Abstract
Though heavy metals are widely reported to induce antibiotic resistance propagation, how antibiotic resistance changes in response to heavy metal abundances remains unclearly. In this study, the tylosin fermentation dregs (TFDs) and swine manure co-composting process amended with two exposure levels of heavy metal Zn were performed. Results showed that the bioavailable Zn contents decreased 2.6-fold averagely, and the removal percentage of total tylosin resistance genes was around 23.5% after the co-composting completed. Furthermore, the tylosin resistance genes and some generic bacteria may exhibited a hormetic-like dose-response with the high-dosage inhibition and low dosage stimulation induced by bioavailable Zn contents during the co-composting process, which represented a beneficial aspect of adaptive responses to harmful environmental stimuli. This study provided a comprehensive understanding and predicted risk assessment for the Zn-contaminate solid wastes deposal and suggested that low levels of Zn or other heavy metals should receive more attention for their potential to the induction of resistance bacteria and propagation of antibiotic resistance genes.
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Data Availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Berg J, Thorsen MK, Holm PE, Jensen J, Nybroe O, Brandt KK (2010) Cu Exposure under field conditions coselects for antibiotic resistance as determined by a novel cultivation-independent bacterial community tolerance assay. Environ Sci Technol 44:8724–8728
Calabrese EJ (2001) Overcompensation stimulation: a mechanism for hormetic effects. Crit Rev Toxicol 31(4&5):425–470
Calabrese EJ, Baldwin LA (2003) Hormesis: the dose-response revolution. Annu Rev Pharmacol Toxicol 43:175–197
Calabrese EJ, Mattson MP (2017) How does hormesis impact biology, toxicology, and medicine? NPJ Aging Mech Dis 3:13
Carlson JC, Mabury SA (2006) Dissipation kinetics and mobility of chlortetracycline, tylosin, and monensin in an agricultural soil in northumberland county, Ontario, Canada. Environ Toxicol Chem 25(1):1
Chen Z, Wang Y, Wen Q (2018) Effects of chlortetracycline on the fate of multi-antibiotic resistance genes and the microbial community during swine manure composting. Environ Pollut 237:977–987
Choudhury R, Srivastava S (2001) Zinc resistance mechanisms in bacteria. Curr Sci 81(7):768–775
Cui E, Wu Y, Zuo Y, Chen H (2016) Effect of different biochars on antibiotic resistance genes and bacterial community during chicken manure composting. Bioresour Technol 203:11–17
de Moraes CP, de Brito I, Tropaldi L, Carbonari CA, Velini ED (2020) Hormetic effect of glyphosate on Urochloa decumbens plants. J Environ Sci Health B 55(4):376–381
Dewey KA, Gaw SK, Northcott GL, Lauren DR, Hackenburg S (2012) The effects of copper on microbial activity and the degradation of atrazine and indoxacarb in a New Zealand soil. Soil Biol Biochem 52:64–74
Di Cesare A, Eckert EM, D'Urso S, Bertoni R, Gillan DC, Wattiez R, Corno G (2016) Co-occurrence of integrase 1, antibiotic and heavy metal resistance genes in municipal wastewater treatment plants. Water Res 94:208–214
Dolliver H, Gupta S, Noll S (2008) Antibiotic degradation during manure composting. J Environ Qual 37(3):1245–1253
Fan H, Liao J, Abass OK, Liu L, Huang X, Wei L, Li J, Xie W, Liu C (2019) Effects of compost characteristics on nutrient retention and simultaneous pollutant immobilization and degradation during co-composting process. Bioresour Technol 275:61–69
Guerin E, Cambray G, Sanchez-Alberola N, Campoy S, Erill I, Da Re S, Gonzalez-Zorn B, Barbe J, Ploy MC, Mazel D (2009) The SOS response controls integron recombination. Science 324(5930):1034
Hamdi H, Manusadzianas L, Aoyama I, Jedidi N (2006) Effects of anthracene, pyrene and benzo[a]pyrene spiking and sewage sludge compost amendment on soil ecotoxicity during a bioremediation process. Chemosphere 65(7):1153–1162
Hu D, Coats JR (2007) Aerobic Degradation and Photolysis of Tylosin in Water and Soil. Environ Toxicol Chem 26(5):884–889
Ingelmo F, Molina MJ, Soriano MD, Gallardo A, Lapena L (2012) Influence of organic matter transformations on the bioavailability of heavy metals in a sludge based compost. J Environ Manag 95(Suppl):S104–S109
Kaplan JB (2011) Antibiotic-induced biofilm formation. Int J Artif Organs 34(9):737–751
