. Sci Total Environ 521–522:101–107
Li WC (2014) Occurrence, sources, and fate of pharmaceuticals in aquatic environment and soil. A Review Environ Pollut 187:193–201
Li ZG, Luo YM, Teng Y (2008) Research method of soil and environment microorganisms. Science Press, Beijing (in Chinese)
Li FF, Chen LJ, Chen WD, Bao YY, Zheng YH, Huang B, Mu QL, Wen DH, Feng CP (2020) Antibiotics in coastal water and sediments of the East China Sea: distribution, ecological risk assessment and indicators screening. Mar Pollut Bull 151:110810
Liang X, Chen B, Nie X, Shi Z, Huang X, Li X (2013) The distribution and partitioning of common antibiotics in water and sediment of the pearl river estuary, south China. Chemsphere 92: 1410e1416
Lee SH, Oh BI, Kim JG (2008) Effects of various amendments on heavy mineral oil bioremediation and soil microbial activity. Bioresour Technol 99:2578–2587
Ma T, Pan X, Chen L, Liu W, Christie P, Luo Y, Wu L (2016) Effects of different concentrations and application frequencies of oxytetracycline on soil enzyme activities and microbial community diversity. Eur J Soil Biol 76:53–60
Mackay AA, Seremet DE (2008) Probe compounds to quantify cation exchange and complexation interactions of ciprofloxacin with soils. Environ Sci Technol 42:8270–8276
Matozzo V (2014) Effects of pharmaceuticals on immune parameters of aquatic invertebrates; A review. Invert Surviv J 11:163–173
Martínez JL (2008) Antibiotics and antibiotic resistance genes in natural environments. Science 321:365–367
Merino C, Godoy R, Matus R (2016) Soil enzymes and biological activity at different levels of organic matter stability. J Soil Sci Plant Nut 16:14–30
Murray AK, Zhang L, Yin X, Zhang T, Buckling A, Snape J, Gaze WH (2018) Novel insights into selection for antibiotic resistance in complex microbial communities. mBio 9(4): e00969–18
McBride SG, Strickland MS (2019) Quorum sensing modulates microbial efficiency by regulating bacterial investment in nutrient acquisition enzymes. Soil Biol Biochem136: 107514
Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670
Nosrati K, Govers G, Ahmadi H, Sharifi F, Amoozegar MA, Merckx R, Vanmaercke M (2011) An exploratory study on the use of enzyme activities as sediment tracers: Biochemical fingerprints? Int J Sediment Res 26:136–151
Neela FA, Nonaka L, Suzuki S (2007) The diversity of multi-drug resistance profiles in tetracycline-resistant Vibrio species isolated from coastal sediments and seawater. J Microbiol 45:64–68
Paola G, Valeria A, Anna BC (2018) Ecological effects of antibiotics on natural ecosystems. Microchem J 136:25–29
Qiao M, Ying GG, Singer AC, Zhu YG (2018) Review of antibiotic resistance in China and its environment. Environ Int 110: 160e172.
Roose-Amsaleg C, Laverman AM (2016) Do antibiotics have environmental side effects? Impact of synthetic antibiotics on biogeochemical processes. Environ Sci Pollut Res Int 23:4000–4012
Rochette P, Gregorich EG (1998) Dynamics of soil microbial biomass C, soluble organic C, and CO2 evolution after three years of manure application. Can J Soil Sci 78:283–290
Sarmah AK, Meyer MT, Boxall ABA (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate, and effects of veterinary antibiotics (VAs) in the environment. Chemsphere 65:725–759
Singh A, Ghoshal N (2013) Impact of herbicide and various soil amendments on soil enzyme activities in a tropical rainfed agroecosystem. Eur J Soil Biol 54:56–62
Shen XX, Jin GQ, Zhao YJ, Shao XH (2020) Prevalence and distribution analysis of antibiotic resistance genes in alarge-scale aquaculture environments. Sci Total Environ 711: 134626
Tolls J (2001) Sorption of veterinary pharmaceuticals in soils: a review. Environ Sci Tech 35:3397–3406
Thiele-Bruhn S, Beck IC (2005) Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 59:457–465
Telesiński A, Krzyśko-Łupicka T, Cybulska K, Pawłowska B, Biczak R, Śnieg M, Wróbel J (2019) Comparison of oxidoreductive enzyme activities in three coal tar creosote-contaminated soils. Soil Res 57:814–824
Telesinski A, Platkowski M, Cybulska K, Telesinska N, Wrobel J, Pawlowska B (2018) Response of soil enzymes to two antibiotics: polymyxin B And penicillin G. Fresen Environ Bull 27:3837–3845
Uddin M, Chen JW, Qiao XL, Tian R, Zhu MH (2020) Insight into the dynamics and bioavailability of antibiotics in paddy soils by in situ soil moisture sampler. Sci Total Environ 703(135562):8
Veres Z, Kotroczó Z, Fekete I, Tóth JA, Lajtha K, Townsend K, Tóthmérész B (2015) Soil extracellular enzyme activities are sensitive indicators of detrital inputs and carbon availability. Appl Soil Ecol 92:18–23
Wang SR (2014) Sediment-water interface process of lakes: Theories and methods. Science Press, Beijing (in Chinese)
Wang W, Wang H, Zhang W, Liang H, Gao D (2017) Occurrence, distribution, and risk assessment of antibiotics in the songhua river in China. Environ Sci Pollut Res Int 24 (23): 1e11.
