Neglected positive role of inactivating antibiotic resistance genes in the environment


  • Djordjevic, S. P. et al. Genomic surveillance for antimicrobial resistance—a One Health perspective. Nat. Rev. Genet. 25, 142–157 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Larsson, D. G. J., Gaze, W. H., Laxminarayan, R. & Topp, E. AMR, One Health and the environment. Nat. Microbiol. 8, 754–755 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hernando-Amado, S., Coque, T. M., Baquero, F. & Martínez, J. L. Defining and combating antibiotic resistance from One Health and Global Health perspectives. Nat. Microbiol. 4, 1432–1442 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rodriguez-Mozaz, S. et al. Occurrence of antibiotics and antibiotic resistance genes in hospital and urban wastewaters and their impact on the receiving river. Water Res. 69, 234–242 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Larsson, D. G. J. & Flach, C.-F. Antibiotic resistance in the environment. Nat. Rev. Microbiol. 20, 257–269 (2022). This review synthesizes the environmental dimensions of antibiotic resistance, establishing a framework for understanding the origins, evolution and transmission of resistance determinants that involves the external environment.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kraupner, N. et al. Evidence for selection of multi-resistant E. coli by hospital effluent. Environ. Int. 150, 106436 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhao, Y. et al. Antibiotic resistome in the livestock and aquaculture industries: status and solutions. Crit. Rev. Environ. Sci. Technol. 51, 2159–2196 (2021).

    Article 
    CAS 

    Google Scholar
     

  • Berglund, F., Ebmeyer, S., Kristiansson, E. & Larsson, D. G. J. Evidence for wastewaters as environments where mobile antibiotic resistance genes emerge. Commun. Biol. 6, 321 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ashbolt Nicholas, J. et al. Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environ. Health Perspect. 121, 993–1001 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • World Health Organization. Guidance on Wastewater and Solid Waste Management for Manufacturing of Antibiotics (World Health Organization, 2024); https://www.who.int/publications/i/item/9789240097254

  • United Nations Environment Programme. Bracing for Superbugs: Strengthening Environmental Action in the One Health Response to Antimicrobial Resistance (Unied Nations, 2023); https://www.unep.org/resources/superbugs/environmental-action

  • Yurtsev, E. A., Chao, H. X., Datta, M. S., Artemova, T. & Gore, J. Bacterial cheating drives the population dynamics of cooperative antibiotic resistance plasmids. Mol. Syst. Biol. 9, 683 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sorg, R. A. et al. Collective resistance in microbial communities by intracellular antibiotic deactivation. PLoS Biol. 14, e2000631 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lee, D.-H. et al. Colistin-degrading proteases confer collective resistance to microbial communities during polymicrobial infections. Microbiome. 10, 129 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bottery, M. J., Pitchford, J. W. & Friman, V.-P. Ecology and evolution of antimicrobial resistance in bacterial communities. ISME J. 15, 939–948 (2021).

    Article 
    PubMed 

    Google Scholar
     

  • Dantas, G., Sommer, M. O. A., Oluwasegun, R. D. & Church, G. M. Bacteria subsisting on antibiotics. Science 320, 100–103 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Allen, H. K. et al. Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8, 251–259 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wright, G. D. The antibiotic resistome: the nexus of chemical and genetic diversity. Nat. Rev. Microbiol. 5, 175–186 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Benveniste, R. & Davies, J. Aminoglycoside antibiotic-inactivating enzymes in actinomycetes similar to those present in clinical isolates of antibiotic-resistant bacteria. Proc. Natl Acad. Sci. USA 70, 2276–2280 (1973).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • D’Costa, V. M. et al. Antibiotic resistance is ancient. Nature 477, 457–461 (2011).

