Sterilization of hydrogen peroxide resistant bacterial spores with stabilized chlorine dioxide

AMB Express

Volumn 5, Issue 1, 2015, Pages 1-6

  Friedline, Anthony ^a   Zachariah, Malcolm ^a   Middaugh, Amy ^a   Heiser, Matt ^b   Khanna, Neeraj ^b   Vaishampayan, Parag ^c   Rice, Charles V ^a  

^a UNIVERSITY OF OKLAHOMA   (United States)

^b Bio Cide International Inc   (United States)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Bacillus pumilus; Bacillus subtilis; Chlorine dioxide; Spore killing; Spores

Indexed keywords

CHLORINE DIOXIDE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACILLUS PUMILUS; BACILLUS SUBTILIS; BACTERIAL SPORE; BACTERIAL STERILIZATION; BACTERIAL SURVIVAL; BACTERIAL VIABILITY; BACTERIUM ISOLATION; COLONY FORMING UNIT; CONTROLLED STUDY; DISINFECTION; NONHUMAN; PHASE CONTRAST MICROSCOPY; QUANTITATIVE ASSAY; ULTRAVIOLET RADIATION;

EID: 84928330260     PISSN: None     EISSN: 21910855     Source Type: Journal    
DOI: 10.1186/s13568-015-0109-4     Document Type: Article

References (52)

