Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Antimicrobial Effect of 2-Phenylethynyl-Butyltellurium in Escherichia coli and Its Association with Oxidative Stress

  • Pinheiro, Franciane Cabral (Laboratorio de Avaliacoes Farmacologicas e Toxicologicas aplicadas as Moleculas Bioativas - Unipampa, Universidade Federal do Pampa - Campus Itaqui) ;
  • Bortolotto, Vandreza Cardoso (Laboratorio de Avaliacoes Farmacologicas e Toxicologicas aplicadas as Moleculas Bioativas - Unipampa, Universidade Federal do Pampa - Campus Itaqui) ;
  • Araujo, Stifani Machado (Laboratorio de Avaliacoes Farmacologicas e Toxicologicas aplicadas as Moleculas Bioativas - Unipampa, Universidade Federal do Pampa - Campus Itaqui) ;
  • Poetini, Marcia Rosula (Laboratorio de Avaliacoes Farmacologicas e Toxicologicas aplicadas as Moleculas Bioativas - Unipampa, Universidade Federal do Pampa - Campus Itaqui) ;
  • Sehn, Carla Pohl (Laboratorio de Avaliacoes Farmacologicas e Toxicologicas aplicadas as Moleculas Bioativas - Unipampa, Universidade Federal do Pampa - Campus Itaqui) ;
  • Neto, Jose S.S. (Laboratorio de Sintese, Reatividade e Avaliacao Farmacologica e Toxicologica de Organocalcogenios, Centro de Ciencias Naturais e Exatas, Universidade Federal de Santa Maria) ;
  • Zeni, Gilson (Laboratorio de Sintese, Reatividade e Avaliacao Farmacologica e Toxicologica de Organocalcogenios, Centro de Ciencias Naturais e Exatas, Universidade Federal de Santa Maria) ;
  • Prigol, Marina (Laboratorio de Avaliacoes Farmacologicas e Toxicologicas aplicadas as Moleculas Bioativas - Unipampa, Universidade Federal do Pampa - Campus Itaqui)
  • Received : 2018.02.02
  • Accepted : 2018.05.11
  • Published : 2018.07.28
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Abstract

This study aimed to evaluate the antimicrobial activity of 2-phenylethynyl-butyltellurium (PEBT) in Escherichia coli and the relation to its pro-oxidant effect. For this, we carried out the disk diffusion test, minimum inhibitory concentration (MIC) assay, and survival curve analysis. We also measured the level of extracellular reactive oxygen species (ROS), activity of the antioxidant enzymes superoxide dismutase (SOD) and catalase (CAT), and level of non-protein thiols (NPSH). PEBT at 1.28 and 0.128 mg/disk exhibited antimicrobial capability in the disk diffusion test, with an MIC value of 1.92 mg/ml, whereas PEBT at 0.96, 1.92, and 3.84 mg/ml inhibited bacterial growth after a 9-h exposure. PEBT at 3.84, 1.92, and 0.96 mg/ml increased extracellular ROS production, decreased the intracellular NPSH level, and reduced the SOD and CAT activities. Glutathione or ascorbic acid in the medium protected the bacterial cells from the antimicrobial effect of PEBT. In conclusion, PEBT exhibited antimicrobial activity against E. coli, involving the generation of ROS, oxidation of NPSH, and reduction of the antioxidant defenses in the bacterial cells.

