Advertisement

Environmental Science and Pollution Research

, Volume 26, Issue 27, pp 28352–28360 | Cite as

The impact and mechanism of quaternary ammonium compounds on the transmission of antibiotic resistance genes

  • Yue Han
  • Zhen-Chao Zhou
  • Lin Zhu
  • Yuan-Yuan Wei
  • Wan-Qiu Feng
  • Lan Xu
  • Yang Liu
  • Ze-Jun Lin
  • Xin-Yi Shuai
  • Zhi-Jian Zhang
  • Hong ChenEmail author
Research Article

Abstract

The emergence of antibiotic resistance genes (ARGs) in microbes can be largely attributed to the abuse and misuse of antibiotics and biocides. Quaternary ammonium compounds (QACs) have been used worldwide as common disinfectants and detergents; however, their potential impact on the spread and diffusion of ARGs is still unknown. In this study, we detected the QAC resistance gene (qacEΔ1), the 1 integron gene (intI1), and 12 ARGs (sul1, sul2, cfr, cml, fexA, tetA, tetG, tetQ, tetX, ermB, blaTEM, and dfrA1) in 48 water samples from three watersheds by quantitative PCR (qPCR). We investigated the evolution of bacterial antibiotic resistance under QAC and antibiotic environmental pressures by long-term continuous culture. In addition, five QACs were selected to investigate the effect of QAC on the efficiency of conjugation transfer. The changes in bacterial cell membrane and production of reactive oxygen species (ROS) were detected by flow cytometry, revealing the mechanism by which QAC affects the spread of antibiotic resistance. Our results showed that the QAC resistance gene was ubiquitous in watersheds and it had significant correlation with intI1 and seven ARGs (r = 0.999, p < 0.01). QACs could increase the resistance of bacteria to multiple antibiotics. Furthermore, all five QACs promoted the conjugation transfer of the RP4 plasmid; the optimal concentration of QACs was about 10−1–10−2 mg/L and their transfer efficiencies were between 1.33 × 10−6 and 8.87 × 10−5. QACs enhanced membrane permeability of bacterial cells and stimulated bacteria to produce ROS, which potentially promoted the transfer of plasmids between bacteria. In conclusion, this study demonstrated that QACs may facilitate the evolution and gene transfer of antibiotic resistance gene among microbiome.

Keywords

Antibiotic resistance gene Quaternary ammonium compounds Conjugation transfer 

Notes

Acknowledgments

This work was supported by Natural Science Foundation of China (21677121 and 41571130064).

Supplementary material

11356_2019_5673_MOESM1_ESM.docx (6.1 mb)
ESM 1 (DOCX 6274 kb)

