Decade-long warming accelerates antibiotic resistance in grassland soils
Wang, F. et al. Antibiotic resistance in the soil ecosystem: a One Health perspective. Curr. Opin. Environ. Sci. Health 20, 100230 (2021).Article
Google Scholar
Zheng, D. et al. Global biogeography and projection of soil antibiotic resistance genes. Sci. Adv. 8, eabq8015 (2022).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Bahram, M. et al. Structure and function of the global topsoil microbiome. Nature 560, 233–237 (2018).Article
ADS
CAS
PubMed
Google Scholar
Liu, C. et al. Protist predation promotes antimicrobial resistance spread through antagonistic microbiome interactions. ISME J. 18, wrae169 (2024).Article
CAS
PubMed
PubMed Central
Google Scholar
Nguyen, T. B.-A. et al. Protistan predation selects for antibiotic resistance in soil bacterial communities. ISME J. 17, 2182–2189 (2023).Article
CAS
PubMed
PubMed Central
Google Scholar
Wang, Y.-F. et al. Microplastic diversity increases the abundance of antibiotic resistance genes in soil. Nat. Commun. 15, 9788 (2024).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Guo, X. et al. Climate warming leads to divergent succession of grassland microbial communities. Nat. Clim. Change 8, 813–818 (2018).Article
ADS
Google Scholar
Rillig, M. C. et al. The role of multiple global change factors in driving soil functions and microbial biodiversity. Science 366, 886–890 (2019).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Yuan, M. M. et al. Climate warming enhances microbial network complexity and stability. Nat. Clim. Change 11, 343–348 (2021).Article
ADS
Google Scholar
Zhou, J. et al. Microbial mediation of carbon-cycle feedbacks to climate warming. Nat. Clim. Change 2, 106–110 (2012).Article
ADS
CAS
Google Scholar
Holmes, A. H. et al. Understanding the mechanisms and drivers of antimicrobial resistance. Lancet 387, 176–187 (2016).Article
CAS
PubMed
Google Scholar
Nathan, C. & Cars, O. Antibiotic resistance—problems, progress, and prospects. N. Engl. J. Med. 371, 1761–1763 (2014).Article
PubMed
Google Scholar
O’Neill, J. Tackling Drug-resistant Infections Globally: Final Report and Recommendations (Review on Antimicrobial Resistance, 2016).Larsson, D. & Flach, C.-F. Antibiotic resistance in the environment. Nat. Rev. Microbiol. 20, 257–269 (2022).Article
CAS
PubMed
Google Scholar
Ellabaan, M. M., Munck, C., Porse, A., Imamovic, L. & Sommer, M. O. Forecasting the dissemination of antibiotic resistance genes across bacterial genomes. Nat. Commun. 12, 2435 (2021).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Tang, X. et al. Effects of long-term manure applications on the occurrence of antibiotics and antibiotic resistance genes (ARGs) in paddy soils: evidence from four field experiments in south of China. Soil Biol. Biochem. 90, 179–187 (2015).Article
CAS
Google Scholar
Pan, M. & Chu, L. Occurrence of antibiotics and antibiotic resistance genes in soils from wastewater irrigation areas in the Pearl River Delta region, southern China. Sci. Total Environ. 624, 145–152 (2018).Article
ADS
CAS
PubMed
Google Scholar
Zhu, Y.-G. et al. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc. Natl Acad. Sci. USA 110, 3435–3440 (2013).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Jutkina, J., Marathe, N., Flach, C.-F. & Larsson, D. Antibiotics and common antibacterial biocides stimulate horizontal transfer of resistance at low concentrations. Sci. Total Environ. 616, 172–178 (2018).Article
ADS
PubMed
Google Scholar
Imran, M., Das, K. R. & Naik, M. M. Co-selection of multi-antibiotic resistance in bacterial pathogens in metal and microplastic contaminated environments: an emerging health threat. Chemosphere 215, 846–857 (2019).Article
ADS
CAS
PubMed
Google Scholar