    Article 
    PubMed 

    Google Scholar
     

  • Van Goethem, M. W. et al. A reservoir of ‘historical’ antibiotic resistance genes in remote pristine Antarctic soils. Microbiome 6, 40 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Boolchandani, M., D’Souza, A. W. & Dantas, G. Sequencing-based methods and resources to study antimicrobial resistance. Nat. Rev. Genet. 20, 356–370 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Darby, E. M. et al. Molecular mechanisms of antibiotic resistance revisited. Nat. Rev. Microbiol. 21, 280–295 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Blair, J. M. A., Webber, M. A., Baylay, A. J., Ogbolu, D. O. & Piddock, L. J. V. Molecular mechanisms of antibiotic resistance. Nat. Rev. Microbiol. 13, 42–51 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Meredith, H. R., Srimani, J. K., Lee, A. J., Lopatkin, A. J. & You, L. Collective antibiotic tolerance: mechanisms, dynamics and intervention. Nat. Chem. Biol. 11, 182–188 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Vega, N. M. & Gore, J. Collective antibiotic resistance: mechanisms and implications. Curr. Opin. Microbiol. 21, 28–34 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bush, K. & Bradford, P. A. Epidemiology of β-lactamase-producing pathogens. Clin. Microbiol. Rev. 33, e00047-19 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tao, W. et al. Inactivation of chloramphenicol and florfenicol by a novel chloramphenicol hydrolase. Appl. Environ. Microbiol. 78, 6295–6301 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dhindwal, P. et al. A neglected and emerging antimicrobial resistance gene encodes for a serine-dependent macrolide esterase. Proc. Natl Acad. Sci. USA 120, e2219827120 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fillgrove, K. L., Pakhomova, S., Newcomer, M. E. & Armstrong, R. N. Mechanistic diversity of fosfomycin resistance in pathogenic microorganisms. J. Am. Chem. Soc. 125, 15730–15731 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gasparrini, A. J. et al. Tetracycline-inactivating enzymes from environmental, human commensal, and pathogenic bacteria cause broad-spectrum tetracycline resistance. Commun. Biol. 3, 241 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ma, X. et al. Molecular mechanism of chloramphenicol and thiamphenicol resistance mediated by a novel oxidase, CmO, in Sphingomonadaceae. Appl. Environ. Microbiol. 89, e0154722 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Huang, Y. et al. Strain-level diversity in sulfonamide biodegradation: adaptation of Paenarthrobacter to sulfonamides. ISME J. 18, wrad040 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen, Z. et al. Deglycosylation inactivation initiated by a novel periplasmic dehydrogenase complex provides a novel strategy for eliminating the recalcitrant antibiotic kanamycin. Environ. Sci. Technol. 57, 4298–4307 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liu, L.-K. et al. The structure of the antibiotic deactivating, N-hydroxylating rifampicin monooxygenase. J. Biol. Chem. 291, 21553–21562 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Olaitan, A. O. et al. Decoding a cryptic mechanism of metronidazole resistance among globally disseminated fluoroquinolone-resistant Clostridioides difficile. Nat. Commun. 14, 4130 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Crofts, T. S. et al. Discovery and characterization of a nitroreductase capable of conferring bacterial resistance to chloramphenicol. Cell Chem. Biol. 26, 559–570.e556 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Löffler, P., Escher, B. I., Baduel, C., Virta, M. P. & Lai, F. Y. Antimicrobial transformation products in the aquatic environment: global occurrence, ecotoxicological risks and potential of antibiotic resistance. Environ. Sci. Technol. 57, 9474–9494 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hu, J., Lyu, Y., Chen, H., Li, S. & Sun, W. Suspect and nontarget screening reveal the underestimated risks of antibiotic transformation products in wastewater treatment plant effluents. Environ. Sci. Technol. 57, 17439–17451 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bhattacharya, A. & Khare, S. K. Utilizing the β-lactam hydrolyzing activity of ß-lactamase produced by Bacillus cereus EMB20 for remediation of β-lactam antibiotics. Int. Biodeterior. Biodegrad. 168, 105363 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Gal, M. & Brazier, J. S. Metronidazole resistance in Bacteroides spp. Carrying nim genes and the selection of slow-growing metronidazole-resistant mutants. J. Antimicrob. Chemother. 54, 109–116 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li, Q. et al. Positive contribution of antimicrobial biodegradation in mitigating conjugative transfer of antibiotic resistance genes. Environ. Sci. Technol. 59, 21645–21656 (2025). This study provides direct experimental evidence that antimicrobial biodegradation can reduce conjugative transfer of ARGs to high‑risk pathogens, highlighting how antibiotic fate processes can modulate AMR dissemination risk across microbiotas.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Robicsek, A. et al. Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat. Med. 12, 83–88 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Majewsky, M. et al. Antibacterial activity of sulfamethoxazole transformation products (TPs): general relevance for sulfonamide TPs modified at the para position. Chem. Res. Toxicol. 27, 1821–1828 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Halling-Sørensen, B., Sengeløv, G. & Tjørnelund, J. Toxicity of tetracyclines and tetracycline degradation products to environmentally relevant bacteria, including selected tetracycline-resistant bacteria. Arch. Environ. Contam. Toxicol. 42, 263–271 (2002).

