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Here, we conducted a 366-day soil microcosm experiment in which agricultural soils were exposed to single and combined heavy metal and polycyclic aromatic hydrocarbon (PAH) contamination, with metagenomic profiling across 12 time points. Relative to initial levels, ARG relative abundance across pollution treatments increased by an average of 23% by day 114 and reached 62% above baseline by day 254, after which it stabilized through day 366. These temporal patterns were associated with shifts in the correlates of ARG variation across biological scales: early-stage ARG variation was primarily associated with bacterial community composition, middle-stage variation was most strongly associated with mobile genetic element (MGE) abundance and mobility-related signals, and late-stage variation was more consistently associated with tolerance-related functional traits. Genome-resolved analyses further revealed stronger microdiversity signals from the middle stage onward, and these stage-associated ecological and molecular patterns were generally more pronounced under combined pollution than under single-pollutant exposure. Taken together, these findings indicate a stage-dependent pattern of ARG dynamics under long-term pollutant exposure and provide a temporal framework for understanding long-term resistome reorganization in polluted agricultural soils.<\/jats:p>","DOI":"10.1021\/acs.est.6c06561","type":"journal-article","created":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T13:01:24Z","timestamp":1789045284000},"page":"26197-26212","source":"Crossref","is-referenced-by-count":0,"title":["Stage-Dependent\nDynamics of Soil Antibiotic Resistance\nGenes under Long-Term Pollutant Exposure"],"prefix":"10.1021","volume":"60","author":[{"given":"Tian-Lun","family":"Zhang","sequence":"first","affiliation":[{"name":"Institute of Urban Environment, Chinese Academy of Sciences , , ,","place":["Xiamen, China, 361021"]},{"name":"University of Chinese Academy of Sciences , ,","place":["Beijing, China, 100049"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shao-Yang","family":"Zhang","sequence":"additional","affiliation":[{"name":"Institute of Urban Environment, Chinese Academy of Sciences , , ,","place":["Xiamen, China, 361021"]},{"name":"University of Chinese Academy of Sciences , ,","place":["Beijing, China, 100049"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuai","family":"Du","sequence":"additional","affiliation":[{"name":"Institute of Urban Environment, Chinese Academy of Sciences , , ,","place":["Xiamen, China, 361021"]},{"name":"CAS Haixi Industrial Technology Innovation Center , , ,","place":["Ningbo, China, 315830"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jun-Jie","family":"Zhu","sequence":"additional","affiliation":[{"name":"Xi\u2019an Jiaotong-Liverpool University , , ,","place":["Suzhou, China, 215123"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jia-Yang","family":"Xu","sequence":"additional","affiliation":[{"name":"Institute of Urban Environment, Chinese Academy of Sciences , , ,","place":["Xiamen, China, 361021"]},{"name":"University of Chinese Academy of Sciences , ,","place":["Beijing, China, 100049"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jun-Wei","family":"Peng","sequence":"additional","affiliation":[{"name":"Institute of Urban Environment, Chinese Academy of Sciences , , ,","place":["Xiamen, China, 361021"]},{"name":"CAS Haixi Industrial Technology Innovation Center , , ,","place":["Ningbo, China, 315830"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bang","family":"Ni","sequence":"additional","affiliation":[{"name":"Institute of Urban Environment, Chinese Academy of Sciences , , ,","place":["Xiamen, China, 361021"]},{"name":"CAS Haixi Industrial Technology Innovation Center , , ,","place":["Ningbo, China, 315830"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Da","family":"Lin","sequence":"additional","affiliation":[{"name":"Institute of Urban Environment, Chinese Academy of Sciences , , ,","place":["Xiamen, China, 361021"]},{"name":"University of Chinese Academy of Sciences , ,","place":["Beijing, China, 100049"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4183-8160","authenticated-orcid":true,"given":"Zhu-Gen","family":"Yang","sequence":"additional","affiliation":[{"name":"Cranfield University , , , ,","place":["Cranfield, Bedfordshire, U.K., MK43 0AL"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ni","family":"Ni","sequence":"additional","affiliation":[{"name":"Ministry of Ecology and Environment of the People\u2019s Republic of China , , ,","place":["Nanjing, China, 210042"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9617-0300","authenticated-orcid":true,"given":"Na","family":"Wang","sequence":"additional","affiliation":[{"name":"Ministry of Ecology and Environment of the People\u2019s Republic of China , , ,","place":["Nanjing, China, 210042"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi-Yue","family":"Zhang","sequence":"additional","affiliation":[{"name":"Institute of Urban Environment, Chinese Academy of Sciences , , ,","place":["Xiamen, China, 361021"]},{"name":"CAS Haixi Industrial Technology Innovation Center , , ,","place":["Ningbo, China, 315830"]},{"name":"Institute of Urban Environment, Chinese Academy of Sciences , , ,","place":["Xiamen, China, 361021"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0826-6423","authenticated-orcid":true,"given":"Dong","family":"Zhu","sequence":"additional","affiliation":[{"name":"Institute of Urban Environment, Chinese Academy of Sciences , , ,","place":["Xiamen, China, 361021"]},{"name":"University of Chinese Academy of Sciences , ,","place":["Beijing, China, 100049"]},{"name":"CAS Haixi Industrial Technology Innovation Center , , ,","place":["Ningbo, China, 315830"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3861-8482","authenticated-orcid":true,"given":"Yong-Guan","family":"Zhu","sequence":"additional","affiliation":[{"name":"Institute of Urban Environment, Chinese Academy of Sciences , , ,","place":["Xiamen, China, 361021"]},{"name":"University of Chinese Academy of Sciences , ,","place":["Beijing, China, 100049"]},{"name":"Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences , , ,","place":["Beijing, China, 100085"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,9,10]]},"reference":[{"key":"2026092210095505200_cit1","doi-asserted-by":"publisher","first-page":"105059","DOI":"10.1016\/j.envint.2019.105059","article-title":"Soil biota, antimicrobial\nresistance and planetary health","volume":"131","author":"Zhu","year":"2019","journal-title":"Environ. Int."},{"issue":"6","key":"2026092210095505200_cit2","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1038\/s41893-019-0293-3","article-title":"Emerging\nhuman infectious diseases and the\nlinks to global food production","volume":"2","author":"Rohr","year":"2019","journal-title":"Nat. Sustainable"},{"key":"2026092210095505200_cit3","doi-asserted-by":"publisher","first-page":"5168","DOI":"10.1038\/s41467-024-49165-5","article-title":"Organic fertilization\nco-selects\ngenetically linked antibiotic and metal(loid) resistance genes in\nglobal soil microbiome","volume":"15","author":"Liu","year":"2024","journal-title":"Nat. Commun."},{"key":"2026092210095505200_cit4","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1186\/s40168-022-01405-w","article-title":"The global distribution\nand environmental drivers of\nthe soil antibiotic resistome","volume":"10","author":"Delgado-Baquerizo","year":"2022","journal-title":"Microbiome"},{"key":"2026092210095505200_cit5","doi-asserted-by":"publisher","first-page":"109362","DOI":"10.1016\/j.soilbio.2024.109362","article-title":"The effects\nof cadmium-copper\nstress on the accumulation of antibiotic-resistance genes in soil\nand pakchoi leaves","volume":"191","author":"Pan","year":"2024","journal-title":"Soil Biol. Biochem."},{"key":"2026092210095505200_cit6","doi-asserted-by":"publisher","first-page":"121216","DOI":"10.1016\/j.jhazmat.2019.121216","article-title":"Profiles of\nantibiotic resistome with animal manure application in black soils\nof northeast China","volume":"384","author":"Li","year":"2020","journal-title":"J. Hazard. Mater."},{"issue":"9","key":"2026092210095505200_cit7","doi-asserted-by":"publisher","first-page":"3435","DOI":"10.1073\/pnas.1222743110","article-title":"Diverse and abundant\nantibiotic resistance genes in Chinese swine farms","volume":"110","author":"Zhu","year":"2013","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2026092210095505200_cit8","doi-asserted-by":"publisher","first-page":"1005","DOI":"10.1016\/j.envpol.2016.11.047","article-title":"Polycyclic\naromatic hydrocarbons (PAHs) enriching antibiotic resistance genes\n(ARGs) in the soils","volume":"220","author":"Chen","year":"2017","journal-title":"Environ. Pollut."