References

  1. Alekshun MN, Levy SB (2007) Molecular mechanisms of antibacterial multidrug resistance. Cell 128:1037–1050CrossRefGoogle Scholar
  2. Bakeraustin C, Wright MS, Stepanauskas R, Mcarthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182CrossRefGoogle Scholar
  3. Bouzada ML, Silva VL, Moreira FA, Silva GA, Diniz CG (2010) Antimicrobial resistance and disinfectants susceptibility of persistent bacteria in a tertiary care hospital. J Microbiol Antimicrob 2:105–112Google Scholar
  4. Brazas MD, Hancock RE (2005) Ciprofloxacin induction of a susceptibility determinant in Pseudomonas aeruginosa. Antimicrob Agents Chemother 49:3222–3227CrossRefGoogle Scholar
  5. Chapman JS (2003) Disinfectant resistance mechanisms, cross-resistance, and co-resistance. Int Biodeterior Biodegrad 51:271–276CrossRefGoogle Scholar
  6. Chen I, Christie PJ, Dubnau D (2005) The ins and outs of DNA transfer in bacteria. Science 310:1456–1460CrossRefGoogle Scholar
  7. Cui E, Wu Y, Zuo Y, Chen H (2016) Effect of different biochars on antibiotic resistance genes and bacterial community during chicken manure composting. Bioresour Technol 203:11–17CrossRefGoogle Scholar
  8. García MT, Campos E, Sanchez-Leal J, Ribosa I (1999) Effect of the alkyl chain length on the anaerobic biodegradability and toxicity of quaternary ammonium based surfactants. Chemosphere 38:3473–3483CrossRefGoogle Scholar
  9. Gaze WH, Zhang L, Abdouslam NA, Hawkey PM, Calvobado L, Royle J, Brown H, Davis S, Kay P, Boxall ABA (2011) Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. ISME J 5:1253–1261CrossRefGoogle Scholar
  10. Gilbert P, Moore LE (2005) Cationic antiseptics: diversity of action under a common epithet. J Appl Microbiol 99:703–715CrossRefGoogle Scholar
  11. Gillings MR, Duan X, Hardwick SA, Holley MP, Stokes HW (2009a) Gene cassettes encoding resistance to quaternary ammonium compounds: a role in the origin of clinical class 1 integrons? ISME J. 3:209–215CrossRefGoogle Scholar
  12. Gillings MR, Holley MP, Stokes HW (2009b) Evidence for dynamic exchange of qac gene cassettes between class 1 integrons and other integrons in freshwater biofilms. FEMS Microbiol Lett 296:282–288CrossRefGoogle Scholar
  13. Gillings MR, Gaze WH, Pruden A, Smalla K, Tiedje JM, Zhu YG (2015) Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J. 9:1269–1279CrossRefGoogle Scholar
  14. Heerklotz H (2008) Interactions of surfactants with lipid membranes. Q Rev Biophys 41:205–264CrossRefGoogle Scholar
  15. Hegstad K, Langsrud S, Lunestad BT, Scheie AA, Sunde M, Yazdankhah SP (2010) Does the wide use of quaternary ammonium compounds enhance the selection and spread of antimicrobial resistance and thus threaten our health? Microb Drug Resist 16:91–104CrossRefGoogle Scholar
  16. Holmberg K (2002) Handbook of applied surface and colloid chemistry. Aust J Chem 55:383–402Google Scholar
  17. Jansen AC, Boucher CE, Coetsee E, Kock JLF, Wyk PWJV, Swart HC, Bragg RR (2013) The influence of didecyldimethylammonium chloride on the morphology and elemental composition of Staphylococcus aureus as determined by NanoSAM. Sci Res Essays 8:152–160Google Scholar
  18. Jiao YN, Chen H, Gao RX, Zhu YG, Rensing C (2017) Organic compounds stimulate horizontal transfer of antibiotic resistance genes in mixed wastewater treatment systems. Chemosphere 184:53–61CrossRefGoogle Scholar
  19. Jutkina J, Marathe NP, Flach CF, Larsson DGJ (2018) Antibiotics and common antibacterial biocides stimulate horizontal transfer of resistance at low concentrations. Sci Total Environ 616-617:172–178CrossRefGoogle Scholar
  20. Kholodii GY, Mindlin SZ, Bass IA, Yurieva OV, Minakhina SV, Nikiforov VG (1995) Four genes, two ends, and a res region are involved in transposition of Tn5053: a paradigm for a novel family of transposons carrying either a mer operon or an integron. Mol Microbiol 17:1189–1200CrossRefGoogle Scholar