Wang M, Ren P, Liu H, Dai X (2021) Investigating antibiotics, antibiotic resistance genes in soil, groundwater and vegetables in relation to agricultural field - applicated with lincomycin mycelial residues compost. Sci Total Environ 777: 146066.
Weintraub SR, Wieder WR, Cleveland CC, Townsend AR (2013) Organic matter inputs shift soil enzyme activity and allocation patterns in wet tropical forest. Biogeochemistry 114:313–326
Wepking C, Badgley B, Barrett JE, Knowlton KF, Lucas JM, Minick KJ, Ray PP, Shawver SE, Strickland MS (2019) Prolonged exposure to manure from livestock-administered antibiotics decreases ecosystem carbon-use efficiency and alters nitrogen cycling. Ecol Lett 22:2067–2076
Wyszkowska J, Boros-Lajszner E, Lajszner W, Kucharski J (2017) Reaction of soil enzymes and spring barley to copper chloride and copper sulfate. Environ Earth Sci 76:403
Xi XP, Wang M, Chen YS, Yu S, Hong YW, Ma J, Wu Q, Lin QY, Xu XR (2015) Adaption of the microbial community to continuous exposure of multiple residual antibiotics in sediments from a salt-water aquacultural farm. J Hazard Mater 290:96–105
Xie HW, Hao HS, Xu N, Liang XX, Gao DX, Xu YR, Gao Y, Tao HC, Wong MH (2019) Pharmaceuticals and personal care products in water, sediments, aquatic organisms, and fish feeds in the Pearl RiverDelta: occurrence, distribution, potential sources, and health risk assessment. Sci Total Environ 659:230–239
Xu J, Xu Y, Wang HM, Guo CS, Qiu HY, He Y, Zhang Y, Li XC, Meng W (2015) Occurrence of antibiotics and antibiotic resistance genes in a sewage treatment plant and its effluent-receiving river. Chemsphere 119:1379–1385
Xun WB, Huang T, Zhao J, Ran W, Wang B, Shen Q, Zhang RF (2015) Environmental conditions rather than microbial inoculum composition determine the bacterial composition, microbial biomass and enzymatic activity of reconstructed soil microbial communities. Soil Biol Biochem 90:10–18
Yao ZP, Li ZJ, Lang YC, Zhang YQ, Yao JH, Xie XY (2009) Dynamic responses of soil enzymatic activities to oxytetracycline in soil. Plant Nutri and Ferti Sci 15:696–700 (in Chinese)
Yang Y, Song W, Lin H, Wang W, Du L, Xing W (2018) Antibiotics and antibiotic resistance genes in global lakes: a review and meta-analysis. Environ Int 116: 60e73.
Yuan JL, Ni M, Liu M, Zheng Y, Gu ZM (2019) Occurrence of antibiotics and antibiotic resistance genes in a typical estuary aquaculture region of Hangzhou Bay, China. Mar Pollut Bull 138:376–384
Zielezny Y, Groeneweg J, Vereecken H, Tappe W (2006) Impact of sulfadiazine and chlorotetracycline on soil bacterial community structure and respiratory activity. Soil Biol Biochem 38:2372–2380
Zhang LL, Shen LN, Qin S, Cui JS, Liu Y (2020). Quinolones antibiotics in the Baiyangdian Lake, China: occurrence, distribution, predicted no-effect concentrations (PNECs) and ecological risks by three methods. Environ Pollut 256: 113458.
Zhang C, Qiu L (2018) Comprehensive sustainability assessment of a biogas-linked agro-ecosystem: a case study in China. Clean Techol Envir 20:1847–1860
Zhang QQ, Ying GG, Pan CG, Liu YS, Zhao JL (2015a) Comprehensive evaluation of antibiotic emission and fate in the river basins of China: source analysis, multimedia modeling, and linkage to bacterial resistance. Environ Sci Tech 49:6772–6782
Zhang YL, Chen LJ, Chen XH, Tan ML, Duan ZH, Wu ZJ, Li XJ, Fan XH (2015b) Response of soil enzyme activity to long-term restoration of desertified land. CATENA 133:64–70
Zhen L, Gu J, Hu T, Chen ZX (2018) Effects of compost containing oxytetracycline on enzyme activities and microbial communities in maize rhizosphere soil. Environ Sci Pollut Res Int 25:29459–29467
Funding
This research was supported by the National Natural Science Foundation of China (Grant Nos. 41671495, 41301572) and the Program for New Century Excellent Talents in Fujian Province University.
Author information
Authors and Affiliations
Contributions
CYS designed the work plan, HJC, XJH, and YBF performed all experiments, and FY and CYS analyzed the data and wrote manuscript. JJP helped in modifying this manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Robert Duran
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Feng, Y., Hu, J., Chen, Y. et al. Ecological response to antibiotics re-entering the aquaculture environment with possible long-term antibiotics selection based on enzyme activity in sediment. Environ Sci Pollut Res 29, 19033–19044 (2022). https://doi.org/10.1007/s11356-021-17114-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-17114-0