Tiedje, J. M. et al. Microbes and climate change: a research prospectus for the future. mBio 13, e00800-22 (2022).Article
PubMed
PubMed Central
Google Scholar
IPCC Climate Change 2023: Synthesis Report (eds Core Writing Team, Lee, H. & Romero, J.) (Cambridge Univ. Press, 2023).Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).Article
Google Scholar
Guerra, C. A. et al. Global hotspots for soil nature conservation. Nature 610, 693–698 (2022).Article
ADS
CAS
PubMed
Google Scholar
Zhou, J. et al. Temperature mediates continental-scale diversity of microbes in forest soils. Nat. Commun. 7, 12083 (2016).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Wu, L. et al. Reduction of microbial diversity in grassland soil is driven by long-term climate warming. Nat. Microbiol. 7, 1054–1062 (2022).Article
CAS
PubMed
Google Scholar
Guo, X. et al. Climate warming accelerates temporal scaling of grassland soil microbial biodiversity. Nat. Ecol. Evol. 3, 612–619 (2019).Article
PubMed
Google Scholar
Xue, K. et al. Annual removal of aboveground plant biomass alters soil microbial responses to warming. mBio 7, e00976-16 (2016).Article
PubMed
PubMed Central
Google Scholar
Delnat, V., Verborgt, J., Janssens, L. & Stoks, R. Daily temperature variation lowers the lethal and sublethal impact of a pesticide pulse due to a higher degradation rate. Chemosphere 263, 128114 (2021).Article
CAS
PubMed
Google Scholar
MacFadden, D. R., McGough, S. F., Fisman, D., Santillana, M. & Brownstein, J. S. Antibiotic resistance increases with local temperature. Nat. Clim. Change 8, 510–514 (2018).Article
ADS
CAS
Google Scholar
Li, Z. et al. Climate warming increases the proportions of specific antibiotic resistance genes in natural soil ecosystems. J. Hazard. Mater. 430, 128442 (2022).Article
CAS
PubMed
Google Scholar
Lin, D. et al. Climate warming fuels the global antibiotic resistome by altering soil bacterial traits. Nat. Ecol. Evolut. 9, 1512–1526 (2025).Article
Google Scholar
Delgado-Baquerizo, M. et al. The global distribution and environmental drivers of the soil antibiotic resistome. Microbiome 10, 219 (2022).Article
PubMed
PubMed Central
Google Scholar
Carey, J. C. et al. Temperature response of soil respiration largely unaltered with experimental warming. Proc. Natl Acad. Sci. USA 113, 13797–13802 (2016).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Alcock, B. P. et al. CARD 2023: expanded curation, support for machine learning, and resistome prediction at the Comprehensive Antibiotic Resistance Database. Nucleic Acids Res. 51, D690–D699 (2023).Article
CAS
PubMed
PubMed Central
Google Scholar
Zhou, J. et al. High-throughput metagenomic technologies for complex microbial community analysis: open and closed formats. mBio 6, e02288-14 (2015).Article
PubMed
PubMed Central
Google Scholar
Wood, D. E., Lu, J. & Langmead, B. Improved metagenomic analysis with Kraken 2. Genome Biol. 20, 257 (2019).Article
CAS
PubMed
PubMed Central
Google Scholar
Delgado-Baquerizo, M. et al. The proportion of soil-borne pathogens increases with warming at the global scale. Nat. Clim. Change 10, 550–554 (2020).Article
ADS
Google Scholar
Lee, K. et al. Population-level impacts of antibiotic usage on the human gut microbiome. Nat. Commun. 14, 1191 (2023).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Brito, I. L. et al. Mobile genes in the human microbiome are structured from global to individual scales. Nature 535, 435–439 (2016).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Zhang, A.-N. et al. An omics-based framework for assessing the health risk of antimicrobial resistance genes. Nat. Commun. 12, 4765 (2021).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Hudzicki, J. Kirby-Bauer disk diffusion susceptibility test protocol. Am. Soc. Microbiol. 15, 55–63 (2009).