  21. Levin-Reisman I, Ronin I, Gefen O, Braniss I, Shoresh N, Balaban NQ (2017) Antibiotic tolerance facilitates the evolution of resistance. Science 355(6327):826–830CrossRefGoogle Scholar
  22. Li X, Brownawell BJ (2010) Quaternary ammonium compounds in urban estuarine sediment environments—a class of contaminants in need of increased attention? Environ Sci Technol 44:7561–7568CrossRefGoogle Scholar
  23. Li D, Zeng S, He M, Gu AZ (2016) Water disinfection byproducts induce antibiotic resistance-role of environmental pollutants in resistance phenomena. Environ Sci Technol 50(6):3193–3201CrossRefGoogle Scholar
  24. Liu WJ, Fu L, Huang M, Zhang JP, Wu Y, Zhou YS, Zeng J, Wang GX (2017) Frequency of antiseptic resistance genes and reduced susceptibility to biocides in carbapenem-resistant Acinetobacter baumannii. J Med Microbiol 66Google Scholar
  25. Lopatkin AJ, Huang S, Smith RP, Srimani JK, Sysoeva TA, Bewick S, Karig DK, You L (2016) Antibiotics as a selective driver for conjugation dynamics. Nat Microbiol 1:16044CrossRefGoogle Scholar
  26. Loughlin MF, Jones MV, Lambert PA (2002) Pseudomonas aeruginosa cells adapted to benzalkonium chloride show resistance to other membrane-active agents but not to clinically relevant antibiotics. J Antimicrob Chemother 49:631–639CrossRefGoogle Scholar
  27. Luo Y, Wang Q, Lu Q, Mu Q, Mao D (2014) An ionic liquid facilitates the proliferation of antibiotic resistance genes mediated by class I integrons. Environ Sci Technol Lett 1:266–270CrossRefGoogle Scholar
  28. Maillard JY (2002) Bacterial target sites for biocide action. J Appl Microbiol 92:16S–27SCrossRefGoogle Scholar
  29. Marathe NP, Pal C, Gaikwad SS, Jonsson V, Kristiansson E, Dgj L (2017) Untreated urban waste contaminates Indian river sediments with resistance genes to last resort antibiotics. Water Res 124:388–397CrossRefGoogle Scholar
  30. Mc Cay PH, Ocampo-Sosa AA, Fleming GT (2010) Effect of subinhibitory concentrations of benzalkonium chloride on the competitiveness of Pseudomonas aeruginosa grown in continuous culture. Microbiology 156:30–38CrossRefGoogle Scholar
  31. Mcdonnell G, Russell AD (1999) Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 12:147–179CrossRefGoogle Scholar
  32. Mcmanus PS, Stockwell VO, Sundin GW, Jones AL (2002) Antibiotic use in plant agriculture. Annu Rev Phytopathol 40:443–465CrossRefGoogle Scholar
  33. Moriguchi K, Yamamoto S, Ohmine Y, Suzuki K (2016) A fast and practical yeast transformation method mediated by Escherichia coli based on a trans-kingdom conjugal transfer system: just mix two cultures and wait one hour. PLoS One 11:e0148989CrossRefGoogle Scholar
  34. Nagai K, Murata T, Ohta S, Zenda H, Ohnishi M, Hayashi T (2003) Two different mechanisms are involved in the extremely high-level benzalkonium chloride resistance of a Pseudomonas fluorescens strain. Microbiol Immunol 47:709–715CrossRefGoogle Scholar
  35. Pal C, Bengtssonpalme J, Kristiansson E, Larsson DG (2015) Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genomics 16:1–14CrossRefGoogle Scholar
  36. Patrauchan MA, Oriel PJ (2003) Degradation of benzyldimethylalkylammonium chloride by Aeromonas hydrophila sp. K. J Appl Microbiol 94:266–272CrossRefGoogle Scholar
  37. Pruden A, Pei R, Storteboom H, Carlson KH (2006) Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ Sci Technol 40:7445–7450CrossRefGoogle Scholar
  38. Qiu Z, Yu Y, Chen Z, Jin M, Yang D, Zhao Z, Wang J, Shen Z, Wang X, Qian D (2012) Nanoalumina promotes the horizontal transfer of multiresistance genes mediated by plasmids across genera. Proc Natl Acad Sci U S A 109:4944–4949CrossRefGoogle Scholar
  39. Recchia GD, Hall RM (1995) Gene cassettes: a new class of mobile element. Microbiology 141 ( Pt 12:3015–3027CrossRefGoogle Scholar
