Skip to main content
Log in

Application of spray-dried erythromycin fermentation residue as a soil amendment: antibiotic resistance genes, nitrogen cycling, and microbial community structure

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Erythromycin fermentation residue (EFR) after spray drying could be reused as a soil amendment. However, the effects of spray-dried EFR on antibiotic resistance genes (ARGs), nitrogen cycling, and microbial community structure in soil are rarely reported. In this study, a pot experiment was conducted by adding spray-dried EFR to soil. For the application of 1.0% spray-dried EFR, the residual erythromycin (ERY) could be rapidly removed with the half-life of 22.2 d; the total relative abundance of ARGs increased at first, but decreased to the initial level of the control group in the end; genes related to ammonium assimilation (glnA, gltB, gltD), ammonification (gdhA, gudB, cynT, cynS, ncd2), denitrification (narI, narG, narH), assimilatory nitrate reduction (nirA, nasA), and dissimilatory nitrate reduction (nirD) were enriched; soil microbial community structure presented temporary variation. Network analysis showed significant negative correlations between ARGs and nitrogen cycling genes. The addition of 6.0% spray-dried EFR resulted in the amplification of ARGs and inhibition of nitrogen cycling. This work provides new insights into the effects of spray-dried EFR on ARGs, nitrogen cycling, and microbial community structure within the fertilized soil.

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.

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 article and its supplementary material.

References

  • An Z, Gao D, Chen F, Wu L, Zhou J, Zhang Z, Dong H, Yin G, Han P, Liang X, Liu M, Hou L, Zheng Y (2021) Crab bioturbation alters nitrogen cycling and promotes nitrous oxide emission in intertidal wetlands: Influence and microbial mechanism. Sci Total Environ 797:149176

    Article  CAS  Google Scholar 

  • Bewick M (1979) The use of antibiotic fermentation wastes as fertilizers for tomatoes. J Agr Sci 92(3):669–674

    Article  Google Scholar 

  • Bi Z, Song G, Sun X (2022) Deciphering antibiotic resistance genes and microbial community of anammox consortia under sulfadiazine and chlortetracycline stress. Ecotox Environ Safe 234:113343

    Article  CAS  Google Scholar 

  • Bottoni P, Caroli S, Caracciolo AB (2010) Pharmaceuticals as priority water contaminants. Toxicol Environ Chem 92:549–565

    Article  CAS  Google Scholar 

  • Cai C, Gong P, Wang Y, Wang M, Zhang B, Wang B, Liu H (2018) Investigating the environmental risks from the use of spray-dried cephalosporin mycelial dreg (CMD) as a soil amendment. J Hazard Mater 359:300–306

    Article  CAS  Google Scholar 

  • Cai C, Li L, Hua Y, Liu H, Dai X (2021) Ferroferric oxide promotes metabolism in Anaerolineae other than microbial syntrophy in anaerobic methanogenesis of antibiotic fermentation residue. Sci Total Environ 758:143601

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336

    Article  CAS  Google Scholar 

  • Chen Q, An X, Li H, Su J, Ma Y, Zhu YG (2016) Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil. Environ Int 92–93:1–10

    Article  Google Scholar 

  • Chen Q-L, An X-L, Li H, Zhu Y-G, Su J-Q, Cui L (2017) Do manure-borne or indigenous soil microorganisms influence the spread of antibiotic resistance genes in manured soil? Soil Biol Biochem 114:229–237

    CAS  Google Scholar 

  • Chen C, Ray P, Knowlton KF, Pruden A, Xia K (2018) Effect of composting and soil type on dissipation of veterinary antibiotics in land-applied manures. Chemosphere 196:270–279

    Article  CAS  Google Scholar 

  • Chinese NEPA (2012) Water and wastewater monitoring methods, 4th edn. Chinese Environmental Science Publishing House, Beijing

  • Cusidó JA, Cremades LV (2012) Atomized sludges via spray-drying at low temperatures: An alternative to conventional wastewater treatment plants. J Environ Ma 105:61–65

