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Deciphering and predicting changes in antibiotic resistance genes during pig manure aerobic composting via machine learning model

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Abstract

Livestock manure is one of the most important pools of antibiotic resistance genes (ARGs) in the environment. Aerobic composting can effectively reduce the spread of antibiotic resistance risk in livestock manure. Understanding the effect of aerobic composting process parameters on manure-sourced ARGs is important to control their spreading risk. In this study, the effects of process parameters on ARGs during aerobic composting of pig manure were explored through data mining based on 191 valid data collected from literature. Machine learning (ML) models (XGBoost and Random Forest) were utilized to predict the rate of ARGs changes during pig manure composting. The model evaluation index of the XGBoost model (R2 = 0.651) was higher than that of the Random Forest (R2 = 0.490), indicating that XGBoost had better prediction performance. Feature importance was further calculated for the XGBoost model, and the XGBoost black box model was interpreted by Shapley additive explanations analysis. Results indicated that the influencing factors on the ARGs variation in pig manure were sequentially divided into thermophilic period, total composting period, composting real time, and thermophilic stage average temperature. The findings gave an insight into the application of ML models to predict and decipher the ARG changes during manure composting and provided suggestions for better composting manipulation and optimization of process parameters.

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References

  • Awasthi SK, Duan Y, Liu T, Zhou Y, Qin S, Liu H, Varjani S, Awasthi MK, Zhang Z, Pandey A, Taherzadeh MJ (2021) Sequential presence of heavy metal resistant fungal communities influenced by biochar amendment in the poultry manure composting process. J Clean Prod 291:125947

    Article  CAS  Google Scholar 

  • Bao J, Wang X, Gu J, Dai X, Zhang K, Wang Q, Ma J, Peng H (2020) Effects of macroporous adsorption resin on antibiotic resistance genes and the bacterial community during composting. Bioresour Technol 295:121997

    Article  CAS  Google Scholar 

  • Cai R, Zhang S, Cui X, Xu C (2023) Reasonable water replenishment strategies can improve the fermentation efficiency and bacterial community of sheep manure composting on the Qinghai-Tibet Plateau. J Mater Cycles Waste Manage 25:1204–1215

    Article  Google Scholar 

  • Cao R, Wang J, Ben W, Qiang Z (2020) The profile of antibiotic resistance genes in pig manure composting shaped by composting stage: mesophilic-thermophilic and cooling-maturation stages. Chemosphere 250:126181

    Article  CAS  Google Scholar 

  • Chen Z, Bao H, Wen Q, Wu Y, Fu Q (2022a) Effects of H3PO4 modified biochar on heavy metal mobility and resistance genes removal during swine manure composting. Bioresour Technol 346:126632

    Article  CAS  Google Scholar 

  • Chen Z, Fu Q, Wen Q, Wu Y, Bao H, Guo J (2022b) Microbial community competition rather than high-temperature predominates ARGs elimination in swine manure composting. J Hazard Mater 423:127149

    Article  CAS  Google Scholar 

  • Dai X, Wang X, Gu J, Bao J, Wang J, Guo H, Yu J, Zhao W, Lei L (2021) Responses of bacterial communities and antibiotic resistance genes to nano-cellulose addition during pig manure composting. J Environ Manage 300:113734

  • Ding S, Huang W, Xu W, Wu Y, Zhao Y, Fang P, Hu B, Lou L (2022) Improving kitchen waste composting maturity by optimizing the processing parameters based on machine learning model. Bioresour Technol 360:127606

    Article  CAS  Google Scholar 

  • Duan M, Gu J, Wang X, Li Y, Zhang S, Zhang R (2018) Effects of genetically modified cotton stalks on antibiotic resistance genes, intI1, and intI2 during pig manure composting. Ecotoxicol Environ Saf 147:637–642

    Article  CAS  Google Scholar 

  • Guo H, Gu J, Wang X, Yu J, Nasir M, Peng H, Zhang R, Hu T, Wang Q, Ma J (2019) Responses of antibiotic and heavy metal resistance genes to bamboo charcoal and bamboo vinegar during aerobic composting. Environ Pollut 252:1097–1105

    Article  CAS  Google Scholar 

  • Guo W, Huang C, Xi B, Tang Z, Tan W, Li W, Zhang Y, Li W (2021) The maturity period is the main stage of antibiotic resistance genes reduction in aerobic composting process of swine manure in sub-scale farms. Bioresour Technol 319:124139

    Article  CAS  Google Scholar 

  • Haffiez N, Chung TH, Zakaria BS, Shahidi M, Mezbahuddin S, Maal Bared R, Dhar BR (2022) Exploration of machine learning algorithms for predicting the changes in abundance of antibiotic resistance genes in anaerobic digestion. Sci Total Environ 839:156211

