Mycobacterium vaccae Adaptation to Disinfectants and Hand Sanitisers, and Evaluation of Cross-Tolerance with Antimicrobials
Abstract
:1. Introduction
2. Results
2.1. Membrane Fatty Acid Composition Induced by Disinfectants
2.2. Effect of the Culture Age during Exposure
2.3. Adaptation of M. vaccae Cells to Disinfectants
2.4. Tolerance of Disinfectant Adapted Cells to Antibiotics and Efflux Pump Inhibitors
3. Discussion
4. Materials and Methods
4.1. Bacterial Strain and Growth Conditions
4.2. Bacterial Growth in the Presence of Disinfectants
4.3. Bacterial Adaptation to Disinfectants and Hand Sanitisers
4.4. Fatty Acid Composition
4.5. Zeta Potential Measurements
4.6. Fluorescence Microscopy
4.7. Determination of Minimum Inhibitory Concentration
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Bell, K.S.; Philp, J.C.; Aw, D.W.J.; Christofi, N. The genus Rhodococcus. J. Appl. Microbiol. 1998, 85, 195–210. [Google Scholar] [CrossRef] [PubMed]
- de Carvalho, C.C.C.R.; Costa, S.; Fernandes, P.; Couto, I.; Viveiros, M. Membrane transport systems and the biodegradation potential and pathogenicity of genus Rhodococcus. Front. Physiol. 2014, 5. [Google Scholar] [CrossRef]
- Tauch, A.; Sandbote, J. The family Corynebacteriaceae. In The Prokaryotes: Actinobacteria; Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., Thompson, F., Eds.; Springer: Berlin/Heidelberg, Germany, 2014; pp. 239–277. ISBN 978-3-642-30138-4. [Google Scholar]
- Arenskötter, M.; Bröker, D.; Steinbüchel, A. Biology of the metabolically diverse genus Gordonia. Appl. Environ. Microbiol. 2004, 70, 3195–3204. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- World Health Organization. WHO Global Tuberculosis Report 2019; World Health Organization: Geneva, Switzerland, 2019; p. 283. ISBN 978-92-4-156571-4. [Google Scholar]
- Hachem, R.; Raad, I.; Rolston, K.; Whimbey, E.; Katz, R.; Tarrand, J.; Libshitz, H. Cutaneous and pulmonary infections caused by Mycobacterium vaccae. Clin. Infect. Dis. 1996, 23, 173–175. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huang, C.-Y.; Hsieh, W.-Y. Efficacy of Mycobacterium vaccae immunotherapy for patients with tuberculosis: A systematic review and meta-analysis. Hum. Vaccin. Immunother. 2017, 13, 1960–1971. [Google Scholar] [CrossRef] [Green Version]
- Lehrer, A.; Bressanelli, A.; Wachsmann, V.; Bottasso, O.; Bay, M.-L.; Singh, M.; Stanford, C.; Stanford, J. Immunotherapy with Mycobacterium vaccae in the treatment of psoriasis. FEMS Immunol. Med. Microbiol. 1998, 21, 71–77. [Google Scholar] [CrossRef] [Green Version]
- O’Brien, M.E.R.; Anderson, H.; Kaukel, E.; O’Byrne, K.; Pawlicki, M.; von Pawel, J.; Reck, M. SRL172 (killed Mycobacterium vaccae) in addition to standard chemotherapy improves quality of life without affecting survival, in patients with advanced non-small-cell lung cancer: Phase III results. Ann. Oncol. 2004, 15, 906–914. [Google Scholar] [CrossRef]
- Cananzi, F.C.M.; Mudan, S.; Dunne, M.; Belonwu, N.; Dalgleish, A.G. Long-term survival and outcome of patients originally given Mycobacterium vaccae for metastatic malignant melanoma. Hum. Vaccines Immunother. 2013, 9, 2427–2433. [Google Scholar] [CrossRef]
- Falkinham, J.O., III. Surrounded by mycobacteria: Nontuberculous mycobacteria in the human environment. J. Appl. Microbiol. 2009, 107, 356–367. [Google Scholar] [CrossRef]