Google Scholar
Hsu, T. Y. et al. Profiling lateral gene transfer events in the human microbiome using WAAFLE. Nat. Microbiol. 10, 94–111 (2025).Article
CAS
PubMed
Google Scholar
Smith, T. M. et al. Rapid adaptation of a complex trait during experimental evolution of Mycobacterium tuberculosis. eLife 11, e78454 (2022).Article
CAS
PubMed
PubMed Central
Google Scholar
Chuckran, P. F. et al. Edaphic controls on genome size and GC content of bacteria in soil microbial communities. Soil Biol. Biochem. 178, 108935 (2023).Article
CAS
Google Scholar
Gralka, M., Pollak, S. & Cordero, O. X. Genome content predicts the carbon catabolic preferences of heterotrophic bacteria. Nat. Microbiol. 8, 1799–1808 (2023).Article
CAS
PubMed
Google Scholar
Forsberg, K. J. et al. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337, 1107–1111 (2012).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Nesme, J. & Simonet, P. The soil resistome: a critical review on antibiotic resistance origins, ecology and dissemination potential in telluric bacteria. Environ. Microbiol. 17, 913–930 (2015).Article
PubMed
Google Scholar
McGough, S. F., MacFadden, D. R., Hattab, M. W., Mølbak, K. & Santillana, M. Rates of increase of antibiotic resistance and ambient temperature in Europe: a cross-national analysis of 28 countries between 2000 and 2016. Eurosurveillance 25, 1900414 (2020).Article
CAS
PubMed
PubMed Central
Google Scholar
Li, W. et al. Association between antibiotic resistance and increasing ambient temperature in China: an ecological study with nationwide panel data. Lancet Reg. Health West. Pac. 30, 100628 (2023).PubMed
Google Scholar
Borer, E. T. & Stevens, C. J. Nitrogen deposition and climate: an integrated synthesis. Trends Ecol. Evol. 37, 541–552 (2022).Article
CAS
PubMed
Google Scholar
Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892 (2008).Article
ADS
CAS
PubMed
Google Scholar
Sun, S. et al. Antibiotic resistance gene abundance and bacterial community structure in soils altered by ammonium and nitrate concentrations. Soil Biol. Biochem. 149, 107965 (2020).Article
CAS
Google Scholar
Xu, X., Sherry, R. A., Niu, S., Li, D. & Luo, Y. Net primary productivity and rain-use efficiency as affected by warming, altered precipitation, and clipping in a mixed-grass prairie. Glob. Change Biol. 19, 2753–2764 (2013).Article
ADS
Google Scholar
Li, D., Zhou, X., Wu, L., Zhou, J. & Luo, Y. Contrasting responses of heterotrophic and autotrophic respiration to experimental warming in a winter annual-dominated prairie. Glob. Change Biol. 19, 3553–3564 (2013).Article
ADS
Google Scholar
Sherry, R. A. et al. Lagged effects of experimental warming and doubled precipitation on annual and seasonal aboveground biomass production in a tallgrass prairie. Glob. Change Biol. 14, 2923–2936 (2008).Article
ADS
Google Scholar
McLean, E. in Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties (ed. Page, A. L.) 199–224 (1982).Zhou, J., Bruns, M. A. & Tiedje, J. M. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62, 316–322 (1996).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Bushnell, B. BBMap: A Fast, Accurate, Splice-aware Aligner (US Department of Energy, 2014).Li, D., Liu, C. M., Luo, R., Sadakane, K. & Lam, T. W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674–1676 (2015).Article
CAS
PubMed
Google Scholar
Qiu, Z. et al. BASALT refines binning from metagenomic data and increases resolution of genome-resolved metagenomic analysis. Nat. Commun. 15, 2179 (2024).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).Article
CAS
PubMed
PubMed Central
Google Scholar
Peng, Y., Leung, H. C., Yiu, S.-M. & Chin, F. Y. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420–1428 (2012).Article
CAS
PubMed
Google Scholar
Kang, D. D. et al. MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ 7, e7359 (2019).Article
PubMed
PubMed Central
Google Scholar
Wu, Y.-W., Simmons, B. A. & Singer, S. W. MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics 32, 605–607 (2015).Article
PubMed
Google Scholar
Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).Article
CAS
PubMed
PubMed Central
Google Scholar
Asnicar, F. et al. Precise phylogenetic analysis of microbial isolates and genomes from metagenomes using PhyloPhlAn 3.0. Nat. Commun. 11, 2500 (2020).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Asnicar, F., Weingart, G., Tickle, T. L., Huttenhower, C. & Segata, N. Compact graphical representation of phylogenetic data and metadata with GraPhlAn. PeerJ 3, e1029 (2015).Article
PubMed
PubMed Central
Google Scholar
Shi, Z. et al. Functional gene array-based ultrasensitive and quantitative detection of microbial populations in complex communities. mSystems 4, e00296-19 (2019).Article
PubMed
PubMed Central
Google Scholar
Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinf. 11, 119 (2010).Article