},{"key":"2026092210095505200_cit9","doi-asserted-by":"publisher","first-page":"132952","DOI":"10.1016\/j.jhazmat.2023.132952","article-title":"The pH-specific response\nof soil resistome to triclocarban and arsenic\nco-contamination","volume":"464","author":"Wang","year":"2024","journal-title":"J. Hazard. Mater."},{"key":"2026092210095505200_cit10","doi-asserted-by":"publisher","first-page":"136372","DOI":"10.1016\/j.jhazmat.2024.136372","article-title":"Impacts of\nsoil type on the temporal dynamics of antibiotic resistance gene profiles\nfollowing application of composted manure","volume":"480","author":"Song","year":"2024","journal-title":"J.\nHazard. Mater."},{"issue":"13","key":"2026092210095505200_cit11","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2535653123","article-title":"Phages drive the dissemination of antibiotic resistance\ngenes by facilitating host adaptation to heavy metal stress","volume":"123","author":"Shen","year":"2026","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2026092210095505200_cit12","doi-asserted-by":"publisher","first-page":"133335","DOI":"10.1016\/j.jhazmat.2023.133335","article-title":"Effects of\nheavy metal and disinfectant on antibiotic resistance genes and virulence\nfactor genes in the plastisphere from diverse soil ecosystems","volume":"465","author":"Ni","year":"2024","journal-title":"J. Hazard. Mater."},{"issue":"1","key":"2026092210095505200_cit13","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1038\/s44259-024-00026-7","article-title":"Co-selection for antibiotic resistance\nby environmental contaminants","volume":"2","author":"Murray","year":"2024","journal-title":"Npj Antimicrob.\nResist."},{"key":"2026092210095505200_cit14","doi-asserted-by":"publisher","first-page":"108318","DOI":"10.1016\/j.envint.2023.108318","article-title":"Key taxa and\nmobilome-mediated responses co-reshape the soil antibiotic resistome\nunder dazomet fumigation stress","volume":"182","author":"Zhang","year":"2023","journal-title":"Environ. Int."},{"key":"2026092210095505200_cit15","doi-asserted-by":"publisher","first-page":"137398","DOI":"10.1016\/j.jhazmat.2025.137398","article-title":"Microcosm experiments\ndeciphered resistome coalescence, risks and source-sink relationship\nof antibiotic resistance in the soil irrigated with reclaimed water","volume":"488","author":"Liu","year":"2025","journal-title":"J. Hazard. Mater."},{"key":"2026092210095505200_cit16","doi-asserted-by":"publisher","first-page":"136587","DOI":"10.1016\/j.jhazmat.2024.136587","article-title":"Significant effects of bioavailable\nheavy metals on antibiotic resistome in paddy soils as revealed by\nmetagenomic analysis","volume":"482","author":"Hou","year":"2025","journal-title":"J. Hazard. Mater."},{"issue":"7502","key":"2026092210095505200_cit17","doi-asserted-by":"publisher","first-page":"612","DOI":"10.1038\/nature13377","article-title":"Bacterial phylogeny\nstructures soil\nresistomes across habitats","volume":"509","author":"Forsberg","year":"2014","journal-title":"Nature"},{"issue":"12","key":"2026092210095505200_cit18","doi-asserted-by":"publisher","first-page":"2182","DOI":"10.1038\/s41396-023-01524-8","article-title":"Protistan predation selects for antibiotic resistance in soil bacterial\ncommunities","volume":"17","author":"Nguyen","year":"2023","journal-title":"ISME J."},{"issue":"10","key":"2026092210095505200_cit19","doi-asserted-by":"publisher","first-page":"2969","DOI":"10.1038\/s41396-021-00980-4","article-title":"Chlorine disinfection\nfacilitates\nnatural transformation through ROS-mediated oxidative stress","volume":"15","author":"Zhang","year":"2021","journal-title":"ISME J."},{"issue":"1","key":"2026092210095505200_cit20","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1186\/s40168-022-01314-y","article-title":"Non-antibiotic pharmaceuticals\npromote conjugative plasmid transfer at a community-wide level","volume":"10","author":"Wang","year":"2022","journal-title":"Microbiome"},{"issue":"4","key":"2026092210095505200_cit21","doi-asserted-by":"publisher","DOI":"10.1093\/femsre\/fuae017","article-title":"Unravelling the\nmechanisms of antibiotic and heavy\nmetal resistance co-selection in environmental bacteria","volume":"48","author":"Gillieatt","year":"2024","journal-title":"FEMS Microbiol. Rev."