- Brennan, P.J.; Nikaido, H. The envelope of mycobacteria. Annu. Rev. Biochem. 1995, 64, 29–63. [Google Scholar] [CrossRef]
- Dulberger, C.L.; Rubin, E.J.; Boutte, C.C. The mycobacterial cell envelope—A moving target. Nat. Rev. Microbiol. 2020, 18, 47–59. [Google Scholar] [CrossRef] [PubMed]
- Barry, C.E.; Lee, R.E.; Mdluli, K.; Sampson, A.E.; Schroeder, B.G.; Slayden, R.A.; Yuan, Y. Mycolic acids: Structure, biosynthesis and physiological functions. Prog. Lipid Res. 1998, 37, 143–179. [Google Scholar] [CrossRef] [Green Version]
- Batt, S.M.; Minnikin, D.E.; Besra, G.S. The thick waxy coat of mycobacteria, a protective layer against antibiotics and the host’s immune system. Biochem. J. 2020, 477, 1983–2006. [Google Scholar] [CrossRef] [PubMed]
- de Carvalho, C.C.C.R.; Cruz, A.; Angelova, B.; Fernandes, P.; Pons, M.N.; Pinheiro, H.M.; Cabral, J.M.S.; da Fonseca, M.M.R. Behaviour of Mycobacterium sp. NRRL B-3805 whole cells in aqueous, organic-aqueous and organic media studied by fluorescence microscopy. Appl. Microbiol. Biotechnol. 2004, 64, 695–701. [Google Scholar] [CrossRef] [PubMed]
- de Carvalho, C.C.C.R.; da Cruz, A.; Pons, M.N.; Pinheiro, H.; Cabral, J.M.S.; da Fonseca, M.M.R.; Ferreira, B.S.; Fernandes, P. Mycobacterium sp., Rhodococcus erythropolis, and Pseudomonas putida behavior in the presence of organic solvents. Microsc. Res. Tech. 2004, 64, 215–222. [Google Scholar] [CrossRef] [PubMed]
- de Carvalho, C.C.C.R.; Fernandes, P. Biocatalysis of steroids with Mycobacterium sp. in aqueous and organic media. Methods Mol. Biol. 2017, 1645, 313–320. [Google Scholar] [CrossRef] [PubMed]
- Pacífico, C.; Fernandes, P.; de Carvalho, C.C.C.R. Mycobacterial response to organic solvents and possible implications on cross-resistance with antimicrobial agents. Front. Microbiol. 2018, 9. [Google Scholar] [CrossRef] [Green Version]
- Melchior, D.L. Lipid phase transitions and regulation of membrane fluidity in prokaryotes. In Current Topics in Membranes and Transport; Bronner, F., Kleinteller, A., Eds.; Academic Press: Cambridge, MA, USA, 1982; Volume 17, pp. 263–316. [Google Scholar]
- Sinensky, M. Homeoviscous adaptation—A homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc. Natl. Acad. Sci. USA 1974, 71, 522–525. [Google Scholar] [CrossRef] [Green Version]
- Chapman, J.S. Disinfectant resistance mechanisms, cross-resistance, and co-resistance. Int. Biodeterior. Biodegrad. 2003, 51, 271–276. [Google Scholar] [CrossRef]
- Sundheim, G.; Langsrud, S.; Heir, E.; Holck, A.L. Bacterial resistance to disinfectants containing quaternary ammonium compounds. Int. Biodeterior. Biodegrad. 1998, 41, 235–239. [Google Scholar] [CrossRef]
- Jennings, M.C.; Minbiole, K.P.C.; Wuest, W.M. Quaternary ammonium compounds: Antimicrobial mainstay and platform for innovation to address bacterial resistance. ACS Infect. Dis. 2015, 1, 288–303. [Google Scholar] [CrossRef] [PubMed]
- Cortesia, C.; Bello, T.; Lopez, G.; Franzblau, S.; Waard, J.D.; Takiff, H. Use of green fluorescent protein labeled non-tuberculous mycobacteria to evaluate the activity quaternary ammonium compound disinfectants and antibiotics. Braz. J. Microbiol. 2017, 48, 151–158. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cortesia, C.; Lopez, G.J.; de Waard, J.H.; Takiff, H.E. The use of quaternary ammonium disinfectants selects for persisters at high frequency from some species of non-tuberculous mycobacteria and may be associated with outbreaks of soft tissue infections. J. Antimicrob. Chemother. 2010, 65, 2574–2581. [Google Scholar] [CrossRef] [PubMed]