Google Scholar
Alcock, B. P. et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res. 48, D517–D525 (2020).CAS
PubMed
PubMed Central
Google Scholar
Gibson, M. K., Forsberg, K. J. & Dantas, G. Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology. ISME J. 9, 207–216 (2015).Article
CAS
PubMed
Google Scholar
Chaumeil, P.-A., Mussig, A. J., Hugenholtz, P. & Parks, D. H. GTDB-Tk v2: memory friendly classification with the genome taxonomy database. Bioinformatics 38, 5315–5316 (2022).Article
CAS
PubMed
PubMed Central
Google Scholar
Parks, D. H. et al. A complete domain-to-species taxonomy for Bacteria and Archaea. Nat. Biotechnol. 38, 1079–1086 (2020).Article
CAS
PubMed
Google Scholar
Young, J. M. et al. Names of Plant Pathogenic Bacteria, 1864-2004 (International Society for Plant Pathology, accessed 15 January 2026); https://www.isppweb.org/names_bacterial_revised.asp.Animal Diseases (World Organisation for Animal Health, accessed 15 January 2026); https://www.woah.org/en/what-we-do/animal-health-and-welfare/animal-diseases/.Yuan, L. et al. Pathogenic and indigenous denitrifying bacteria are transcriptionally active and key multi-antibiotic-resistant players in wastewater treatment plants. Environ. Sci. Technol. 55, 10862–10874 (2021).Article
ADS
CAS
PubMed
Google Scholar
Liu, B., Zheng, D., Jin, Q., Chen, L. & Yang, J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res. 47, D687–D692 (2019).Article
CAS
PubMed
PubMed Central
Google Scholar
Douglas, G. M. et al. Co-occurrence is associated with horizontal gene transfer across marine bacteria independent of phylogeny. ISME J. 20, wraf275 (2025).Steinegger, M. & Söding, J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat. Biotechnol. 35, 1026–1028 (2017).Article
CAS
PubMed
Google Scholar
Rahman, S. F., Olm, M. R., Morowitz, M. J. & Banfield, J. F. Machine learning leveraging genomes from metagenomes identifies influential antibiotic resistance genes in the infant gut microbiome. mSystems 3, e00123-17 (2018).Article
PubMed
PubMed Central
Google Scholar
Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–2504 (2003).Article
CAS
PubMed
PubMed Central
Google Scholar
Krawczyk, P. S., Lipinski, L. & Dziembowski, A. PlasFlow: predicting plasmid sequences in metagenomic data using genome signatures. Nucleic Acids Res. 46, e35 (2018).Article
PubMed
PubMed Central
Google Scholar
Mistry, J. et al. Pfam: the protein families database in 2021. Nucleic Acids Res. 49, 412–419 (2021).Article
Google Scholar
Smillie, C. S. et al. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480, 241–244 (2011).Article
ADS
CAS
PubMed
Google Scholar
Buyer, J. S. & Sasser, M. High throughput phospholipid fatty acid analysis of soils. Appl. Soil Ecol. 61, 127–130 (2012).Article
Google Scholar
Bengtsson-Palme, J. et al. METAXA2: improved identification and taxonomic classification of small and large subunit rRNA in metagenomic data. Mol. Ecol. Resour. 15, 1403–1414 (2015).Article
CAS
PubMed
Google Scholar
Karaoz, U. & Brodie, E. L. microTrait: a toolset for a trait-based representation of microbial genomes. Front. Bioinformatics 2, 918853 (2022).Article
Google Scholar
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation, 2020).Olm, M. R. et al. inStrain profiles population microdiversity from metagenomic data and sensitively detects shared microbial strains. Nat. Biotechnol. 39, 727–736 (2021).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Dong, X. et al. Phylogenetically and catabolically diverse diazotrophs reside in deep-sea cold seep sediments. Nat. Commun. 13, 4885 (2022).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Cantalapiedra, C. P., Hernández-Plaza, A., Letunic, I., Bork, P. & Huerta-Cepas, J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol. Biol. Evol. 38, 5825–5829 (2021).Article
CAS
PubMed
PubMed Central
Google Scholar
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2014).Fox, J. & Weisberg, S. An R Companion to Applied Regression (Sage Publications, 2018).Oksanen, J. et al. vegan: Community Ecology Package v.2, 6–8 (R Project, 2023).Paradis, E. & Schliep, K. Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).Article
CAS
PubMed
Google Scholar
Simpson, G. L. Permute: Functions for Generating Restricted Permutations of Data (R Project, 2025).Barton, M. K. MuMIn v.1 (R Project, 2015).Ning, D., Deng, Y., Tiedje, J. M. & Zhou, J. A general framework for quantitatively assessing ecological stochasticity. Proc. Natl Acad. Sci. USA 116, 16892–16898 (2019).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Liang, Y. et al. Century long fertilization reduces stochasticity controlling grassland microbial community succession. Soil Biol. Biochem. 151, 108023 (2020).Article
CAS
Google Scholar
Liaw, A. & Wiener, M. Classification and regression by randomForest. R News 2, 18–22 (2002).
Google Scholar