Antibiotic resistance currently causes hundreds of thousands of deaths worldwide; it is a major and growing public health threat globally. The origins of many resistance genes in pathogenic bacteria can be traced down to the environment; while a staggering number of resistant bacteria and resistance genes, selected for by human activities, are released into the environment. The nature, quantities and fates of this bidirectional flux of organisms and genes are mostly unknown. In order to understand the evolution of resistance within clinical settings, and the impact of the release of resistant bacteria into the environment, it is crucial to assess these questions and to assemble an integrated view of the problem. This review aims at providing an update on related issues previously discussed elsewhere, and to contribute to the comprehensive understanding of the environment as a source, receptacle and reservoir of antibiotic resistance.
Citation: Carlos F. Amábile-Cuevas. Antibiotic resistance from, and to the environment[J]. AIMS Environmental Science, 2021, 8(1): 18-35. doi: 10.3934/environsci.2021002
Antibiotic resistance currently causes hundreds of thousands of deaths worldwide; it is a major and growing public health threat globally. The origins of many resistance genes in pathogenic bacteria can be traced down to the environment; while a staggering number of resistant bacteria and resistance genes, selected for by human activities, are released into the environment. The nature, quantities and fates of this bidirectional flux of organisms and genes are mostly unknown. In order to understand the evolution of resistance within clinical settings, and the impact of the release of resistant bacteria into the environment, it is crucial to assess these questions and to assemble an integrated view of the problem. This review aims at providing an update on related issues previously discussed elsewhere, and to contribute to the comprehensive understanding of the environment as a source, receptacle and reservoir of antibiotic resistance.
[1] | O'Neil J (2016) Tackling drug-resistant infections globally: final report and recommendations. London: Wellcome Trust / HM Government. |
[2] | Laxminarayan R, Amábile-Cuevas CF, Cars O, et al. (2016) UN High-Level Meeting on antimicrobials -what do we need? Lancet 388: 218-220. |
[3] | O'Neil J (2019) Review of progress on antimicrobial resistance. London: Chatham House. |
[4] | Amábile-Cuevas CF (2016) Antibiotics and antibiotic resistance in the environment. Leiden: CRC Press/Balkema. |
[5] | Martínez JL, Coque TM, Baquero F (2015) What is a resistance gene? Ranking risk in resistomes. Nat Rev Microbiol 13: 116-123. doi: 10.1038/nrmicro3399 |
[6] | Benveniste R, Davies J (1973) 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. doi: 10.1073/pnas.70.8.2276 |
[7] | Cantón R (2009) Antibiotic resistance genes from the environment: a perspective through newly identified antibiotic resistance mechanisms in the clinical setting. Clin Microbiol Infect 15 (suppl. 1): 20-25. |
[8] | Miao V, Davies D, Davies J (2012) Path to resistance. In: Keen PL, Montforts MHMM, editors. Antimicrobial resistance in the environment. Hoboken: John Willey & Sons. pp. 7-14. |
[9] | D'Costa VM, McGrann KM, Hughes DW, et al. (2006) Sampling the antibiotic resistome. Science 311: 374-377. doi: 10.1126/science.1120800 |
[10] | D'Costa VM, King CE, Kalan L, et al. (2011) Antibiotic resistance is ancient. Nature 477: 457-461. doi: 10.1038/nature10388 |
[11] | Forsberg KJ, Patel S, Gibson MK, et al. (2014) Bacterial phylogeny structures soil resistomes across habitats. Nature 509: 612-616. doi: 10.1038/nature13377 |
[12] | Wright GD (2012) Antibiotic resistome: a framework linking the clinic and the environment. In: Keen PL, Montforts MHMM, editors. Antimicrobial resistance in the environment. Hoboken: John Wiley & Sons. pp. 15-27. |