- Shinoda, N.; Mitarai, S.; Suzuki, E.; Watanabe, M. Disinfectant-susceptibility of multi-drug-resistant Mycobacterium tuberculosis isolated in Japan. Antimicrob. Resist. Infect. Control 2016, 5, 3. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kohler, A.T.; Rodloff, A.C.; Labahn, M.; Reinhardt, M.; Truyen, U.; Speck, S. Evaluation of disinfectant efficacy against multidrug-resistant bacteria: A comprehensive analysis of different methods. Am. J. Infect. Control 2019, 47, 1181–1187. [Google Scholar] [CrossRef]
- Woo, P.C.Y.; Leung, K.-W.; Wong, S.S.Y.; Chong, K.T.K.; Cheung, E.Y.L.; Yuen, K.-Y. Relatively alcohol-resistant mycobacteria are emerging pathogens in patients receiving acupuncture treatment. J. Clin. Microbiol. 2002, 40, 1219–1224. [Google Scholar] [CrossRef] [Green Version]
- Pidot, S.J.; Gao, W.; Buultjens, A.H.; Monk, I.R.; Guerillot, R.; Carter, G.P.; Lee, J.Y.H.; Lam, M.M.C.; Grayson, M.L.; Ballard, S.A.; et al. Increasing tolerance of hospital Enterococcus faecium to handwash alcohols. Sci. Transl. Med. 2018, 10, eaar6115. [Google Scholar] [CrossRef] [Green Version]
- Heipieper, H.J.; de Bont, J.A. Adaptation of Pseudomonas putida S12 to ethanol and toluene at the level of fatty acid composition of membranes. Appl. Environ. Microbiol. 1994, 60, 4440–4444. [Google Scholar] [CrossRef] [Green Version]
- de Carvalho, C.C.C.R.; Parreño-Marchante, B.; Neumann, G.; da Fonseca, M.M.R.; Heipieper, H.J. Adaptation of Rhodococcus erythropolis DCL14 to growth on n-alkanes, alcohols and terpenes. Appl. Microbiol. Biotechnol. 2005, 67, 383–388. [Google Scholar] [CrossRef]
- Suutari, M.; Laakso, S. Microbial fatty acids and thermal adaptation. Crit. Rev. Microbiol. 1994, 20, 285–328. [Google Scholar] [CrossRef]
- de Carvalho, C.C.C.R.; Caramujo, M.J. The various roles of fatty acids. Molecules 2018, 23, 2583. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weber, F.J.; de Bont, J.A.M. Adaptation mechanisms of microorganisms to the toxic effects of organic solvents on membranes. Biochim. Biophys. Acta 1996, 1286, 225–245. [Google Scholar] [CrossRef]
- Kabelitz, N.; Santos, P.M.; Heipieper, H.J. Effect of aliphatic alcohols on growth and degree of saturation of membrane lipids in Acinetobacter calcoaceticus. FEMS Microbiol. Lett. 2003, 220, 223–227. [Google Scholar] [CrossRef] [Green Version]
- Hassell, J.E.; Fox, J.H.; Arnold, M.R.; Siebler, P.H.; Lieb, M.W.; Schmidt, D.; Spratt, E.J.; Smith, T.M.; Nguyen, K.T.; Gates, C.A.; et al. Treatment with a heat-killed preparation of Mycobacterium vaccae after fear conditioning enhances fear extinction in the fear-potentiated startle paradigm. Brain Behav. Immun. 2019, 81, 151–160. [Google Scholar] [CrossRef] [PubMed]
- Reber, S.O.; Siebler, P.H.; Donner, N.C.; Morton, J.T.; Smith, D.G.; Kopelman, J.M.; Lowe, K.R.; Wheeler, K.J.; Fox, J.H.; Hassell, J.E.; et al. Immunization with a heat-killed preparation of the environmental bacterium Mycobacterium vaccae promotes stress resilience in mice. Proc. Natl. Acad. Sci. USA 2016, 113, E3130–E3139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smith, D.G.; Martinelli, R.; Besra, G.S.; Illarionov, P.A.; Szatmari, I.; Brazda, P.; Allen, M.A.; Xu, W.; Wang, X.; Nagy, L.; et al. Identification and characterization of a novel anti-inflammatory lipid isolated from Mycobacterium vaccae, a soil-derived bacterium with immunoregulatory and stress resilience properties. Psychopharmacology 2019, 236, 1653–1670. [Google Scholar] [CrossRef]