},{"issue":"8","key":"2026092210095505200_cit22","doi-asserted-by":"publisher","first-page":"2179","DOI":"10.1038\/s41396-020-0679-2","article-title":"Non-antibiotic pharmaceuticals\nenhance the transmission of exogenous antibiotic resistance genes\nthrough bacterial transformation","volume":"14","author":"Wang","year":"2020","journal-title":"ISME J."},{"issue":"8","key":"2026092210095505200_cit23","doi-asserted-by":"publisher","first-page":"1512","DOI":"10.1038\/s41559-025-02740-5","article-title":"Climate warming fuels the global antibiotic resistome by altering\nsoil bacterial traits","volume":"9","author":"Lin","year":"2025","journal-title":"Nat. Ecol. Evol."},{"issue":"1","key":"2026092210095505200_cit24","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1016\/j.gpb.2018.12.003","article-title":"Antibiotic treatment\ndrives the diversification of\nthe human gut resistome","volume":"17","author":"Li","year":"2019","journal-title":"Genomics, Proteomics\nBioinf."},{"issue":"1","key":"2026092210095505200_cit25","doi-asserted-by":"publisher","first-page":"9788","DOI":"10.1038\/s41467-024-54237-7","article-title":"Microplastic diversity increases\nthe abundance of antibiotic resistance\ngenes in soil","volume":"15","author":"Wang","year":"2024","journal-title":"Nat. Commun."},{"issue":"7","key":"2026092210095505200_cit26","doi-asserted-by":"publisher","first-page":"1834","DOI":"10.1038\/s41396-020-0655-x","article-title":"Soil bacterial populations are shaped by recombination\nand gene-specific selection across a grassland meadow","volume":"14","author":"Crits-Christoph","year":"2020","journal-title":"ISME J."},{"issue":"2","key":"2026092210095505200_cit27","doi-asserted-by":"publisher","first-page":"250301","DOI":"10.1007\/s42832-025-0301-7","article-title":"Land-use types\nimpact\nsoil ecosystem functions by altering the soil multitrophic biodiversity\nand interactions","volume":"7","author":"Zhang","year":"2025","journal-title":"Soil Ecol. Lett."},{"issue":"10","key":"2026092210095505200_cit28","doi-asserted-by":"publisher","first-page":"1674","DOI":"10.1093\/bioinformatics\/btv033","article-title":"MEGAHIT:\nan ultra-fast single-node solution for large and complex metagenomics\nassembly via succinct de Bruijn graph","volume":"31","author":"Li","year":"2015","journal-title":"Bioinformatics"},{"key":"2026092210095505200_cit29","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1186\/1471-2105-11-119","article-title":"Prodigal: prokaryotic gene recognition and translation\ninitiation site identification","volume":"11","author":"Hyatt","year":"2010","journal-title":"BMC Bioinf."},{"issue":"5","key":"2026092210095505200_cit30","doi-asserted-by":"publisher","first-page":"555","DOI":"10.1038\/s41587-020-00777-4","article-title":"Improved metagenome\nbinning and assembly using deep\nvariational autoencoders","volume":"39","author":"Nissen","year":"2021","journal-title":"Nat. Biotechnol."},{"issue":"7","key":"2026092210095505200_cit31","doi-asserted-by":"publisher","first-page":"1043","DOI":"10.1101\/gr.186072.114","article-title":"CheckM: assessing the quality of\nmicrobial genomes\nrecovered from isolates, single cells, and metagenomes","volume":"25","author":"Parks","year":"2015","journal-title":"Genome Res."},{"issue":"23","key":"2026092210095505200_cit32","doi-asserted-by":"publisher","first-page":"3150","DOI":"10.1093\/bioinformatics\/bts565","article-title":"CD-HIT:\naccelerated for clustering the next-generation sequencing data","volume":"28","author":"Fu","year":"2012","journal-title":"Bioinformatics"},{"issue":"23","key":"2026092210095505200_cit33","doi-asserted-by":"publisher","first-page":"5315","DOI":"10.1093\/bioinformatics\/btac672","article-title":"GTDB-Tk v2: memory\nfriendly classification with the genome taxonomy database","volume":"38","author":"Chaumeil","year":"2022","journal-title":"Bioinformatics"},{"issue":"12","key":"2026092210095505200_cit34","doi-asserted-by":"publisher","first-page":"5825","DOI":"10.1093\/molbev\/msab293","article-title":"eggNOG-mapper\nv2: Functional Annotation, Orthology\nAssignments, and Domain Prediction at the Metagenomic Scale","volume":"38","author":"Cantalapiedra","year":"2021","journal-title":"Mol. Biol. Evol."