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Heavy Metal Induced Antibiotic Resistance in Bacterium LSJC7

Chen, Songcan, Li, Xiaomin, Sun, Guoxin, Zhang, Yingjiao, Su, Jianqiang, Ye, Jun·2015·International Journal of Molecular Sciences

Abstract

Co-contamination of antibiotics and heavy metals prevails in the environment, and may play an important role in disseminating bacterial antibiotic resistance, but the selective effects of heavy metals on bacterial antibiotic resistance is largely unclear. To investigate this, the effects of heavy metals on antibiotic resistance were studied in a genome-sequenced bacterium, LSJC7. The results showed that the presence of arsenate, copper, and zinc were implicated in fortifying the resistance of LSJC7 towards tetracycline. The concentrations of heavy metals required to induce antibiotic resistance, i.e., the minimum heavy metal concentrations (MHCs), were far below (up to 64-fold) the minimum inhibition concentrations (MIC) of LSJC7. This finding indicates that the relatively low heavy metal levels in polluted environments and in treated humans and animals might be sufficient to induce bacterial antibiotic resistance. In addition, heavy metal induced antibiotic resistance was also observed for a combination of arsenate and chloramphenicol in LSJC7, and copper/zinc and tetracycline in antibiotic susceptible strain Escherichia coli DH5α. Overall, this study implies that heavy metal induced antibiotic resistance might be ubiquitous among various microbial species and suggests that it might play a role in the emergence and spread of antibiotic resistance in metal and antibiotic co-contaminated environments.

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  • Pollution with heavy metals such as chromium, lead, cadmium, and mercury is well-documented to induce antibiotic resistance through co-selection.

    “Moreover, pollution with heavy metals such as chromium, lead, cadmium, and mercury is well-documented to induce antibiotic resistance through co-selection10–12.”

    From Impact of untreated tannery wastewater in the evolution of multidrug-resistant bacteria in Bangladesh (2024) · cites this paper as [11]

    The Introduction (page unavailable) describes heavy-metal contamination contributing to antibiotic resistance and reports that cadmium increased resistance in microcosms. But the paper's own antibiotic-resistance findings concern arsenate, copper, and zinc; our copy does not establish that chromium, lead, or mercury induce antibiotic resistance through co-selection. (LLM, conf=0.87)

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Research works printed but not linked: 51