[13] | Strahilevitz J, Jacoby GA, Hooper DC, et al. (2009) Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev 22: 664-689. doi: 10.1128/CMR.00016-09 |
[14] | Zhang H, Wei W, Huang M, et al. (2019) Definition of a family of nonmobile colistin resistance (NMCR-1) determinants suggests aquatic reservoirs for MCR-4. Adv Sci 2019: 1900038. doi: 10.1002/advs.201900038 |
[15] | Editorial (2011) Microbiology by numbers. Nat Rev Microbiol 9: 628. doi: 10.1038/nrmicro2644 |
[16] | Klein EY, Van Boeckel TP, Martinez EM, et al. (2018) Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci USA 115: E3463-E3470. doi: 10.1073/pnas.1717295115 |
[17] | Dolliver HAS (2007) Fate and transport of veterinary antibiotics in the environment: University of Minnesota. |
[18] | Mahon BM, Brehony C, McGrath E, et al. (2017) Indistinguishable NDM-producing Escherichia coli isolated from recreational waters, sewage, and a clinical specimen in Ireland, 2016 to 2017. Euro Surveill 22: 30513. doi: 10.2807/1560-7917.ES.2017.22.15.30513 |
[19] | Al-Tawfiq JA, Laxminarayan R, Mendelson M (2017) How should we respond to the emergence of plasmid-mediated colistin resistance in humans and animals? Int J Infect Dis 54: 77-84. |
[20] | Hutinel M, Huijbers PMC, Fick J, et al. (2019) Population-level surveillance of antibiotic resistance in Escherichia coli through sewage analysis. Euro Surveill 24: pii = 1800497. |
[21] | Mahnert A, Moissl-Eichinger C, Zojer M, et al. (2019) Man-made microbial resistances in built environments. Nat Commun 10: 968. doi: 10.1038/s41467-019-08864-0 |
[22] | Hendriksen RS, Munk P, Njage P, et al. (2019) Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage. Nat Commun 10: 1124. doi: 10.1038/s41467-019-08853-3 |
[23] | Amábile-Cuevas CF (2021) Antibiotic usage and resistance in Mexico: an update after a decade of change. J Infect Dev Ctries accepted. |
[24] | Rosas I, Amábile Cuevas CF, Calva E, et al. (2019) Animal and human waste as components of urban dust pollution: health implications. In: Nriagu JO, editor. Encyclopedia of environmental health, 2nd ed. pp. 95-102. |
[25] | Zhang T, Shi XC, Xia Y, et al. (2019) Escherichia coli adaptation and response to exposure to heavy atmospheric pollution. Sci Rep 9: 10879. doi: 10.1038/s41598-019-47427-7 |
[26] | Ng C, Goh SG, Saeidi N, et al. (2018) Occurrence of Vibrio species, beta-lactam resistant Vibrio species, and indicator bacteria in ballast and port waters of a tropical harbor. Sci Total Environ 610-611: 651-656. |
[27] | Heß S, Kneis D, Österlund T, et al. (2019) Sewage from airplanes exhibits high abundance and diversity of antibiotic resistance genes. Environ Sci Technol 53: 13898-13905. doi: 10.1021/acs.est.9b03236 |
[28] | Zhang Y, Marrs CF, Simon C, et al. (2009) Wastewater treatment contributes to selective increase of antibiotic resistance among Acinetobacter spp. Sci Total Environ 407: 3702-3706. doi: 10.1016/j.scitotenv.2009.02.013 |
[29] | Czekalski N, Berthold T, Caucci S, et al. (2012) Increased levels of multiresistant bacteria and resistance genes after wastewater treatment and their dissemination into Lake Geneva, Switzerland. Front Microbiol 3: 106. doi: 10.3389/fmicb.2012.00106 |
[30] | Schlüter A, Szczepanowski R, Pühler A, et al. (2007) Genomics of IncP-1 antibiotic resistance plasmids isolated from wastewater treatment plants provides evidence for a widely accessible drug resistance gene pool. FEMS Microbiol Rev 31: 449-477. doi: 10.1111/j.1574-6976.2007.00074.x |
[31] | Szczepanowski R, Braun S, Riedel V, et al. (2005) The 120592 bp IncF plasmid pRSB107 isolated from a sewage-treatment plant encodes nine different antibiotic-resistance determinants, two iron-acquisition systems and other putative virulence-associated functions. Microbiology 151: 1095-1111. doi: 10.1099/mic.0.27773-0 |
[32] | Jovanovic O, Amábile Cuevas CF, Shang C, et al. (2019) Are ESBL-producing E. coli isolated from a WWTP effluent more resistant to UV light at different wavelengths? 11th Micropol & Ecohazard Conference. Seoul: International Water Association. |