    Article  CAS  Google Scholar 

  • Hermans SM, Buckley HL, Case BS, Curran Cournane F, Taylor M, Lear G (2020) Using soil bacterial communities to predict physico-chemical variables and soil quality. Microbiome 8(1):79

    Article  CAS  Google Scholar 

  • Hernandez Matheus A, Loschenbrand M, Berg K, Fuchs I, Aragues Penalba M, Bullich Massague E, Sumper A (2022) A systematic review of machine learning techniques related to local energy communities. Renew Sust Energ Rev 170:112651

    Article  Google Scholar 

  • Huang G, He X, Xiong J, Yang Z, Han L (2022) Exploring the impact of biochar on antibiotics and antibiotics resistance genes in pig manure aerobic composting through untargeted metabolomics and metagenomics. Bioresour Technol 352:127118

    Article  Google Scholar 

  • Huang Q, Chen G, Wang Y, Xu L, Chen WQ (2020) Identifying the socioeconomic drivers of solid waste recycling in China for the period 2005-2017. Sci Total Environ 725:138137

    Article  CAS  Google Scholar 

  • Huang X, Zheng J, Tian S, Liu C, Liu L, Wei L, Fan H, Zhang T, Wang L, Zhu G, Xu K (2019) Higher temperatures do not always achieve better antibiotic resistance gene removal in anaerobic digestion of swine manure. Appl Environ Microbiol 85(7):e02878–e02818

    Article  CAS  Google Scholar 

  • Kuppusamy S, Kakarla D, Venkateswarlu K, Megharaj M, Yoon YE, Lee YB (2018) Veterinary antibiotics (VAs) contamination as a global agro-ecological issue: A critical view. Agric Ecosyst Environ 257:47–59

    Article  CAS  Google Scholar 

  • Li H, Cheng W, Li B, Xu Y, Zheng X (2020) The fate of antibiotic resistance genes during co-composting of swine manure with cauliflower and corn straw. Bioresour Technol 300:122669

    Article  CAS  Google Scholar 

  • Li Y, Li S, Sun X, Hao D (2022) Prediction of carbon dioxide production from green waste composting and identification of critical factors using machine learning algorithms. Bioresour Technol 360:127587

    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(B):105203

    Article  CAS  Google Scholar 

  • Liu B, Yu K, Ahmed I, Gin K, Xi B, Wei Z, He Y, Zhang B (2021) Key factors driving the fate of antibiotic resistance genes and controlling strategies during aerobic composting of animal manure: a review. Sci Total Environ 791:148372

    Article  CAS  Google Scholar 

  • Liu YW, Cheng DM, Xue JM, Weaver L, Wakelin SA, Feng Y, Li ZJ (2020) Changes in microbial community structure during pig manure composting and its relationship to the fate of antibiotics and antibiotic resistance genes. J Hazard Mater 389:122082

    Article  CAS  Google Scholar 

  • Ma W, Wang L, Xu X, Huo M, Zhou K, Mi K, Tian X, Cheng G, Huang L (2022) Fate and exposure risk of florfenicol, thiamphenicol and antibiotic resistance genes during composting of swine manure. Sci Total Environ 839:156243

    Article  CAS  Google Scholar 

  • Pei M, Zhang B, He Y, Su J, Gin K, Lev O, Shen G, Hu S (2019) State of the art of tertiary treatment technologies for controlling antibiotic resistance in wastewater treatment plants. Environ Int 131:105026

    Article  CAS  Google Scholar 

  • Pence I, Kumas K, Siseci MC, Akyuz A (2023) Modeling of energy and emissions from animal manure using machine learning methods: the case of the Western Mediterranean Region, Turkey. Environ Sci Pollut Res 30:22631–22652

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Qian X, Gu J, Sun W, Wang X, Li H (2019) Effects of passivators on antibiotic resistance genes and related mechanisms during composting of copper-enriched pig manure. Sci Total Environ 674:383–391

    Article  CAS  Google Scholar 

  • Qian X, Gu J, Sun W, Wang XJ, Su JQ, Stedfeld R (2018) Diversity, abundance, and persistence of antibiotic resistance genes in various types of animal manure following industrial composting. J Hazard Mater 344:716–722

    Article  CAS  Google Scholar 

  • Qian X, Sun W, Gu J, Wang XJ, Zhang YJ, Duan ML, Li HC, Zhang RR (2016) Reducing antibiotic resistance genes, integrons, and pathogens in dairy manure by continuous thermophilic composting. Bioresour Technol 220:425–432

    Article  CAS  Google Scholar 

  • Ren JJ, Xu CB, Shen YP, Li CY, Dong LP, Huhe TL, Zhi JQ, Wang CQ, Jiang XM, Niu DZ (2023) Environmental factors induced macrolide resistance genes in composts consisting of erythromycin fermentation residue, cattle manure, and maize straw. Environ Sci Pollut Res 30:65119–65128

