Physiological and transcriptional response of Bacillus cereus treated with low-temperature nitrogen gas plasma

Journal of Applied Microbiology

Volumn 115, Issue 3, 2013, Pages 689-702

  Mols, M ^a,b   Mastwijk, H ^a   Nierop Groot, M ^a   Abee, T ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Atmospheric pressure; Bacterial inactivation; Low temperature plasma; Microarray analysis; Surface disinfection

Indexed keywords

ATMOSPHERIC TEMPERATURE; BACILLUS CEREUS; BACTERIOLOGY; CYTOLOGY; GASES; GENE EXPRESSION; NITROGEN PLASMA; OPTICAL EMISSION SPECTROSCOPY; OXYGEN; PHYSIOLOGICAL MODELS; PHYSIOLOGY; RNA;

BACTERIAL INACTIVATION; CELL-BE; CELL/B.E; CELL/BE; LOW TEMPERATURE PLASMAS; LOW-TEMPERATURE NITROGEN; MICROARRAY ANALYSIS; NITROGEN GAS PLASMA; SURFACE DISINFECTION; VEGETATIVE CELLS;

ATMOSPHERIC PRESSURE;

AGAR; BACTERIAL RNA; HYDROGEN PEROXIDE; HYDROXYL GROUP; NITROGEN; PEROXYNITRITE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; TRANSCRIPTOME;

FLUORESCENCE; FREE RADICAL; LOW TEMPERATURE; MICROBIAL COMMUNITY; OXIDATION; RNA; ULTRAVIOLET RADIATION;

ANTIBACTERIAL ACTIVITY; ARTICLE; ATMOSPHERIC PRESSURE; BACILLUS CEREUS; BACTERIAL CELL; BACTERIAL GROWTH; CELL SURVIVAL; COLONY FORMING UNIT; CONTROLLED STUDY; DNA DAMAGE; DNA MICROARRAY; FLAME PHOTOMETRY; FLUORESCENCE ANALYSIS; GENE EXPRESSION; LOW TEMPERATURE PROCEDURES; NONHUMAN; OXIDATIVE STRESS; RNA ANALYSIS; RNA EXTRACTION; RNA ISOLATION; ULTRAVIOLET RADIATION;

BACILLUS CEREUS; BACTERIA (MICROORGANISMS);

ATMOSPHERIC PRESSURE; BACTERIAL INACTIVATION; LOW-TEMPERATURE PLASMA; MICROARRAY ANALYSIS; SURFACE DISINFECTION;

ANTI-BACTERIAL AGENTS; BACILLUS CEREUS; COLD TEMPERATURE; DECONTAMINATION; DNA REPAIR; GENE EXPRESSION PROFILING; NITROGEN; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLASMA GASES; TRANSCRIPTOME; ULTRAVIOLET RAYS;

EID: 84881668690     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12278     Document Type: Article

References (37)