    Article  Google Scholar 

  • Dang C, Liu S, Chen Q, Sun W, Zhong H, Hu J, Liang E, Ni J (2021) Response of microbial nitrogen transformation processes to antibiotic stress in a drinking water reservoir. Sci Total Environ 797:149119

    Article  CAS  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998

    Article  CAS  Google Scholar 

  • Gerber PF, Xiao C-T, Chen Q, Zhang J, Halbur PG, Opriessnig T (2014) The spray-drying process is sufficient to inactivate infectious porcine epidemic diarrhea virus in plasma. Vet Microbiol 174(1–2):86–92

    Article  Google Scholar 

  • Gong P, Liu H, Cai C, Wang G, Xin Y, Dai X (2020) Alkaline-thermally treated penicillin V mycelial residue amendment improved the soil properties without triggering antibiotic resistance. Waste Manage 105:248–255

    Article  CAS  Google Scholar 

  • Han X-M, Hu H-W, Chen Q-L, Yang L-Y, Li H-L, Zhu Y-G, Li X-Z, Ma Y-B (2018) Antibiotic resistance genes and associated bacterial communities in agricultural soils amended with different sources of animal manures. Soil Biol Biochem 126:91–102

    Article  CAS  Google Scholar 

  • Hardwick SA, Stokes H, Findlay S, Taylor M, Gillings MR (2008) Quantification of class 1 integron abundance in natural environments using real-time quantitative PCR. FEMS Microbiol Lett 278(2):207–212

    Article  CAS  Google Scholar 

  • Hu Y, Wang J, Shen Y (2020) Enhanced performance of anaerobic digestion of cephalosporin C fermentation residues by gamma irradiation-induced pretreatment. J Hazard Mater 384:121335

    Article  CAS  Google Scholar 

  • Hutinel M, Fick J, Larsson DGJ, Flach CF (2021) Investigating the effects of municipal and hospital wastewaters on horizontal gene transfer. Environ Pollut 276:116733

    Article  CAS  Google Scholar 

  • Li C, Wang R, Yang X, Zhou M, Pan X, Cai G, Zhang Y, Zhu G (2021) Deeper investigation on methane generation from synthetic wastewater containing oxytetracycline in a scale up acidic anaerobic baffled reactor. Bioresour Technol 333:125156

    Article  CAS  Google Scholar 

  • Li J, Yang H, Qin K, Wei L, Xia X, Zhu F, Tan X, Xue C, Zhao Q (2022a) Effect of pig manure-derived sulfadiazine on species distribution and bioactivities of soil ammonia-oxidizing microorganisms after fertilization. J Hazard Mater 423(Pt A):126994

    Article  CAS  Google Scholar 

  • Li N, Li X, Fan XY (2022b) Storage tank as a pretreatment unit for rainwater cleaner production: role of biofilm bacterial communities and functional genera in water quality improvement. J Environ Manage 303:114118

    Article  CAS  Google Scholar 

  • Liao H, Zhao Q, Cui P, Chen Z, Yu Z, Geisen S, Friman V-P, Zhou S (2019) Efficient reduction of antibiotic residues and associated resistance genes in tylosin antibiotic fermentation waste using hyperthermophilic composting. Environ Int 133:105203

    Article  CAS  Google Scholar 

  • Liu W, Ling N, Guo J, Ruan Y, Wang M, Shen Q, Guo S (2021) Dynamics of the antibiotic resistome in agricultural soils amended with different sources of animal manures over three consecutive years. J Hazard Mater 401:123399

    Article  CAS  Google Scholar 

  • Luan X, Han Z, Shen Y, Yang M, Zhang Y (2021) Assessing the effect of treated erythromycin fermentation residue on antibiotic resistome in soybean planting soil: in situ field study. Sci Total Environ 779:146329