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Shan G, Liu J, Zhu B, Tan W, Li W, Tang Z, Hu X, Zhu L, Xi B (2023) Effect of hydrochar on antibiotic-resistance genes and relevant mechanisms during chicken manure composting. J Hazard Mater 454:131459

    Article  CAS  Google Scholar 

  • Song T, Zhu C, Xue S, Li B, Ye J, Geng B, Li L, Sarder MF, Li N, Feng S, Li H (2020) Comparative effects of different antibiotics on antibiotic resistance during swine manure. Bioresour Technol 315:123820

    Article  CAS  Google Scholar 

  • Sun X, Zhao J, Wang Q, Ren X, Li R, Awasthi MK, Zhang Z (2020) Behaviors and related mechanisms of Zn resistance and antibiotic resistance genes during co-composting of erythromycin manufacturing wastes and pig manure. Bioresour Technol 318:124048

    Article  CAS  Google Scholar 

  • Sun Y, Clarke B, Clarke J, Li X (2021) Predicting antibiotic resistance gene abundance in activated sludge using shotgun metagenomics and machine learning. Water Res 202:117384

    Article  CAS  Google Scholar 

  • Tong Z, Liu F, Sun B, Tian Y, Zhang J, Duan J, Bi W, Qin J, Xu S (2023) Effect of biochars with different particle sizes on fates of antibiotics and antibiotic resistance genes during composting of swine manure. Bioresour Technol 370:128542

    Article  CAS  Google Scholar 

  • Wan X, Li J, Xie L, Wei Z, Wu J, Tong YW, Wang X, He Y, Zhang J (2022) Machine learning framework for intelligent prediction of compost maturity towards automation of food waste composting system. Bioresour Technol 365:128107

    Article  CAS  Google Scholar 

  • Wang G, Kong Y, Yang Y, Ma R, Li L, Li G, Yuan J (2022) Composting temperature directly affects the removal of antibiotic resistance genes and mobile genetic elements in livestock manure. Environ Pollut 303:119174

    Article  CAS  Google Scholar 

  • Wang J, Ben W, Zhang Y, Yang M, Qiang Z (2015) Effects of thermophilic composting on oxytetracycline, sulfamethazine, and their corresponding resistance genes in swine manure. Environ Sci Process Impacts 17:1654–1660

    Article  Google Scholar 

  • Wang J, Gu J, Wang X, Song Z, Dai X, Guo H, Yu J, Zhao W, Lei L (2021) Enhanced removal of antibiotic resistance genes and mobile genetic elements during swine manure composting inoculated with mature compost. J Hazard Mater 411:125135

    Article  CAS  Google Scholar 

  • Wang R, Zhang J, Sui Q, Wan H, Tong J, Chen M, Wei Y, Wei D (2016) Effect of red mud addition on tetracycline and copper resistance genes and microbial community during the full scale swine manure composting. Bioresour Technol 216:1049–1057

    Article  CAS  Google Scholar 

  • Wu N, Xie S, Zeng M, Xu X, Li Y, Liu X, Wang X (2020) Impacts of pile temperature on antibiotic resistance, metal resistance and microbial community during swine manure composting. Sci Total Environ 744:140920

    Article  CAS  Google Scholar 

  • Wu S, Shen Z, Yang C, Zhou Y, Li X, Zeng G, Ai S, He H (2017) Effects of C/N ratio and bulking agent on speciation of Zn and Cu and enzymatic activity during pig manure composting. Int Biodeterior Biodegrad 119:429–436

    Article  CAS  Google Scholar 

  • Wu Y, Wen Q, Chen Z, Fu Q, Bao H (2022) Response of antibiotic resistance to the co-exposure of sulfamethoxazole and copper during swine manure composting. Sci Total Environ 805:150086

    Article  CAS  Google Scholar 

  • Xiao R, Awasthi MK, Li R, Park J, Pensky SM, Wang Q, Wang JJ, Zhang Z (2017) Recent developments in biochar utilization as an additive in organic solid waste composting: a review. Bioresour Technol 246:203–213

    Article  CAS  Google Scholar 

  • Xu X, Ma W, Zhou K, An B, Huo M, Lin X, Wang L, Wang H, Liu Z, Cheng G, Huang L (2022) Effects of composting on the fate of doxycycline, microbial community, and antibiotic resistance genes in swine manure and broiler manure. Sci Total Environ 832:155039

    Article  CAS  Google Scholar 

  • Zhang L, Gu J, Wang X, Sun W, Yin Y, Sun Y, Guo A, Tuo X (2017) Behavior of antibiotic resistance genes during co-composting of swine manure with Chinese medicinal herbal residues. Bioresour Technol 244:252–260