Li H, Duan M, Gu J, Zhang Y, Qian X, Ma J, Zhang R, Wang X (2017a) Effects of bamboo charcoal on antibiotic resistance genes during chicken manure composting. Ecotoxicol Environ Saf 140:1–6
Li HH, Chen LJ, Yu L, Guo ZB, Shan CQ, Lin JQ, Gu YG, Yang ZB, Yang YX, Shao JR, Zhu XM, Cheng Z (2017b) Pollution characteristics and risk assessment of human exposure to oral bioaccessibility of heavy metals via urban street dusts from different functional areas in Chengdu, China. Sci Total Environ 586:1076–1084
Li J, Xin Z, Zhang Y, Chen J, Yan J, Li H, Hu H (2017c) Long-term manure application increased the levels of antibiotics and antibiotic resistance genes in a greenhouse soil. Appl Soil Ecol 121:193–200
Li X, Gu AZ, Zhang Y, Xie B, Li D, Chen J (2019) Sub-lethal concentrations of heavy metals induce antibiotic resistance via mutagenesis. J Hazard Mater 369:9–16
Liao H, Zhao Q, Cui P, Chen Z, Yu Z, Geisen S, Friman VP, Zhou S (2019) Efficient reduction of antibiotic residues and associated resistance genes in tylosin antibiotic fermentation waste using hyperthermophilic composting. Environ Int 133(Pt B):105203
Liu T, Liu Z, Zheng Q, Lang Q, Xia Y, Peng N, Gai C (2018a) Effect of hydrothermal carbonization on migration and environmental risk of heavy metals in sewage sludge during pyrolysis. Bioresour Technol 247:282–290
Liu Y, Feng Y, Cheng D, Xue J, Wakelin S, Li Z (2018b) Dynamics of bacterial composition and the fate of antibiotic resistance genes and mobile genetic elements during the co-composting with gentamicin fermentation residue and lovastatin fermentation residue. Bioresour Technol 261:249–256
Lu D, Wang L, Yan B, Ou Y, Guan J, Bian Y, Zhang Y (2014) Speciation of Cu and Zn during composting of pig manure amended with rock phosphate. Waste Manag 34(8):1529–1536
Lu Z, Na G, Gao H, Wang L, Bao C, Yao Z (2015) Fate of sulfonamide resistance genes in estuary environment and effect of anthropogenic activities. Sci Total Environ 527-528:429–438
Meng J, Wang L, Zhong L, Liu X, Brookes PC, Xu J, Chen H (2017) Contrasting effects of composting and pyrolysis on bioavailability and speciation of Cu and Zn in pig manure. Chemosphere 180:93–99
Murado MA, Vazquez JA (2007) The notion of hormesis and the dose-response theory: a unified approach. J Theor Biol 244(3):489–499
Nemati K, Abu Bakar NK, Abas MR, Sobhanzadeh E (2011) Speciation of heavy metals by modified BCR sequential extraction procedure in different depths of sediments from Sungai Buloh, Selangor, Malaysia. J Hazard Mater 192(1):402–410
Nies DH (1992) Resistance to Cadmium, Cobalt, Zinc, and Nickel in Microbes. Plasmid 27:17–28
Novo A, André S, Viana P, Nunes OC, Manaia CM (2013) Antibiotic resistance, antimicrobial residues and bacterial community composition in urban wastewater. Water Res 47(5):1875–1887
Peltier E, Vincent J, Finn C, Graham DW (2010) Zinc-induced antibiotic resistance in activated sludge bioreactors. Water Res 44(13):3829–3836
Peng H, Gu J, Wang X, Wang Q, Sun W, Hu T, Guo H, Ma J, Bao J (2020) Insight into the fate of antibiotic resistance genes and bacterial community in co-composting green tea residues with swine manure. J Environ Manag 266:110581
Pezzoni M, Pizarro RA, Costa CS (2018) Exposure to low doses of UVA increases biofilm formation in Pseudomonas aeruginosa. Biofouling 34(6):673–684
Ren S, Guo X, Lu A, Guo X, Wang Y, Sun G, Guo W, Ren C, Wang L (2018) Effects of co-composting of lincomycin mycelia dregs with furfural slag on lincomycin degradation, maturity and microbial communities. Bioresour Technol 265:155–162
Ren S, Lu A, Guo X, Zhang Q, Wang Y, Guo X, Wang L, Zhang B (2019) Effects of co-composting of lincomycin mycelia dregs with furfural slag on lincomycin degradation, degradation products, antibiotic resistance genes and bacterial community. Bioresour Technol 272:83–91
Roosa S, Wattiez R, Prygiel E, Lesven L, Billon G, Gillan DC (2014) Bacterial metal resistance genes and metal bioavailability in contaminated sediments. Environ Pollut 189:143–151
Silver S (1996) Bacterial resistances to toxic metal ions - a review. Gene 179:9–19
Sun H, Ge H, Zheng M, Lin Z, Liu Y (2016) Mechanism underlying time-dependent cross-phenomenon between concentration-response curves and concentration addition curves: a case study of sulfonamides-erythromycin mixtures on Escherichia coli. Sci Rep 6:33718