[33] | Hembach N, Alexander J, Hiller C, et al. (2019) Dissemination prevention of antibiotic resistant and facultative pathogenic bacteria by ultrafiltration and ozone treatment at an urban wastewater treatment plant. Sci Rep 9: 12843. doi: 10.1038/s41598-019-49263-1 |
[34] | Iakovides IC, Michael-Kordatou I, Moreira NFF, et al. (2019) Continuous ozonation of urban wastewater: removal of antibiotics, antibiotic-resistant Escherichia coli and antibiotic resistance genes and phytotoxicity. Water Res 159: 333-347. doi: 10.1016/j.watres.2019.05.025 |
[35] | Hiller CX, Hübner U, Fajnorova S, et al. (2019) Antibiotic microbial resistance (AMR) removal efficiencies by conventional and advanced wastewater treatment processes: a review. Sci Total Environ 685: 596-608. doi: 10.1016/j.scitotenv.2019.05.315 |
[36] | Díaz-Mejía JJ, Amábile-Cuevas CF, Rosas I, et al. (2008) An analysis of the evolutionary relationships of integron integrases, with emphasis on the prevalence of class 1 integron in Escherichia coli isolates from clinical and environmental origins. Microbiology 154: 94-102. doi: 10.1099/mic.0.2007/008649-0 |
[37] | Sütterlin S, Bray JE, Maiden MCJ, et al. (2020) Distribution of class 1 integrons in historic and contemporary collections of human pathogenic Escherichia coli. PLoS One 15: e0233315. doi: 10.1371/journal.pone.0233315 |
[38] | Amábile-Cuevas CF (2013) Antibiotic resistance: from Darwin to Lederberg to Keynes. Microb Drug Resist 19: 73-87. doi: 10.1089/mdr.2012.0115 |
[39] | Amábile-Cuevas CF, Chicurel ME (1992) Bacterial plasmids and gene flux. Cell 70: 189-199. doi: 10.1016/0092-8674(92)90095-T |
[40] | Ceccherini MT, Poté J, Kay E, et al. (2003) Degradation and transformability of DNA from transgenic leaves. Appl Environ Microbiol 69: 673-678. doi: 10.1128/AEM.69.1.673-678.2003 |
[41] | Pontiroli A, Rizzi A, Simonet P, et al. (2009) Visual evidence of horizontal gene transfer between plants and bacteria in the phytosphere of transplastomic tobacco. Appl Environ Microbiol 75: 3314-3322. doi: 10.1128/AEM.02632-08 |
[42] | Pruden A, Arabi M (2012) Quantifying anthropogenic impacts on environmental reservoirs of antibiotic resistance. In: Keen PL, Montforts MHMM, editors. Antimicrobial resistance in the environment. New Jersey: John Wiley & Sons. pp. 173-201. |
[43] | McLain JE, Cytryn E, Durso LM, et al. (2016) Culture-based methods for detection of antibiotic resistance in agroecosystems: advantages, challenges, and gaps in knowledge. J Environ Qual 45: 432-440. doi: 10.2134/jeq2015.06.0317 |
[44] | Singer AC, Xu Q, Keller VDJ (2019) Translating antibiotic prescribing into antibiotic resistance in the environment: a hazard characterisation case study. PLoS One 14: e0221568. doi: 10.1371/journal.pone.0221568 |
[45] | Schar D, Klein EY, Laxminarayan R, et al. (2020) Global trends in antimicrobial use in aquaculture. Sci Rep 10: 21878. doi: 10.1038/s41598-020-78849-3 |
[46] | Kristiansen JE (1991) Antimicrobial activity of nonantibiotics. ASM News 57: 135-139. |
[47] | Lancellotti P, Musumeci L, Jacques N, et al. (2019) Antibacterial activity of ticagrelor in conventional antiplatelet dosages against antibiotic-resistant gram-positive bacteria. JAMA Cardiol. |
[48] | Wang Y, Lu J, Mao L, et al. (2019) Antiepileptic drug carbamazepine promotes horizontal transfer of plasmid-borne multi-antibiotic resistance genes within and across bacteria genera. ISME J 13: 509-522. doi: 10.1038/s41396-018-0275-x |
[49] | Gaze WH, Abdouslam N, Hawkey PM, et al. (2005) Incidence of class 1 integrons in quaternary ammonium compound-polluted environment. Antimicrob Agents Chemother 49: 1802-1807. doi: 10.1128/AAC.49.5.1802-1807.2005 |
[50] | Westfall C, Flores-Mireles AL, Robinson JI, et al. (2019) The widely used antimicrobial triclosan induces high levels of antibiotic tolerance in vitro and reduces antibiotic efficacy up to 100-fold in vivo. Antimicrob Agents Chemother 63: e02312-02318. doi: 10.1128/AAC.02312-18 |