- Yang, X.Y.; Chen, Q.F.; Li, Y.P.; Wu, S.M. Mycobacterium vaccae as adjuvant therapy to antituberculosis chemotherapy in never-treated tuberculosis patients: A meta-analysis. PLoS ONE 2011, 6, e23826. [Google Scholar] [CrossRef] [Green Version]
- Stanford, J.; Stanford, C. Mycobacteria and their world. Int. J. Mycobacteriol. 2012, 1, 3–12. [Google Scholar] [CrossRef] [Green Version]
- Claeys, T.A.; Robinson, R.T. The many lives of nontuberculous mycobacteria. J. Bacteriol. 2018, 200, e00739-17. [Google Scholar] [CrossRef] [Green Version]
- Pontiroli, A.; Khera, T.T.; Oakley, B.B.; Mason, S.; Dowd, S.E.; Travis, E.R.; Erenso, G.; Aseffa, A.; Courtenay, O.; Wellington, E.M.H. Prospecting environmental mycobacteria: Combined molecular approaches reveal unprecedented diversity. PLoS ONE 2013, 8, e68648. [Google Scholar] [CrossRef] [Green Version]
- Santos, R.; de Carvalho, C.C.C.R.; Stevenson, A.; Grant, I.R.; Hallsworth, J.E. Extraordinary solute-stress tolerance contributes to the environmental tenacity of mycobacteria. Environ. Microbiol. Rep. 2015, 7, 746–764. [Google Scholar] [CrossRef]
- Rastogi, N.; Barrow, W.W. Cell envelope constituents and the multifaceted nature of Mycobacterium avium pathogenicity and drug resistance. Res. Microbiol. 1994, 145, 243–252. [Google Scholar] [CrossRef]
- Nikaido, H.; Kim, S.-H.; Rosenberg, E.Y. Physical organization of lipids in the cell wall of Mycobacterium chelonae. Mol. Microbiol. 1993, 8, 1025–1030. [Google Scholar] [CrossRef]
- Dmitriev, B.A.; Ehlers, S.; Rietschel, E.T.; Brennan, P.J. Molecular mechanics of the mycobacterial cell wall: From horizontal layers to vertical scaffolds. Int. J. Med. Microbiol. 2000, 290, 251–258. [Google Scholar] [CrossRef]
- Bansal-Mutalik, R.; Nikaido, H. Mycobacterial outer membrane is a lipid bilayer and the inner membrane is unusually rich in diacyl phosphatidylinositol dimannosides. Proc. Natl. Acad. Sci. USA 2014, 111, 4958–4963. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ventola, C.L. The antibiotic resistance crisis: Part 1: Causes and threats. Pharm. Ther. 2015, 40, 277–283. [Google Scholar]
- Ghosh, S.; LaPara, T.M. The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME J. 2007, 1, 191–203. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kampf, G. Biocidal agents used for disinfection can enhance antibiotic resistance in Gram-negative species. Antibiotics 2018, 7, 110. [Google Scholar] [CrossRef] [Green Version]
- Gonçalves, F.D.A.; de Carvalho, C.C.C.R. Phenotypic modifications in Staphylococcus aureus cells exposed to high concentrations of vancomycin and teicoplanin. Front. Microbiol. 2016, 7, 13. [Google Scholar] [CrossRef]
- de Carvalho, C.C.C.R.; Marques, M.P.C.; Hachicho, N.; Heipieper, H.J. Rapid adaptation of Rhodococcus erythropolis cells to salt stress by synthesizing polyunsaturated fatty acids. Appl. Microbiol. Biotechnol. 2014, 98, 5599–5606. [Google Scholar] [CrossRef]
- Poger, D.; Caron, B.; Mark, A.E. Effect of methyl-branched fatty acids on the structure of lipid bilayers. J. Phys. Chem. B 2014, 118, 13838–13848. [Google Scholar] [CrossRef] [PubMed]