    Article  CAS  Google Scholar 

  • Zhang R, Gu J, Wang X, Li Y, Zhang K, Yin Y, Zhang X (2018) Contributions of the microbial community and environmental variables to antibiotic resistance genes during co-composting with swine manure and cotton stalks. J Hazard Mater 358:82–91

    Article  CAS  Google Scholar 

  • Zhang T, Yang Y, Pruden A (2015) Effect of temperature on removal of antibiotic resistance genes by anaerobic digestion of activated sludge revealed by metagenomic approach. Appl Microbiol Biotechnol 99:7771–7779

    Article  CAS  Google Scholar 

  • Zhang Y, Cheng D, Xie J, Zhang Y, Wan Y, Zhang Y, Shi X (2022) Impacts of farmland application of antibiotic-contaminated manures on the occurrence of antibiotic residues and antibiotic resistance genes in soil: a meta-analysis study. Chemosphere 300:137050

    Article  Google Scholar 

  • Zhong R, Salehi C, Johnson R (2022) Machine learning for drilling applications: a review. J Nat Gas Sci Eng 108:104807

    Article  Google Scholar 

  • Zhou G, Qiu X, Wu X, Lu S (2021) Horizontal gene transfer is a key determinant of antibiotic resistance genes profiles during chicken manure composting with the addition of biochar and zeolite. J Hazard Mater 408:124883

    Article  CAS  Google Scholar 

  • Zhou Z, Song Z, Gu J, Wang X, Hu T, Guo H, Xie J, Lei L, Ding Q, Jiang H, Xu L (2022) Dynamics and key drivers of antibiotic resistance genes during aerobic composting amended with plant-derived and animal manure-derived biochars. Bioresour Technol 355:127236

    Article  CAS  Google Scholar 

  • Zhu P, Qin H, Zhang H, Luo Y, Ru Y, Li J, San KW, Wang L, Yu X, Guo W (2021) Variations in antibiotic resistance genes and removal mechanisms induced by C/N ratio of substrate during composting. Sci Total Environ 798:149288

    Article  CAS  Google Scholar 

  • Zhu P, Wu Y, Ru Y, Hou Y, San KW, Yu X, Guo W (2022) Industrial-scale aerobic composting of livestock manures with the addition of biochar: variation of bacterial community and antibiotic resistance genes caused by various composting stages. Environ Pollut 314:120270

    Article  CAS  Google Scholar 

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Funding

This work was supported by Open Fund of Key Laboratory of Smart Breeding (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs (2023-TJAUKLSBF-2202), Tianjin Science and Technology Plan Project (23ZYCGSN00050), Tianjin Modern Agricultural Technology System Innovation (ITTPRS2021010), and Scientific Research Project of Tianjin Education Commission (2022KJ021, 2023KJ003).

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Authors and Affiliations

  1. Key Laboratory of Smart Breeding (Co-construction by Ministry and Province) of Ministry of Agriculture and Rural Affairs, Tianjin Agricultural University, Tianjin, 300392, China

    Xiaohui Yu, Qing Wang, Zhiqiang Wang, Nan Wu, Xiaobo Wang & Xiaoyan Xu

  2. College of Engineering and Technology, Tianjin Agricultural University, Tianjin, 300392, China

    Xiaohui Yu, Yang Lv, Qing Wang, Zhiqiang Wang, Nan Wu & Xinyuan Liu

  3. College of Chemical Engineering and Material Science, Tianjin University of Science & Technology, Tianjin, 300457, China

    Wenhao Wang

  4. College of Agronomy and Resource and Environment, Tianjin Agricultural University, Tianjin, 300392, China

    Xiaobo Wang & Xiaoyan Xu

Authors
  1. Xiaohui Yu
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  2. Yang Lv
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  3. Qing Wang
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  4. Wenhao Wang
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  5. Zhiqiang Wang
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  6. Nan Wu
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  7. Xinyuan Liu
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  8. Xiaobo Wang
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  9. Xiaoyan Xu
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Contributions

Xiaohui Yu: conceptualization, methodology, data curation, writing — original draft. Yang Lv: formal analysis. Qing Wang: data curation. Wenhao Wang: methodology. Zhiqiang Wang: formal analysis. Nan Wu: conceptualization, supervision, writing — review and editing. Xinyuan Liu: writing — review and editing. Xiaobo Wang: writing — review and editing. Xiaoyan Xu: funding acquisition.

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Correspondence to Nan Wu.

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Yu, X., Lv, Y., Wang, Q. et al. Deciphering and predicting changes in antibiotic resistance genes during pig manure aerobic composting via machine learning model. Environ Sci Pollut Res (2024). https://doi.org/10.1007/s11356-024-33087-2

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