  1. Martinez, 2011, Metabolic regulation of antibiotic resistance, FEMS Microbiol. Rev., 35, 768, 10.1111/j.1574-6976.2011.00282.x · DOI
  2. Zhu, 2013, Diverse and abundant antibiotic resistance genes in Chinese swine farms, Proc. Natl. Acad. Sci. USA, 110, 3435, 10.1073/pnas.1222743110 · DOI
  3. Looft, 2012, In-feed antibiotic effects on the swine intestinal microbiome, Proc. Natl. Acad. Sci. USA, 109, 1691, 10.1073/pnas.1120238109 · DOI · Paper page
  4. Hvistendahl, 2012, China takes aim at rampant antibiotic resistance, Science, 336, 795, 10.1126/science.336.6083.795 · DOI
  5. Pan, 2011, Residual veterinary antibiotics in swine manure from concentrated animal feeding operations in Shandong Province, China, Chemosphere, 84, 695, 10.1016/j.chemosphere.2011.03.022 · DOI
  6. Wang, 2010, High-performance liquid chromatography inductively coupled plasma mass spectrometry based method for the determination of organic arsenic feed additives and speciation of anionic arsenics in animal feed, J. Agric. Food Chem., 58, 5263, 10.1021/jf1001205 · DOI
  7. Binh, 2008, Piggery manure used for soil fertilization is a reservoir for transferable antibiotic resistance plasmids, FEMS Microbiol. Ecol., 66, 25, 10.1111/j.1574-6941.2008.00526.x · DOI
  8. Lu, 2014, Interaction of veterinary antibiotic tetracyclines and copper on their fates in water and water hyacinth (Eichhornia crassipes), J. Hazard. Mater., 280, 389, 10.1016/j.jhazmat.2014.08.022 · DOI
  9. Hernando, 2006, Environmental risk assessment of pharmaceutical residues in wastewater effluents, surface waters and sediments, Talanta, 69, 334, 10.1016/j.talanta.2005.09.037 · DOI
  10. Skurnik, 2010, Is exposure to mercury a driving force for the carriage of antibiotic resistance genes?, J. Med. Microbiol., 59, 804, 10.1099/jmm.0.017665-0 · DOI
  11. Kong, 2006, The veterinary antibiotic oxytetracycline and Cu influence functional diversity of the soil microbial community, Environ. Pollut., 143, 129, 10.1016/j.envpol.2005.11.003 · DOI
  12. Wright, 2006, Co-selection of antibiotic and metal resistance, Trends Microbiol., 14, 176, 10.1016/j.tim.2006.02.006 · DOI
  13. Peltier, 2010, Zinc-induced antibiotic resistance in activated sludge bioreactors, Water Res., 44, 3829, 10.1016/j.watres.2010.04.041 · DOI
  14. Berg, 2005, Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field, Lett. Appl. Microbiol., 40, 146, 10.1111/j.1472-765X.2004.01650.x · DOI
  15. Stepanauskas, 2006, Coselection for microbial resistance to metals and antibiotics in freshwater microcosms, Environ. Microbiol., 8, 1510, 10.1111/j.1462-2920.2006.01091.x · DOI
  16. Knapp, 2011, Antibiotic resistance gene abundances correlate with metal and geochemical conditions in archived Scottish soils, PLoS ONE, 6, e27300, 10.1371/journal.pone.0027300 · DOI
  17. Su, 2012, Draft genome sequence of a novel bacterial strain, LSJC7, belonging to the family Enterobacteriaceae with dual resistance to arsenic and tetracycline, J. Bacteriol., 194, 7005, 10.1128/JB.01652-12 · DOI
  18. Cuebas, 2011, Isolation and characterization of an arsenic resistant Geobacillus kaustophilus strain from geothermal soils, J. Basic Microb., 51, 364, 10.1002/jobm.201000314 · DOI
  19. Lin, 2007, ArsD: An As(III) metallochaperone for the ArsAB As(III)-translocating ATPase, J. Bioenerg. Biomembr., 39, 453, 10.1007/s10863-007-9113-y · DOI
  20. Schwarz, 2010, Editorial: Assessing the antimicrobial susceptibility of bacteria obtained from animals, J. Antimicrob. Chemother., 65, 601, 10.1093/jac/dkq037 · DOI
  21. Hill, 2000, Growth promotion effects and plasma changes from feeding high dietary concentrations of zinc and copper to weanling pigs (regional study), J. Anim. Sci., 78, 1010, 10.2527/2000.7841010x · DOI
  22. Katouli, 1999, The effect of zinc oxide supplementation on the stability of the intestinal flora with special reference to composition of coliforms in weaned pigs, J. Appl. Microbiol., 87, 564, 10.1046/j.1365-2672.1999.00853.x · DOI
  23. Liu, 2015, Arsenic pollution of agricultural soils by concentrated China animal feeding operations (CAFOs), Chemosphere, 119, 273, 10.1016/j.chemosphere.2014.06.067 · DOI
  24. Rodriguez, 2014, Bioavailability of in-feed tetracyclines is influenced to a greater extent by crude protein rather than calcium, Anim. Feed Sci. Technol., 198, 323, 10.1016/j.anifeedsci.2014.09.027 · DOI
  25. Webber, 2003, The importance of efflux pumps in bacterial antibiotic resistance, J. Antimicrob. Chemother., 51, 9, 10.1093/jac/dkg050 · DOI
  26. Qiao, 2012, Fate of tetracyclines in swine manure of three selected swine farms in China, J. Environ. Sci., 24, 1047, 10.1016/S1001-0742(11)60890-5 · DOI