1. Abee, T., Wels, M., de Been, M. and den Besten, H. (2011) From transcriptional landscapes to the identification of biomarkers for robustness. Microb Cell Fact 10(Suppl 1), S9.
2. Andersson, A., Ronner, U. and Granum, P.E. (1995) What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens? Int J Food Microbiol 28, 145-155.
3. Blakistone, B., Chuyate, R., Kautter, D. Jr, Charbonneau, J. and Suit, K. (1999) Efficacy of oxonia active against selected spore formers. J Food Prot 62, 262-267.
4. Blom, E.J., Bosman, D.W., van Hijum, S.A., Breitling, R., Tijsma, L., Silvis, R., Roerdink, J.B. and Kuipers, O.P. (2007) FIVA: Functional Information Viewer and Analyzer extracting biological knowledge from transcriptome data of prokaryotes. Bioinformatics 23, 1161-1163.
5. Bottone, E.J. (2010) Bacillus cereus, a volatile human pathogen. Clin Microbiol Rev 23, 382-398.
6. Ceragioli, M., Mols, M., Moezelaar, R., Ghelardi, E., Senesi, S. and Abee, T. (2010) Comparative transcriptomic and phenotypic analysis of the responses of Bacillus cereus to various disinfectant treatments. Appl Environ Microbiol 76, 3352-3360.
7. Daeschlein, G., von Woedtke, T., Kindel, E., Brandenburg, R., Weltmann, K.D. and Jünger, M. (2010) Antibacterial activity of an atmospheric pressure plasma jet against relevant wound pathogens in vitro on a simulated wound environment. Plasma Process Polym 7, 224-230.
8. Deilmann, M., Halfmann, H., Bibinov, N., Wunderlich, J. and Awakowicz, P. (2008) Low-pressure microwave plasma sterilization of polyethylene terephthalate bottles. J Food Prot 71, 2119-2123.
9. Deng, S., Ruan, R., Mok, C.K., Huang, G., Lin, X. and Chen, P. (2007) Inactivation of Escherichia coli on almonds using nonthermal plasma. J Food Sci 72, M62-M66.
10. Ermolaeva, S.A., Varfolomeev, A.F., Chernukha, M.Y., Yurov, D.S., Vasiliev, M.M., Kaminskaya, A.A., Moisenovich, M.M., Romanova, J.M. et al. (2011) Bactericidal effects of non-thermal argon plasma in vitro, in biofilms and in the animal model of infected wounds. J Med Microbiol 60, 75-83.
11. Goosen, N. and Moolenaar, G.F. (2008) Repair of UV damage in bacteria. DNA Repair (Amst) 7, 353-379.
12. Heinlin, J., Isbary, G., Stolz, W., Morfill, G., Landthaler, M., Shimizu, T., Steffes, B., Nosenko, T. et al. (2011) Plasma applications in medicine with a special focus on dermatology. J Eur Acad Dermatol Venereol 25, 1-11.
13. Hsiao, A., Ideker, T., Olefsky, J.M. and Subramaniam, S. (2005) VAMPIRE microarray suite: a web-based platform for the interpretation of gene expression data. Nucleic Acids Res 33, W627-W632.
14. Jensen, G.B., Hansen, B.M., Eilenberg, J. and Mahillon, J. (2003) The hidden lifestyles of Bacillus cereus and relatives. Environ Microbiol 5, 631-640.
15. Koulik, P., Begounov, S. and Goloviatinskii, S. (1999) Atmospheric plasma sterilization and deodorization of dielectric surfaces. Plasma Chem Plasma Process 19, 311-326.
16. Lado, B.H. and Yousef, A.E. (2002) Alternative food-preservation technologies: efficacy and mechanisms. Microbes Infect 4, 433-440.
17. Laouami, S., Messaoudi, K., Alberto, F., Clavel, T. and Duport, C. (2011) Lactate dehydrogenase A promotes communication between carbohydrate catabolism and virulence in Bacillus cereus. J Bacteriol 193, 1757-1766.
18. Lee, K.Y., Park, B.J., Lee, D.H., Lee, I.S., Hyun, S.O., Chung, K.H. and Park, J.C. (2005) Sterilization of Escherichia coli and MRSA using microwave-induced argon plasma at atmospheric pressure. Surf Coat Technol 193, 35-38.
19. Machala, Z., Janda, M., Hansel, K., Jedlovsky, I., Lestinska, L., Foltin, V., Martisovits, V. and Morvova, M. (2007) Emission spectroscopy of atmospheric pressure plasmas for bio-medical and environmental applications. J Mol Spectrosc 243, 194-201.
20. Mastwijk, H.C., Wichers, H.J., Dijk, C. and Schuten, H.J. (2009). Observation of free hole gases at ambient conditions. Condensed Matter: Strongly Correlated Electrons, pp. 1-14. arXiv:0711.4737v2.
21. Moisan, M., Barbeau, J., Moreau, S., Pelletier, J., Tabrizian, M. and Yahia, L.H. (2001) Low-temperature sterilization using gas plasmas: a review of the experiments and an analysis of the inactivation mechanisms. Int J Pharm 226, 1-21.
22. Mols, M. and Abee, T. (2011) Primary and secondary oxidative stress in Bacillus. Environ Microbiol 13, 1387-1394.
23. Mols, M., van Kranenburg, R., van Melis, C.C., Moezelaar, R. and Abee, T. (2010) Analysis of acid-stressed Bacillus cereus reveals a major oxidative response and inactivation-associated radical formation. Environ Microbiol 12, 873-885.
24. Mols, M., Ceragioli, M. and Abee, T. (2011) Heat stress leads to superoxide formation in Bacillus cereus detected using the fluorescent probe MitoSOX. Int J Food Microbiol 151, 119-122.
25. Niemira, B.A. (2012) Cold plasma decontamination of foods. Annu Rev Food Sci Technol 3, 125-142.
26. Niemira, B.A. and Sites, J. (2008) Cold plasma inactivates Salmonella Stanley and Escherichia coli O157:H7 inoculated on golden delicious apples. J Food Prot 71, 1357-1365.
27. Noriega, E., Shama, G., Laca, A., Diaz, M. and Kong, M.G. (2011) Cold atmospheric gas plasma disinfection of chicken meat and chicken skin contaminated with Listeria innocua. Food Microbiol 28, 1293-1300.
28. Roth, S., Feichtinger, J. and Hertel, C. (2010) Characterization of Bacillus subtilis spore inactivation in low-pressure, low-temperature gas plasma sterilization processes. J Appl Microbiol 108, 521-531.
29. Saeed, A.I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M. et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374-378.
30. Saeed, A.I., Bhagabati, N.K., Braisted, J.C., Liang, W., Sharov, V., Howe, E.A., Li, J., Thiagarajan, M. et al. (2006) TM4 microarray software suite. Methods Enzymol 411, 134-193.
31. van Schaik, W., van der Voort, M., Molenaar, D., Moezelaar, R., de Vos, W.M. and Abee, T. (2007) Identification of the sigmaB regulon of Bacillus cereus and conservation of sigmaB-regulated genes in low-GC-content Gram-positive bacteria. J Bacteriol 189, 4384-4390.
32. Setsukinai, K., Urano, Y., Kakinuma, K., Majima, H.J. and Nagano, T. (2003) Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J Biol Chem 278, 3170-3175.
33. Sharma, A., Collins, G. and Pruden, A. (2009) Differential gene expression in Escherichia coli following exposure to nonthermal atmospheric pressure plasma. J Appl Microbiol 107, 1440-1449.
34. Sladek, R.E.J., Stoffels, E., Walraven, R., Tielbeek, P.J.A. and Koolhove, R.A. (2004) Plasma treatment of dental cavities: a feasibility study. IEEE Trans Plasma Sci 32, 1540-1543.
35. Stenfors Arnesen, L.P., Fagerlund, A. and Granum, P.E. (2008) From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 32, 579-606.
36. Winter, T., Winter, J., Polak, M., Kusch, K., Mäder, U., Sietmann ., R., Ehlbeck, J., van Hijum, S. et al. (2011) Characterization of the global impact of low temperature gas plasma on vegetative microorganisms. Proteomics 11, 3518-3530.
37. Yang, B., Chen, J., Yu, Q., Li, H., Lin, M., Mustapha, A., Hong, L. and Wang, Y. (2011) Oral bacterial deactivation using a low-temperature atmospheric argon plasma brush. J Dent 39, 48-56.