Swati A, Hait S (2017) Fate and bioavailability of heavy metals during vermicomposting of various organic wastes—A review. Process Saf Environ Prot 109:30–45
Swick MC, Morgan-Linnell SK, Carlson KM, Zechiedrich L (2011) Expression of multidrug efflux pump genes acrAB-tolC, mdfA, and norE in Escherichia coli clinical isolates as a function of fluoroquinolone and multidrug resistance. Antimicrob Agents Chemother 55(2):921–924
Szekeres E, Baricz A, Chiriac CM, Farkas A, Opris O, Soran ML, Andrei AS, Rudi K, Balcazar JL, Dragos N, Coman C (2017) Abundance of antibiotics, antibiotic resistance genes and bacterial community composition in wastewater effluents from different Romanian hospitals. Environ Pollut 225:304–315
Tasho RP, Cho JY (2016) Veterinary antibiotics in animal waste, its distribution in soil and uptake by plants: A review. Sci Total Environ 563-564:366–376
Theophel K, Schacht VJ, Schluter M, Schnell S, Stingu CS, Schaumann R, Bunge M (2014) The importance of growth kinetic analysis in determining bacterial susceptibility against antibiotics and silver nanoparticles. Front Microbiol 5:544
Wang J, Koo Y, Alexander A, Yang Y, Westerhof S, Zhang Q, Schnoor JL, Colvin VL, Braam J, Alvarez PJ (2013) Phytostimulation of poplars and arabidopsis exposed to silver nanoparticles and Ag(+) at sublethal concentrations. Environ Sci Technol 47(10):5442–5449
Wang M, Liu H, Dai X (2020) Dosage effects of lincomycin mycelial residues on lincomycin resistance genes and soil microbial communities. Environ Pollut 256:113392
Xu Y, Xu J, Mao D, Luo Y (2017) Effect of the selective pressure of sub-lethal level of heavy metals on the fate and distribution of ARGs in the catchment scale. Environ Pollut 220(Pt B):900–908
Yang Y, Alvarez PJJ (2015) Sublethal concentrations of silver nanoparticles stimulate biofilm development. Environ Sci Technol Lett 2(8):221–226
Yang L, Zhang S, Chen Z, Wen Q, Wang Y (2016) Maturity and security assessment of pilot-scale aerobic co-composting of penicillin fermentation dregs (PFDs) with sewage sludge. Bioresour Technol 204:185–191
Yang X, Li Q, Tang Z, Zhang W, Yu G, Shen Q, Zhao FJ (2017) Heavy metal concentrations and arsenic speciation in animal manure composts in China. Waste Manag 64:333–339
Zhang J, Sui Q, Tong J, Buhe C, Wang R, Chen M, Wei Y (2016) Sludge bio-drying: Effective to reduce both antibiotic resistance genes and mobile genetic elements. Water Res 106:62–70
Zhang B, Wang MM, Wang B, Xin Y, Gao J, Liu H (2018) The effects of bio-available copper on macrolide antibiotic resistance genes and mobile elements during tylosin fermentation dregs co-composting. Bioresour Technol 251:230–237
Zhao J, Sun X, Awasthi MK, Wang Q, Ren X, Li R, Chen H, Wang M, Liu T, Zhang Z (2018) Performance evaluation of gaseous emissions and Zn speciation during Zn-rich antibiotic manufacturing wastes and pig manure composting. Bioresour Technol 267:688–695
Zhou H, Meng H, Zhao L, Shen Y, Hou Y, Cheng H, Song L (2018) Effect of biochar and humic acid on the copper, lead, and cadmium passivation during composting. Bioresour Technol 258:279–286
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This work was financially supported by the National Natural Science Foundation of China (grant number 51678189).
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BZ: Experiment design and operation, validation, visualization, data curation, software, writing (original) draft, writing (review), and editing
QB Y: Investigation, visualization, formal analysis, data curation, writing (review), and editing
MM W: Methodology, conceptualization, and data curation
RN S: Methodology and data curation
HL L: Resources, project administration, supervision, writing (review), and editing
PW*: Funding acquisition, resources, project administration, supervision, writing (review), and editing
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Zhang, B., Yuan, Q., Wang, M.m. et al. Insights into the effects of Zn exposure on the fate of tylosin resistance genes and dynamics of microbial community during co-composting with tylosin fermentation dregs and swine manure. Environ Sci Pollut Res 28, 14423–14433 (2021). https://doi.org/10.1007/s11356-020-11471-y
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DOI: https://doi.org/10.1007/s11356-020-11471-y