  40. Ruan T, Song S, Wang T, Liu R, Lin Y, Jiang G (2014) Identification and composition of emerging quaternary ammonium compounds in municipal sewage sludge in China. Environ Sci Technol 48:4289–4297CrossRefGoogle Scholar
  41. Sentchilo V, Mayer AP, Guy L, Miyazaki R, Tringe SG, Barry K, Malfatti S, Goessmann A, Robinson-Rechavi M, van der Meer JR (2013) Community-wide plasmid gene mobilization and selection. ISME J. 7(6):1173–1186CrossRefGoogle Scholar
  42. Singer RS, Finch R, Wegener HC, Bywater R, Walters J, Lipsitch M (2003) Antibiotic resistance—the interplay between antibiotic use in animals and human beings. Lancet Infect Dis 3:47–51CrossRefGoogle Scholar
  43. Su JQ, Wei B, Ouyang WY, Huang FY, Zhao Y, Xu HJ, Zhu YG (2015) Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environ Sci Technol 49(12):7356–7363CrossRefGoogle Scholar
  44. Tabata A, Nagamune H, Maeda T, Murakami K, Miyake Y, Kourai H (2003) Correlation between resistance of Pseudomonas aeruginosa to quaternary ammonium compounds and expression of outer membrane protein OprR. Antimicrob Agents Chemother 47:2093–2099CrossRefGoogle Scholar
  45. Tezel U, Pierson JA, Pavlostathis SG (2006) Fate and effect of quaternaryammonium compounds on a mixed methanogenic culture. Water Res 40:3660–3668CrossRefGoogle Scholar
  46. Tezel U, Pierson JA, Pavlostathis SG (2007) Effect of polyelectrolytes and quaternary ammonium compounds on the anaerobic biological treatment of poultry processing wastewater. Water Res 41:1334–1342CrossRefGoogle Scholar
  47. Van dVA, Lorgeoux C, Gromaire MC, Chebbo G (2012) Analysis of quaternary ammonium compounds in urban stormwater samples. Environ Pollut 164:150CrossRefGoogle Scholar
  48. Waters VL (2001) Conjugation between bacterial and mammalian cells. Nat Genet 29:375–376CrossRefGoogle Scholar
  49. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703CrossRefGoogle Scholar
  50. Wistrand-Yuen E, Knopp M, Hjort K, Koskiniemi S, Berg OG, Andersson DI (2018) Evolution of high-level resistance during low-level antibiotic exposure. Nat Commun 9(1):1599CrossRefGoogle Scholar
  51. Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, Walsh TR (2009) Characterization of a new metallo-β-lactamase gene, blaNDM-1, and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother 53:5046–5054CrossRefGoogle Scholar
  52. Zhang Y, Gu AZ, He M, Li D, Chen J (2017) Subinhibitory concentrations of disinfectants promote the horizontal transfer of multidrug resistance genes within and across genera. Environ Sci Technol 51:570–580CrossRefGoogle Scholar
  53. Zheng J, Gao R, Wei Y, Chen T, Fan J, Zhou Z, Makimilua TB, Jiao Y, Chen H (2017) High-throughput profiling and analysis of antibiotic resistance genes in east Tiaoxi River. China Environ Pollut 230:648–654CrossRefGoogle Scholar
  54. Zhou ZC, Zheng J, Wei YY, Chen T, Dahlgren RA, Shang X, Chen H (2017) Antibiotic resistance genes in an urban river as impacted by bacterial community and physicochemical parameters. Environ Sci Pollut Res:1–10Google Scholar
  55. Zhou ZC, Feng WQ, Han Y, Zheng J, Chen T, Wei Y-Y, Gillings M, Zhu Y-G, Chen H (2018) Prevalence and transmission of antibiotic resistance and microbiota between humans and water environments. Environ Int 121:1155–1161CrossRefGoogle Scholar
  56. Zhu YG, Zhao Y, Li B, Huang CL, Zhang SY, Yu S, Chen YS, Zhang T, Gillings MR, Su JQ (2017) Continental-scale pollution of estuaries with antibiotic resistance genes. Nat Microbiol 2:16270CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Yue Han
    • 1
  • Zhen-Chao Zhou
    • 1
  • Lin Zhu
    • 1
  • Yuan-Yuan Wei
    • 1
  • Wan-Qiu Feng
    • 1
  • Lan Xu
    • 1
  • Yang Liu
    • 1
  • Ze-Jun Lin
    • 1
  • Xin-Yi Shuai
    • 1
  • Zhi-Jian Zhang
    • 1
  • Hong Chen
    • 1
    Email author
  1. 1.Institute of Environmental Technology, College of Environmental and Resource SciencesZhejiang UniversityHangzhouChina

Personalised recommendations