    Article 
    PubMed 

    Google Scholar
     

  • Deng, Y. et al. Microbiome assembly for sulfonamide subsistence and the transfer of genetic determinants. ISME J. 15, 2817–2829 (2021). This study links sulfonamide subsistence to the sadA gene and shows that this genetic capability is evolutionarily conserved with limited spread beyond the Micrococcaceae boundary, helping to constrain concerns about widespread horizontal transfer of this inactivating ARGs.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Qi, M. et al. Microbial interactions drive the complete catabolism of the antibiotic sulfamethoxazole in activated sludge microbiomes. Environ. Sci. Technol. 55, 3270–3282 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ma, X. et al. Novel pathway for chloramphenicol catabolism in the activated sludge bacterial isolate Sphingobium sp. CAP-1. Environ. Sci. Technol. 54, 7591–7600 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Woappi, Y., Gabani, P., Singh, A. & Singh, O. V. Antibiotrophs: the complexity of antibiotic-subsisting and antibiotic-resistant microorganisms. Crit. Rev. Microbiol. 42, 17–30 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Deng, Y., Li, B. & Zhang, T. Bacteria that make a meal of sulfonamide antibiotics: blind spots and emerging opportunities. Environ. Sci. Technol. 52, 3854–3868 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ebmeyer, S., Kristiansson, E. & Larsson, D. G. J. A framework for identifying the recent origins of mobile antibiotic resistance genes. Commun. Biol. 4, 8 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Poirel, L., Kämpfer, P. & Nordmann, P. Chromosome-encoded Ambler class a β-lactamase of Kluyvera georgiana, a probable progenitor of a subgroup of CTX-M extended-spectrum β-lactamases. Antimicrob. Agents Chemother. 46, 4038–4040 (2002).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Klümper, U. et al. Selection for antimicrobial resistance is reduced when embedded in a natural microbial community. ISME J. 13, 2927–2937 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wen, X., Langevin, A. M. & Dunlop, M. J. Antibiotic export by efflux pumps affects growth of neighboring bacteria. Sci. Rep. 8, 15120 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Denk-Lobnig, M. K. & Wood, K. B. Spatial population dynamics of bacterial colonies with social antibiotic resistance. Proc. Natl Acad. Sci. USA 122, e2417065122 (2025).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Laborda, P., Gil-Gil, T., Martínez, J. L. & Hernando-Amado, S. Preserving the efficacy of antibiotics to tackle antibiotic resistance. Microb. Biotechnol. 17, e14528 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bottery Michael, J., Wood, A. J. & Brockhurst Michael, A. Selective conditions for a multidrug resistance plasmid depend on the sociality of antibiotic resistance. Antimicrob. Agents Chemother. 60, 2524–2527 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nicoloff, H. & Andersson, D. I. Indirect resistance to several classes of antibiotics in cocultures with resistant bacteria expressing antibiotic-modifying or -degrading enzymes. J. Antimicrob. Chemother. 71, 100–110 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bottery, M. J. et al. Inter-species interactions alter antibiotic efficacy in bacterial communities. ISME J. 16, 812–821 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kelsic, E. D., Zhao, J., Vetsigian, K. & Kishony, R. Counteraction of antibiotic production and degradation stabilizes microbial communities. Nature 521, 516–519 (2015). This study reveals that antibiotic-degrading species, unlike intrinsically resistant ones, can robustly stabilize microbial communities against species loss even under high dispersal rates by attenuating inhibitory interactions, highlighting a fundamental role for degradation-mediated resistance in maintaining ecosystem diversity and stability.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen, J., Chen, X., Zhu, Y., Yan, S. & Xie, S. New insights into bioaugmented removal of sulfamethoxazole in sediment microcosms: degradation efficiency, ecological risk and microbial mechanisms. Microbiome 12, 43 (2024). This study shows that bioaugmentation with sulfonamide degraders (including a sadA-encoded ipso-hydroxylation pathway) can accelerate sulfamethoxazole removal while reducing the abundance of key sulfonamide resistance genes (for example, sul1 and sul2) and lowering overall community ARG and MGE loads, highlighting the potential for antibiotic-inactivating functions to mitigate broader resistome burden at the community level.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Frost, I. et al. Cooperation, competition and antibiotic resistance in bacterial colonies. ISME J. 12, 1582–1593 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yurtsev, E. A., Conwill, A. & Gore, J. Oscillatory dynamics in a bacterial cross-protection mutualism. Proc. Natl Acad. Sci. USA 113, 6236–6241 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Estrela, S. & Brown, S. P. Community interactions and spatial structure shape selection on antibiotic resistant lineages. PLoS Comput. Biol. 14, e1006179 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Meredith, H. R. et al. Applying ecological resistance and resilience to dissect bacterial antibiotic responses. Sci. Adv. 4, eaau1873 (2018). This study establishes a quantitative ecological framework to dissect bacterial responses to antibiotics, highlighting how antibiotic-degrading traits (specifically β-lactamase activity) significantly enhance population resilience by accelerating recovery after antibiotic stress, in contrast to target modification mechanisms that primarily improve resistance but not recovery speed.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Allen, H. K. & Stanton, T. B. Altered egos: antibiotic effects on food animal microbiomes. Annu. Rev. Microbiol. 68, 297–315 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hou, L. et al. Effects of sulfamethazine on denitrification and the associated N2O release in estuarine and coastal sediments. Environ. Sci. Technol. 49, 326–333 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wepking, C. et al. Prolonged exposure to manure from livestock-administered antibiotics decreases ecosystem carbon-use efficiency and alters nitrogen cycling. Ecol. Lett. 22, 2067–2076 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Pathak, A., Angst, D. C., León-Sampedro, R. & Hall, A. R. Antibiotic-degrading resistance changes bacterial community structure via species-specific responses. ISME J. 17, 1495–1503 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cubillos-Ruiz, A. et al. An engineered live biotherapeutic for the prevention of antibiotic-induced dysbiosis. Nat. Biomed. Eng. 6, 910–921 (2022). This study demonstrates a therapeutic application of inactivating ARGs by engineering a Lactococcus lactis strain to express a β-lactamase in the gut, effectively protecting the microbiome from antibiotic-induced dysbiosis without interfering with systemic antibiotic efficacy.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fishbein, S. R. S., Mahmud, B. & Dantas, G. Antibiotic perturbations to the gut microbiome. Nat. Rev. Microbiol. 21, 772–788 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kaleko, M. et al. Development of SYN-004, an oral β -lactamase treatment to protect the gut microbiome from antibiotic-mediated damage and prevent Clostridium difficile infection. Anaerobe 41, 58–67 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • He, Q. et al. Designing a reengineered probiotic yeast to spontaneously degrade residual antibiotics in gut during antimicrobial therapy. J. Clean. Prod. 483, 144177 (2024).