- Parenti, F. Structure and mechanism of action of teicoplanin. J. Hosp. Infect. 1986, 7, 79–83. [Google Scholar] [CrossRef]
- Kieser, K.J.; Baranowski, C.; Chao, M.C.; Long, J.E.; Sassetti, C.M.; Waldor, M.K.; Sacchettini, J.C.; Ioerger, T.R.; Rubin, E.J. Peptidoglycan synthesis in Mycobacterium tuberculosis is organized into networks with varying drug susceptibility. Proc. Natl. Acad. Sci. USA 2015, 112, 13087–13092. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nasiri, M.J.; Haeili, M.; Ghazi, M.; Goudarzi, H.; Pormohammad, A.; Imani Fooladi, A.A.; Feizabadi, M.M. New insights in to the intrinsic and acquired drug resistance mechanisms in mycobacteria. Front. Microbiol. 2017, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- de Keijzer, J.; Mulder, A.; de Haas, P.E.W.; de Ru, A.H.; Heerkens, E.M.; Amaral, L.; van Soolingen, D.; van Veelen, P.A. Thioridazine alters the cell-envelope permeability of Mycobacterium tuberculosis. J. Proteome Res. 2016, 15, 1776–1786. [Google Scholar] [CrossRef] [PubMed]
- Hsu, W.-H.; Kuo, C.-H.; Wang, S.S.W.; Lu, C.-Y.; Liu, C.-J.; Chuah, S.-K.; Kuo, F.-C.; Chen, Y.-H.; Huang, Y.-B.; Hou, M.-F.; et al. Acid suppressive agents and risk of Mycobacterium tuberculosis: Case-control study. BMC Gastroenterol. 2014, 14, 91. [Google Scholar] [CrossRef] [Green Version]
- Fernandes, P.; Ferreira, B.S.; Cabral, J.M.S. Solvent tolerance in bacteria: Role of efflux pumps and cross-resistance with antibiotics. Int. J. Antimicrob. Agents 2003, 22, 211–216. [Google Scholar] [CrossRef]
- Cortes, M.A.L.R.M.; de Carvalho, C.C.C.R. Effect of carbon sources on lipid accumulation in Rhodococcus cells. Biochem. Eng. J. 2015, 94, 100–105. [Google Scholar] [CrossRef]
- de Carvalho, C.C.C.R.; Fatal, V.; Alves, S.S.; da Fonseca, M.M.R. Adaptation of Rhodococcus erythropolis cells to high concentrations of toluene. Appl. Microbiol. Biotechnol. 2007, 76, 1423–1430. [Google Scholar] [CrossRef]
- de Carvalho, C.C.C.R.; Pons, M.-N.; da Fonseca, M.M.R. Principal Components Analysis as a tool to summarise biotransformation data: Influence on cells of solvent type and phase ratio. Biocatal. Biotransform. 2003, 21, 305–314. [Google Scholar] [CrossRef]
- CLSI. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fourth Informational Supplement; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2014. [Google Scholar]
Antibiotic/EPI | MIC (µg/mL) | ||
---|---|---|---|
Non-Adapted Cells | Adapted Cells | ||
Alcohol Gel | Aniosrub | ||
Levofloxacin | 0.6 | 1.25 | 5 |
Teicoplanin | >100 | >100 | >100 |
Thioridazine | 18.7 | 149 | >149 |
Omeprazole | 250 | 500 | 500 |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
de Carvalho, C.C.C.R.; Teixeira, R.; Fernandes, P. Mycobacterium vaccae Adaptation to Disinfectants and Hand Sanitisers, and Evaluation of Cross-Tolerance with Antimicrobials. Antibiotics 2020, 9, 544. https://doi.org/10.3390/antibiotics9090544
de Carvalho CCCR, Teixeira R, Fernandes P. Mycobacterium vaccae Adaptation to Disinfectants and Hand Sanitisers, and Evaluation of Cross-Tolerance with Antimicrobials. Antibiotics. 2020; 9(9):544. https://doi.org/10.3390/antibiotics9090544
Chicago/Turabian Stylede Carvalho, Carla C. C. R., Raquel Teixeira, and Pedro Fernandes. 2020. "Mycobacterium vaccae Adaptation to Disinfectants and Hand Sanitisers, and Evaluation of Cross-Tolerance with Antimicrobials" Antibiotics 9, no. 9: 544. https://doi.org/10.3390/antibiotics9090544