[51] | Amábile-Cuevas CF, Demple B (1991) Molecular characterization of the soxRS genes of Escherichia coli: two genes control a superoxide stress regulon. Nucleic Acids Res 19: 4479-4484. doi: 10.1093/nar/19.16.4479 |
[52] | Kurenbach B, Marjoshi D, Amábile Cuevas CF, et al. (2015) Sublethal exposure to commercial formulations of the herbicides dicamba, 2, 4-dichlorophenoxyacetic acid, and glyphosate cause changes in antibiotic susceptibility in Escherichia coli and Salmonella enterica serovar Typhimurium. mBio 6: e00009-00015. doi: 10.1128/mBio.00009-15 |
[53] | Pal C, Bengtsson-Palme J, Kristiansson E, et al. (2015) Co-ocurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genomics 16: 964. doi: 10.1186/s12864-015-2153-5 |
[54] | Merlin C (2020) Reducing the consumption of antibiotics: would that be enough to slow down the dissemination of resistances in the downstream environment? Front Microbiol 11: 33. |
[55] | Buberg ML, Witsø IL, L'Abée-Lund TM, et al. (2020) Zinc and copper reduce conjugative transfer of resistance plasmids from extended-spectrum beta-lactamase-producing Escherichia coli. Microb Drug Resist 26: 842-849. doi: 10.1089/mdr.2019.0388 |
[56] | Cristóbal-Azkarate J, Dunn JC, Day JMW, et al. (2014) Resistance to antibiotics of clinical relevance in the fecal microbiota of Mexican wildlife. PLoS One 9: e107719. doi: 10.1371/journal.pone.0107719 |
[57] | Alexander KA, Carlson CJ, Lewis BL, et al. (2018) The ecology of pathogen spillover and disease emergence at the human-wildlife-environment interface. In: Hurst CJ, editor. The connections between ecology and infectious disease: Springer. |
[58] | Sengupta S, Chattopadhyay MK, Grossart HP (2013) The multifaceted roles of antibiotics and antibiotic resistance in nature. Front Microbiol 4: 47. doi: 10.3389/fmicb.2013.00047 |
[59] | Liu G, Bogaj K, Bortolaia V, et al. (2019) Antibiotic-induced, increased conjugative transfer is common to diverse naturally occurring ESBL plasmids in Escherichia coli. Front Microbiol 10: 2119. doi: 10.3389/fmicb.2019.02119 |
[60] | Larsson DGJ (2014) Antibiotics in the environment. Upsala J Med Sci 119: 108-112. doi: 10.3109/03009734.2014.896438 |
[61] | Le Page G, Gunnarsson L, Snape J, et al. (2017) Integrating human and environmental health in antibiotic risk assessment: a critical analysis of protection goals, species sensitivity and antimicrobial resistance. Environ Int 109: 155-169. doi: 10.1016/j.envint.2017.09.013 |
[62] | Di Pilato V, Antonelli A, Giani T, et al. (2019) Identification of a novel plasmid lineage associeted with the dissemination of metallo-β-lactamase genes among Pseudomonads. Front Microbiol 10: 1504. doi: 10.3389/fmicb.2019.01504 |
[63] | Tanner WD, Atkinson RM, Goel RK, et al. (2017) Horizontal transfer of the blaNDM-1 gene to Pseudomonas aeruginosa and Acinetobacter baumannii in biofilms. FEMS Microbiol Lett 364: fnx048. |
[64] | Chu C, Murdock MH, Jing D, et al. (2019) The microbiota regulate neuronal function and fear extinction learning. Nature 574: 543-553. doi: 10.1038/s41586-019-1644-y |
[65] | Walsh TR, Weeks J, Livermore DM, et al. (2011) Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect Dis 11: 355-362. doi: 10.1016/S1473-3099(11)70059-7 |
[66] | Chen YM, Holmes EC, Chen X, et al. (2020) Diverse and abundant resistome in terrestrial and aquatic vertebrates revealed by transcriptional analysis. Sci Rep 10: 18870. doi: 10.1038/s41598-020-75904-x |
[67] | Stedt J, Bonnedahl J, Hernandez J, et al. (2014) Antibiotic resistance patterns in Escherichia coli from gulls in nine European countries. Infect Ecol Epidemiol 4: 21565. |
[68] | Witzany C, Bonhoeffer S, Rolff J (2020) Is antimicrobial resistance evolution accelerating? PLoS Pathog 16: e1008905. |
[69] | Amábile-Cuevas CF (2016) Society must seize control of the antibiotics crisis. Nature 533: 439. doi: 10.1038/533439a |