    Article  CAS  Google Scholar 

  • Muurinen J, Stedtfeld R, Karkman A, Pärnänen K, Tiedje J, Virta M (2017) Influence of manure application on the environmental resistome under Finnish agricultural practice with restricted antibiotic use. Environ Sci Technol 51(11):5989–5999

    Article  CAS  Google Scholar 

  • Peng H, Zhang Q, Tan B, Li M, Zhang W, Feng J (2021) A metagenomic view of how different carbon sources enhance the aniline and simultaneous nitrogen removal capacities in the aniline degradation system. Bioresour Technol 335:125277

    Article  CAS  Google Scholar 

  • Popowska M, Rzeczycka M, Miernik A, Krawczyk-Balska A, Walsh F, Duffy B (2012) Influence of soil use on prevalence of tetracycline, streptomycin, and erythromycin resistance and associated resistance genes. Antimicrob Agents Ch 56(3):1434–1443

    Article  CAS  Google Scholar 

  • Qiu X, Zhou G, Wang H (2022) Nanoscale zero-valent iron inhibits the horizontal gene transfer of antibiotic resistance genes in chicken manure compost. J Hazard Mater 422:126883

    Article  CAS  Google Scholar 

  • Sandegren L (2014) Selection of antibiotic resistance at very low antibiotic concentrations. Ups J Med 119(2):103–107

    Article  Google Scholar 

  • Schafhauser BH, Kristofco LA, de Oliveira CMR, Brooks BW (2018) Global review and analysis of erythromycin in the environment: occurrence, bioaccumulation and antibiotic resistance hazards. Environ Pollut 238:440–451

    Article  CAS  Google Scholar 

  • Schlusener MP, Bester K (2006) Persistence of antibiotics such as macrolides, tiamulin and salinomycin in soil. Environ Pollut 143(3):565–571

    Article  Google Scholar 

  • Shen Y, Stedtfeld RD, Guo X, Bhalsod GD, Jeon S, Tiedje JM, Li H, Zhang W (2019) Pharmaceutical exposure changed antibiotic resistance genes and bacterial communities in soil-surface- and overhead-irrigated greenhouse lettuce. Environ Int 131:105031

    Article  CAS  Google Scholar 

  • Shi H, Bai C, Luo D, Wang W, Zhou C, Meharg AA, Yao L (2019) Degradation of tetracyclines in manure-amended soil and their uptake by litchi (Litchi chinensis Sonn.). Environ Sci Pollut Res 26(6):6209–6215

    Article  CAS  Google Scholar 

  • Song S, Jiang M, Yao J, Liu H, Dai X, Wang G (2020) Alkaline-thermal pretreatment of spectinomycin mycelial residues: insights on anaerobic biodegradability and the fate of antibiotic resistance genes. Chemosphere 261:127821

    Article  CAS  Google Scholar 

  • Wang B, Liu H, Cai C, Thabit M, Wang P, Li G, Duan Z (2016) Effect of dry mycelium of Penicillium chrysogenum fertilizer on soil microbial community composition, enzyme activities and snap bean growth. Environ Sci Pollut Res 23(20):20728–20738

    Article  CAS  Google Scholar 

  • Wang M, Xie X, Wang M, Wu J, Zhou Q, Sun Y (2020a) The bacterial microbiota in florfenicol contaminated soils: the antibiotic resistome and the nitrogen cycle. Environ Pollut 259:113901

    Article  CAS  Google Scholar 

  • Wang J, Long Z, Min W, Hou Z (2020b) Metagenomic analysis reveals the effects of cotton straw-derived biochar on soil nitrogen transformation in drip-irrigated cotton field. Environ Sci Pollut Res Int 27(35):43929–43941

    Article  CAS  Google Scholar 

  • Wang Y, Yuan Z, Tang Y (2021) Enhancing food security and environmental sustainability: a critical review of food loss and waste management. Resour Environ Sust 4:100023

    Google Scholar 

  • Wang P, Wu D, You X, Su Y, Xie B (2021b) Antibiotic and metal resistance genes are closely linked with nitrogen-processing functions in municipal solid waste landfills. J Hazard Mater 403:123689