Keywords

References

  1. Holvoet K, Sampers I, Callens B, Dewulf J, Uyttendaele M. 2013. Moderate prevalence of antimicrobial resistance in Escherichia coli isolates from lettuce, irrigation water, and soil. Appl. Environ. Microbiol. 79: 6677-6683. https://doi.org/10.1128/AEM.01995-13
  2. Matuschek E, Brown DF, Kahlmeter G. 2014. Development of the EUCAST disk diffusion antimicrobial susceptibility testing method and its implementation in routine microbiology laboratories. Clin. Microbiol. Infect. 20: 255-266. https://doi.org/10.1111/1469-0691.12373
  3. Andremont A. 2001. The future control of bacterial resistance to antimicrobial agents. Am. J. Infect. Control 29: 256-258. https://doi.org/10.1067/mic.2001.115672
  4. Pesarico AP, Sartori G, dos Santos CFA, Neto JSS, Bortolotto V, Santos RCV, et al. 2013. 2,2-Dithienyl diselenide pro-oxidant activity accounts for antibacterial and antifungal activities. Microbiol. Res. 168: 563-568. https://doi.org/10.1016/j.micres.2013.04.009
  5. Oloketuyi SF, Khan F. 2017. Strategies for biofilm inhibition and virulence attenuation of foodborne pathogen-Escherichia coli O157:H7. Curr. Microbiol. 74: 1477-1489. https://doi.org/10.1007/s00284-017-1314-y
  6. Albesa I, Becerra MC, Battan PC, Paez PL. 2004. Oxidative stress involved in the antibacterial action of different antibiotics. Biochem. Biophys. Res. Commun. 317: 605-609. https://doi.org/10.1016/j.bbrc.2004.03.085
  7. Choia H, Yanga Z, Weisshaar JC. 2015. Single-cell, real-time detection of oxidative stress induced in Escherichia coli by the antimicrobial peptide CM15. Proc. Natl. Acad. Sci. USA 112: 303-310. https://doi.org/10.1073/pnas.1417703112
  8. Paez PL, Bazan CM, Bongiovanni ME, Toneatto J, Albesa I, Becerra MC, et al. 2013. Oxidative stress and antimicrobial activity of chromium(III) and ruthenium(II) complexes on Staphylococcus aureus and Escherichia coli. Biomed. Res. Int. 2013: 906912.
  9. Semchyshyn H, Bagnyukova T, Storey KB, Lushchak V. 2005. Hydrogen peroxide increases the activities of soxRS regulon enzymes and the levels of oxidized proteins and lipids in Escherichia coli. Cell Biol. Int. Rep. 29: 898-902. https://doi.org/10.1016/j.cellbi.2005.08.002
  10. Chasteen TG, Fuentes DE, Tantalean JC, Vasquez CC. 2009. Tellurite: history, oxidative stress, and molecular mechanisms of resistance. FEMS Microbiol. Rev. 33: 820-832. https://doi.org/10.1111/j.1574-6976.2009.00177.x
  11. Zhang Y, Meng D, Wang Z, Guo H, Wang Y, Wang X, et al. 2012. Oxidative stress response in atrazine-degrading bacteria exposed to atrazine. J. Hazard. Mater. 30: 434-438.
  12. Aradska J, Smidak R, Turkovicova L, Turna J, Lubec G. 2013. Proteomic differences between tellurite-sensitive and tellurite-resistant E. coli. PLoS One 8: e78010. https://doi.org/10.1371/journal.pone.0078010
  13. Cabiscol E, Tamarit J, Ros J. 2000. Oxidative stress in bacteria and protein damage by reactive oxygen species. Int. Microbiol. 3: 3-8.
  14. Vásquez WA, Lagunas MJ, Arenas FA, Pinto CA, Cornejo FA, Wansapura PT, et al. 2014. Tellurite reduction by Escherichia coli NDH-II dehydrogenase results in superoxide production in membranes of toxicant-exposed cells. Biometals 27: 237-246. https://doi.org/10.1007/s10534-013-9701-8
  15. Vasquez WA, Lagunas MJ, Cornejo FA, Pinto CA, Arenas FA, Vasquez CC. 2015. Tellurite-mediated damage to the Escherichia coli NDH-dehydrogenases and terminal oxidases in aerobic conditions. Arch. Biochem. Biophys. 566: 67-75. https://doi.org/10.1016/j.abb.2014.10.011
  16. Taylor DE. 1999. Bacterial tellurite resistance. Trends Microbiol. 7: 111-115. https://doi.org/10.1016/S0966-842X(99)01454-7
  17. Turner RJ, Weiner JH, Taylor DE. 1999. Tellurite-mediated thiol oxidation in Escherichia coli. J. Microbiol. 145: 2549-2557. https://doi.org/10.1099/00221287-145-9-2549
  18. Cunha RLOR, Gouvea IE, Juliano L. 2009. A glimpse on biological activities of tellurium compounds. An. Acad. Bras Cienc. 81: 393-407. https://doi.org/10.1590/S0001-37652009000300006
  19. Avila DS, Beque MC, Folmer V, Braga AL, Zeni G, Nogueira CW, et al. 2006. Diethyl 2-phenyl-2 tellurophenyl vinylphosphonate: an organotellurium compound with low toxicity. Toxicology 224: 100-107. https://doi.org/10.1016/j.tox.2006.04.027
  20. Quines CB, Rosa SG, Neto JS, Zeni G, Nogueira CW. 2013. Phenylethynyl-butyltellurium inhibits the sulfhydryl enzyme $Na^{+},\;K^{+}$ ATPase: an effect dependent on the tellurium atom. Biol. Trace Elem. Res. 155: 261-266. https://doi.org/10.1007/s12011-013-9781-x
  21. Quines CB, Rocha JT, Pesarico AP, Neto, JS, Zeni G, Nogueira CW. 2015. Involvement of the serotonergic system in the anxiolytic-like effect of 2-phenylethynyl-butyltellurium in mice. Behav. Brain Res. 277: 221-227. https://doi.org/10.1016/j.bbr.2014.05.071