    Article 
    CAS 

    Google Scholar
     

  • Zhang, L. et al. Complementary biotransformation of antimicrobial triclocarban obviously mitigates nitrous oxide emission toward sustainable microbial denitrification. Environ. Sci. Technol. 57, 7490–7502 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang, H. et al. Mechanisms linking triclocarban biotransformation to functional response and antimicrobial resistome evolution in wastewater treatment systems. Water Res. 260, 121909 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wei, Y. et al. Synergistic control of trimethoprim and the antimicrobial resistome in electrogenic microbial communities. Environ. Sci. Technol. 58, 2847–2858 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Langdon, A., Crook, N. & Dantas, G. The effects of antibiotics on the microbiome throughout development and alternative approaches for therapeutic modulation. Genome Med. 8, 39 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ebmeyer, S., Kristiansson, E. & Larsson, D. G. J. Unraveling the origins of mobile antibiotic resistance genes using random forest classification of large-scale genomic data. Environ. Int. 198, 109374 (2025).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lund, D. et al. Genetic compatibility and ecological connectivity drive the dissemination of antibiotic resistance genes. Nat. Commun. 16, 2595 (2025).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Parras-Moltó, M. et al. The transfer of antibiotic resistance genes between evolutionarily distant bacteria. mSphere 10, e00114–e00125 (2025).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     



  • Source link

    Leave a Reply

    Your email address will not be published. Required fields are marked *