    Article  CAS  Google Scholar 

  • Weber JM, Wierman C, Hutchinson CR (1985) Genetic analysis of erythromycin production in Streptomyces erythreus. J Bacteriol 164(1):425

    Article  CAS  Google Scholar 

  • Wright W, Schauer P, Huling R (1982) Utilization of industrial fermentation residues for turfgrass production. J Environ Qual 11(2):233–236

    Article  Google Scholar 

  • Wu X, Sun Y, Deng L, Meng Q, Jiang X, Bello A, Sheng S, Han Y, Zhu H, Xu X (2020) Insight to key diazotrophic community during composting of dairy manure with biochar and its role in nitrogen transformation. Waste Manag 105:190–197

    Article  CAS  Google Scholar 

  • Yi X, Wang M, Zhou Z (2019) The potential impact of naturally produced antibiotics, environmental factors, and anthropogenic pressure on the occurrence of erm genes in urban soils. Environ Pollut 245:282–289

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zhang MQ, Yuan L, Li ZH, Zhang HC, Sheng GP (2019a) Tetracycline exposure shifted microbial communities and enriched antibiotic resistance genes in the aerobic granular sludge. Environ Int 130:104902. https://doi.org/10.1016/j.envint.2019.06.012

  • Zhang QQ, Zhao YH, Wang CJ, Bai YH, Wu D, Wu J, Tian GM, Shi ML, Mahmood Q, Jin RC (2019b) Expression of the nirS, hzsA, and hdh genes and antibiotic resistance genes in response to recovery of anammox process inhibited by oxytetracycline. Sci Total Environ 681:56–65

    Article  CAS  Google Scholar 

  • Zhang Y, Liu H, Xin Y, Shen Y, Wang J, Cai C, Wang M (2019c) Erythromycin degradation and ERY-resistant gene inactivation in erythromycin mycelial dreg by heat-activated persulfate oxidation. Chem Eng J 358:1446–1453

    Article  CAS  Google Scholar 

  • Zhang Y, Liu H, Dai X, Cai C, Wang J, Wang M, Shen Y, Wang P (2020) Impact of application of heat-activated persulfate oxidation treated erythromycin fermentation residue as a soil amendment: Soil chemical properties and antibiotic resistance. Sci Total Environ 736:139668

    Article  CAS  Google Scholar 

  • Zhang X, Li S, Cheng W, Zhao Y, Cui H, Xie X, Wu J, Wei Z, Liu Y (2021) Oxytetracycline stress reconstruct the core microbial community related to nitrogen transformation during composting. Bioresour Technol 319:124142

    Article  CAS  Google Scholar 

Download references

Funding

This work is financially supported by the National Natural Science Foundation of China (grant number 51978497).

Author information

Authors and Affiliations

Authors

Contributions

Yanxiang Zhang: investigation, formal analysis, data curation, writing—original draft. Gang Wang: writing—review and editing. Xiaohu Dai: writing—review and editing. Huiling Liu: supervision, writing—review and editing.

Corresponding author

Correspondence to Huiling Liu.

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: Diane Purchase

Publisher's note

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

Highlights

• The application of spray-dried EFR as a soil amendment was investigated.

• ARG abundance was temporarily affected with the addition of 1.0% spray-dried EFR.

• N cycling genes were enriched following the application of 1.0% spray-dried EFR.

• Bacterial community presented temporary shifts as 1.0% spray-dried EFR amended.

• Negative correlations were found between ARGs and N cycling genes.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 399 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Y., Wang, G., Liu, H. et al. Application of spray-dried erythromycin fermentation residue as a soil amendment: antibiotic resistance genes, nitrogen cycling, and microbial community structure. Environ Sci Pollut Res 30, 20547–20557 (2023). https://doi.org/10.1007/s11356-022-23361-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-23361-6

Keywords

Navigation