  22. Souza AC, Luchese C, Neto JS, Nogueira CW. 2009. Antioxidant effect of a novel class of telluroacetilene compounds: studies in vitro and in vivo. Life Sci. J. 84: 351-357. https://doi.org/10.1016/j.lfs.2008.12.021
  23. Puntel RL, Roos D, Seeger RL, Rocha JB. 2012. Organochalcogens inhibit mitochondrial complexes I and II in rat brain: possible implications for neurotoxicity. Neurotox. Res. 24: 109-118.
  24. Puntel RL, Roos D, Seeger RL, Rocha JB. 2013. Mitrochondrial inhibition by different organochalcogens. Toxicol. In Vitro 27: 59-79. https://doi.org/10.1016/j.tiv.2012.10.011
  25. Souza AC, Acker CI, Gai BM, Neto JS, Nogueira CW. 2012. 2-Phenylethynyl-butyltellurium improves memory in mice. Neurochem. Int. 60: 409-414. https://doi.org/10.1016/j.neuint.2012.01.011
  26. Comasseto JV, Menezes PH, Stefani HA, Zeni G, Braga AL. 1996. Addition of hydrogen halides to acetylenic selenides. Synthesis of 1-halo-1-selenoalkenes. Tetrahedron 52: 9687-9702. https://doi.org/10.1016/0040-4020(96)00505-4
  27. Clinical and Laboratory Standards Institute. 2009. Performance standards for antimicrobial susceptibility testing; nineteenth informational supplement. CLSI, Wayne, PA.
  28. Politi ASF, Mello PCJ, Migliato FK, Neupomuceno ALA, Moreira DRR, Pietro CLRR. 2011. Antimicrobial, cytotoxic and antioxidant activities and determination of the total tannin content of bark extracts Endopleura uchi. Int. J. Mol. Sci. 12: 2757-2768. https://doi.org/10.3390/ijms12042757
  29. Goswami M, Mangoli SH, Jawali N. 2006. Involvement of reactive oxygen species in the action of ciprofloxacin against Escherichia coli. Antimicrob. Agents Chemother. 50: 949-54. https://doi.org/10.1128/AAC.50.3.949-954.2006
  30. Santos RC, dos Santos Alves CF, Scheneider T, Lopes LQ, Aurich C, Giongo JL, et al. 2012. Antimicrobial activity of Amazonian oils against Paenibacillus species. J. Invertebr. Pathol. 8: 109:265. https://doi.org/10.1016/j.jip.2011.12.002
  31. Socci DJ, Bjugstad KB, Jones HC, Pattisapu JV, Arendash GW. 1999. Evidence that oxidative stress is associated with the pathophysiology of inherited hydrocephalus in the H-Tx rat model. J. Neuropathol. Exp. Neurol. 155: 109-117. https://doi.org/10.1006/exnr.1998.6969
  32. Medeiros FO, Alves FG, Lisboa CR, Martins DR, Burkert CAV. 2008. Ondas ultrassonicas e perolas de vidro: um novo metodo de extracao de ${\beta}$-galactosidase para uso em laboratorio. Quim. Nova 31: 336-339. https://doi.org/10.1590/S0100-40422008000200028
  33. Ellman GL. 1959. Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82: 70-77. https://doi.org/10.1016/0003-9861(59)90090-6
  34. Kostyuk VA, Potapovich AI. 1989. Superoxide driven oxidation of quercetin and a simple sensitive assay for determination of superoxide dismutase. Biochem. Int. 19: 1117-1124.
  35. Aebi H. 1984. Catalase in vitro. Methods Enzymol. 105: 121-126.
  36. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
  37. Soni D, Gupta KP, Humar Y, Chandrashekharn TG. 2005. Antibacterial activity of some unsymmetrical diorganyltellurium (IV) dichlorides. Indian J. Biochem. Biophys. 42: 398-400.
  38. Imlay JA. 2008. Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem. 77: 755-776. https://doi.org/10.1146/annurev.biochem.77.061606.161055
  39. Imlay JA. 2013. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Rev. Nat. Microbiol. 11: 443-454. https://doi.org/10.1038/nrmicro3032
  40. Keele BB, McCord JM, Fridovich I. 1970. Superoxide dismutase from Escherichia coli B: a new manganese-containing enzyme. J. Biol. Chem. 245: 6176-6181.
  41. Loewen PC, Switala J, Triggs-Raine L. 1985. Catalase HPI and HPII in Escherichia coli are induced independently. Arch. Biochem. Biophys. 243: 144-149. https://doi.org/10.1016/0003-9861(85)90782-9
  42. Lin X, Xu X, Yang C, Zhao Y, Feng Z, Dong Y. 2009. Activities of antioxidant enzymes in three bacteria exposed to bensulfuron-methyl. Ecotoxicol. Environ. Saf. 72: 1899-1904. https://doi.org/10.1016/j.ecoenv.2009.04.016
  43. Lu Z, Sang L, Li Z, Min H. 2008. Catalase and superoxide dismutase activities in a Strenotrophomonas maltophilia WZ2 resistant to herbicide pollution. Ecotoxicol. Environ. Saf. 72: 136-143.
  44. Goswami M, Mangoli SH, Jawali N. 2006. Involvement of reactive oxygen species in the action of ciprofloxacin against Escherichia coli. Antimicrob. Agents Chemother. 50: 949-954. https://doi.org/10.1128/AAC.50.3.949-954.2006
  45. Becerra MC, Albesa I. 2002. Oxidative stress induced by ciprofloxacin in Staphylococcus aureus. Ccommunications 4: 1003-1007.

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