},{"issue":"13","key":"2026092210095505200_cit35","doi-asserted-by":"publisher","first-page":"2263","DOI":"10.1093\/bioinformatics\/bty053","article-title":"ARGs-OAP v2.0 with\nan expanded SARG database and Hidden Markov Models for enhancement\ncharacterization and quantification of antibiotic resistance genes\nin environmental metagenomes","volume":"34","author":"Yin","year":"2018","journal-title":"Bioinformatics"},{"issue":"18","key":"2026092210095505200_cit36","doi-asserted-by":"publisher","DOI":"10.1128\/aem.00991-22","article-title":"mobileOG-db: a Manually Curated Database\nof Protein Families Mediating the Life Cycle of Bacterial Mobile Genetic\nElements","volume":"88","author":"Brown","year":"2022","journal-title":"Appl. Environ. Microbiol."},{"issue":"1","key":"2026092210095505200_cit37","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1038\/nmeth.3176","article-title":"Fast and sensitive\nprotein alignment using DIAMOND","volume":"12","author":"Buchfink","year":"2015","journal-title":"Nat. Meth."},{"issue":"4","key":"2026092210095505200_cit38","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast gapped-read\nalignment with Bowtie 2","volume":"9","author":"Langmead","year":"2012","journal-title":"Nat. Meth."},{"issue":"2","key":"2026092210095505200_cit39","doi-asserted-by":"publisher","DOI":"10.1093\/gigascience\/giab008","article-title":"Twelve\nyears of SAMtools and BCFtools","volume":"10","author":"Danecek","year":"2021","journal-title":"Gigascience"},{"issue":"6","key":"2026092210095505200_cit40","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkx1321","article-title":"PlasFlow:\npredicting plasmid sequences\nin metagenomic data using genome signatures","volume":"46","author":"Krawczyk","year":"2018","journal-title":"Nucleic Acids Res."},{"issue":"6","key":"2026092210095505200_cit41","doi-asserted-by":"publisher","first-page":"727","DOI":"10.1038\/s41587-020-00797-0","article-title":"inStrain\nprofiles population microdiversity from metagenomic\ndata and sensitively detects shared microbial strains","volume":"39","author":"Olm","year":"2021","journal-title":"Nat. Biotechnol."},{"key":"2026092210095505200_cit42","unstructured":"Harrell, F. E., Jr.\n          \n          Hmisc: Harrell Miscellaneous. R package version\n4.2-0, 2019."},{"key":"2026092210095505200_cit43","first-page":"1","article-title":"The igraph software","volume":"1695","author":"Csardi","year":"2006","journal-title":"Complex\nSyst."},{"issue":"6","key":"2026092210095505200_cit44","doi-asserted-by":"publisher","first-page":"927","DOI":"10.1111\/j.1654-1103.2003.tb02228.x","article-title":"VEGAN, a package\nof R functions for community ecology","volume":"14","author":"Dixon","year":"2003","journal-title":"J. Veg\nSci."},{"issue":"3","key":"2026092210095505200_cit45","first-page":"18","article-title":"Classification and\nregression by randomForest","volume":"2","author":"Liaw","year":"2002","journal-title":"R News"},{"key":"2026092210095505200_cit46","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1007\/978-3-319-24277-4_9","article-title":"Data analysis","volume-title":"ggplot2: elegant graphics for data analysis","author":"Wickham","year":"2016"},{"issue":"1","key":"2026092210095505200_cit47","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1038\/s43705-021-00018-y","article-title":"Seasonal change\nis a major driver of soil resistomes at a watershed scale","volume":"1","author":"Xiang","year":"2021","journal-title":"ISME Commun."},{"issue":"21","key":"2026092210095505200_cit48","doi-asserted-by":"publisher","first-page":"15054","DOI":"10.1021\/acs.est.2c04730","article-title":"Short-term benzalkonium\nchloride (C12) exposure induced the occurrence of wide-spectrum antibiotic\nresistance in agricultural soils","volume":"56","author":"Zeng","year":"2022","journal-title":"Environ. Sci.\nTechnol."},{"issue":"1","key":"2026092210095505200_cit49","doi-asserted-by":"publisher","first-page":"10034","DOI":"10.1038\/s41467-024-54459-9","article-title":"Evidence of horizontal\ngene transfer and environmental selection impacting antibiotic resistance\nevolution in soil-dwelling Listeria","volume":"15","author":"Goh","year":"2024","journal-title":"Nat. Commun."},{"key":"2026092210095505200_cit50","doi-asserted-by":"publisher","first-page":"108110","DOI":"10.1016\/j.soilbio.2020.108110","article-title":"Amazon deforestation enriches antibiotic resistance\ngenes","volume":"153","author":"Lemos","year":"2021","journal-title":"Soil Biol. 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