  27. Ji, 2012, Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai; China, J. Hazard. Mater., 235, 178, 10.1016/j.jhazmat.2012.07.040 · DOI
  28. Garbarino, 2003, Environmental fate of roxarsone in poultry litter. I. Degradation of roxarsone during composting, Environ. Sci. Technol., 37, 1509, 10.1021/es026219q · DOI
  29. Ghosh, 2007, The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria, ISME J., 1, 191, 10.1038/ismej.2007.31 · DOI
  30. Pruden, 2012, Correlation between upstream human activities and riverine antibiotic resistance genes, Environ. Sci. Technol., 46, 11541, 10.1021/es302657r · DOI
  31. Wei, 2010, A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China, Microchem. J., 94, 99, 10.1016/j.microc.2009.09.014 · DOI
  32. Finley, 2013, The scourge of antibiotic resistance: The important role of the environment, Clin. Infect. Dis., 57, 704, 10.1093/cid/cit355 · DOI · Paper page
  33. Nies, 1999, Microbial heavy-metal resistance, Appl. Microbiol. Biotechnol., 51, 730, 10.1007/s002530051457 · DOI
  34. Gullberg, 2014, Selection of a multidrug resistance plasmid by sublethal levels of antibiotics and heavy metals, MBio, 5, e01918-14, 10.1128/mBio.01918-14 · DOI
  35. Fang, 2014, Concentrations and health risks of lead, cadmium, arsenic, and mercury in rice and edible mushrooms in China, Food Chem., 147, 147, 10.1016/j.foodchem.2013.09.116 · DOI
  36. Smith, 2000, Contamination of drinking-water by arsenic in Bangladesh: A public health emergency, Bull. World Health Organ., 78, 1093
  37. Harris, 2011, Heavy metal and pesticide content in commonly prescribed individual raw Chinese Herbal Medicines, Sci. Total Environ., 409, 4297, 10.1016/j.scitotenv.2011.07.032 · DOI
  38. Mallik, 2012, Proteomic analysis of arsenite—Mediated multiple antibiotic resistance in Yersinia enterocolitica biovar 1A, J. Basic Microb., 52, 306, 10.1002/jobm.201100109 · DOI
  39. Caille, 2007, A copper-activated two-component system interacts with zinc and imipenem resistance in Pseudomonas aeruginosa, J. Bacteriol., 189, 4561, 10.1128/JB.00095-07 · DOI
  40. Hernandez, 1998, Metal accumulation and vanadium-induced multidrug resistance by environmental isolates of Escherichia hermannii and Enterobacter cloacae, Appl. Environ. Microbiol., 64, 4317, 10.1128/AEM.64.11.4317-4320.1998 · DOI
  41. Nishino, 2007, Regulation of multidrug efflux systems involved in multidrug and metal resistance of Salmonella enterica serovar typhimurium, J. Bacteriol., 189, 9066, 10.1128/JB.01045-07 · DOI
  42. Harrison, 2009, Chromosomal antioxidant genes have metal ion-specific roles as determinants of bacterial metal tolerance, Environ. Microbiol., 11, 2491, 10.1111/j.1462-2920.2009.01973.x · DOI
  43. Okusu, 1996, AcrAB efflux pump plays a major role in the antibiotic resistance phenotype of Escherichia coli multiple-antibiotic-resistance (Mar) mutants, J. Bacteriol., 178, 306, 10.1128/jb.178.1.306-308.1996 · DOI
  44. Hao, 2014, The multiple antibiotic resistance regulator MarR is a copper sensor in Escherichia coli, Nat. Chem. Biol., 10, U21, 10.1038/nchembio.1380 · DOI
  45. Zhou, 2015, Combined toxic effects of heavy metals and antibiotics on a Pseudomonas fluorescens strain ZY2 isolated from swine wastewater, Int. J. Mol. Sci., 16, 2839, 10.3390/ijms16022839 · DOI
  46. Zhang, 2011, Adsorption of tetracycline on soil and sediment: Effects of pH and the presence of Cu(II), J. Harzad. Mater., 190, 856, 10.1016/j.jhazmat.2011.04.017 · DOI
  47. Tong, 2015, Joint toxicity of tetracycline with copper(II) and cadmium(II) to Vibrio fischeri: Effect of complexation reaction, Ecotoxicology, 24, 346, 10.1007/s10646-014-1383-7 · DOI
  48. Winkler, 2013, Silver enhances antibiotic activity against gram-negative bacteria, Sci. Transl. Med., 5, 190ra81
  49. Anthony, 2012, Antimicrobial Textiles, Handbook of Experimental Pharmacology, Volume 211, 135, 10.1007/978-3-642-28951-4_9 · DOI
  50. Arias, 2009, Antibiotic-resistant bugs in the 21st century—A clinical super-challenge, N. Engl. J. Med., 360, 439, 10.1056/NEJMp0804651 · DOI
  51. Zhang, 2011, Occurrence of selected antibiotics in Jiulongjiang River in various seasons, South China, J. Environ. Monit., 13, 1953, 10.1039/c0em00765j · DOI

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Metadata

Authors
Chen, S., Li, X., Sun, G., Zhang, Y., Su, J., & Ye, J.
Venue
International Journal of Molecular Sciences
Publisher
MDPI AG
Published
2015-09-29
Volume
16
Issue
10
Pages
23390-23404
ISSN
1422-0067
Cited by
128
References
1
Language
en
Funders
National Natural Science Foundation of China (21210008, 41430858)

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