1. Atrih A, Foster SJ (1999) The role of peptidoglycan structure and structural dynamics during endospore dormancy and germination. Antonie Van Leeuwenhoek 75(4):299–307
2. Atrih A, Zollner P, Allmaier G, Foster SJ (1996) Structural analysis of Bacillus subtilis 168 endospore peptidoglycan and its role during differentiation. J Bacteriol 178(21):6173–83
3. Best EL, Fawley WN, Parnell P, Wilcox MH (2010) The potential for airborne dispersal of Clostridium difficile from symptomatic patients. Clin Infect Dis 50(11):1450–7, doi:10.1086/652648
4. Beuchat LR, Pettigrew CA, Tremblay ME, Roselle BJ, Scouten AJ (2005) Lethality of chlorine, chlorine dioxide, and a commercial fruit and vegetable sanitizer to vegetative cells and spores of Bacillus cereus and spores of Bacillus thuringiensis. J Ind Microbiol Biotechnol 32(7):301–8, doi:10.1007/s10295-005-0212-7
5. Buhr TL, Young AA, Minter ZA, Wells CM, Shegogue DA (2011) Decontamination of a hard surface contaminated with Bacillus anthracis Δ Sterne and B. anthracis Ames spores using electrochemically generated liquid-phase chlorine dioxide (eClO2). J Appl Microbiol 111(5):1057–64, doi:10.1111/j.1365-2672.2011.05122.x
6. Chaudhry R (2011) Botulism: a diagnostic challenge. Ind J Med Res 134:10–2
7. Checinska A, Burbank M, Paszczynski AJ (2012) Protection of Bacillus pumilus spores by catalases. Appl Environ Microbiol 78(18):6413–22, doi:10.1128/AEM. 01211-12
8. Driks A (2002) Overview: Development in bacteria: spore formation in Bacillus subtilis. Cell Mol Life Sci 59(3):389–91
9. Driks A (2004) The Bacillus spore coat. Phytopathology 94(11):1249–51, doi:10.1094/PHYTO.2004.94.11.1249
10. Errington J (1993) Bacillus subtilis sporulation: regulation of gene expression and control of morphogenesis. Microbiol Rev 57(1):1–33
11. Foegeding PM, Hemstapat V, Giesbrecht FG (1986) Chlorine dioxide inactivation of Bacillus and Clostridium spores. J Food Sci 51(1):197–201, doi:10.1111/j.1365-2621.1986.tb10869.x
12. Gioia J, Yerrapragada S, Qin X, Jiang H, Igboeli OC, Muzny D, Dugan-Rocha S, Ding Y, Hawes A, Liu W, Perez L, Kovar C, Dinh H, Lee S, Nazareth L, Blyth P, Holder M, Buhay C, Tirumalai MR, Liu Y, Dasgupta I, Bokhetache L, Fujita M, Karouia F, Eswara Moorthy P, Siefert J, Uzman A, Buzumbo P, Verma A, Zwiya H, McWilliams BD, Olowu A, Clinkenbeard KD, Newcombe D, Golebiewski L, Petrosino JF, Nicholson WL, Fox GE, Venkateswaran K, Highlander SK, Weinstock GM (2007) Paradoxical DNA repair and peroxide resistance gene conservation in Bacillus pumilus SAFR-032. PLoS One 2(9):e928, doi:10.1371/journal.pone.0000928
13. Gordon G, Rosenblatt AA (2005) Chlorine dioxide: The current State of the art. Ozone-Sci Eng 27(3):203–7, doi:10.1080/01919510590945741
14. Gould CV, McDonald LC (2008) Bench-to-bedside review: Clostridium difficile colitis. Crit Care 12(1):203, doi:10.1186/cc6207
15. Hageman JH, Shankweiler GW, Wall PR, Franich K, McCowan GW, Cauble SM, Grajeda J, Quinones C (1984) Single, chemically defined Sporulation medium for Bacillus subtilis: growth, sporulation, and extracellular protease production. J Bacteriol 160(1):438–41
16. Higgins D, Dworkin J (2012) Recent progress in Bacillus subtilis sporulation. FEMS Microbiol Rev 36(1):131–48, doi:10.1111/j.1574-6976.2011.00310.x
17. Kerney KR, Schuerger AC (2011) Survival of Bacillus subtilis endospores on ultraviolet-irradiated rover wheels and Mars regolith under simulated Martian conditions. Astrobiology 11(5):477–85, doi:10.1089/ast.2011.0615
18. Kim BR, Anderson JE, Mueller SA, Gaines WA, Kendall AM (2002) Literature review–efficacy of various disinfectants against Legionella in water systems. Water Res 36(18):4433–44, doi:10.1016/S0043-1354(02)00188-4
19. Link L, Sawyer J, Venkateswaran K, Nicholson W (2004) Extreme spore UV resistance of Bacillus pumilus isolates obtained from an ultraclean spacecraft assembly facility. Microb Ecol 47(2):159–63, doi:10.1007/s00248-003-1029-4
20. Lowe JJ, Gibbs SG, Iwen PC, Smith PW, Hewlett AL (2013) Impact of chlorine dioxide gas sterilization on nosocomial organism viability in a hospital room. Int J Environ Res Public Health 10(6):2596–605, doi:10.3390/ijerph10062596
21. MacLeod-Glover N, Sadowski C (2010) Efficacy of cleaning products for C difficile: Environmental strategies to reduce the spread of Clostridium difficile–associated diarrhea in geriatric rehabilitation. Can Fam Physician 56(5):417–23
22. Magge A, Granger AC, Wahome PG, Setlow B, Vepachedu VR, Loshon CA, Peng L, Chen D, Yq L, Setlow P (2008) Role of dipicolinic acid in the Germination, stability, and viability of spores of Bacillus subtilis. J Bacteriol 190(14):4798–807, doi:10.1128/jb.00477-08
23. Mallidis CG, Scholefield J (1987) Relation of the heat resistance of bacterial spores to chemical composition and structure II. Relation to cortex and structure. J Appl Bacteriol 63(3):207–15
24. Moeller R, Setlow P, Reitz G, Nicholson WL (2009) Roles of small, acid-soluble spore proteins and core water content in survival of Bacillus subtilis spores exposed to environmental solar UV radiation. Appl Environ Microbiol 75(16):5202–8, doi:10.1128/aem. 00789-09
25. Moeller R, Schuerger AC, Reitz G, Nicholson WL (2012) Protective role of spore structural components in determining Bacillus subtilis spore resistance to simulated mars surface conditions. Appl Environ Microbiol 78(24):8849–53, doi:10.1128/AEM. 02527-12
26. Newcombe DA, Schuerger AC, Benardini JN, Dickinson D, Tanner R, Venkateswaran K (2005) Survival of spacecraft-associated microorganisms under simulated Martian UV irradiation. Appl Environ Microbiol 71(12):8147–56, doi:10.1128/aem. 71.12.8147-8156.2005
27. Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64(3):548–72
28. 2, electrolyzed oxidizing water, and chlorine dioxide gas. Food Sci Technol Int 14(5):437–41, doi:10.1177/1082013208098815
29. Paredes-Sabja D, Setlow P, Sarker MR (2011) Germination of spores of Bacillales and Clostridiales species: mechanisms and proteins involved. Trends Microbiol 19(2):85–94, doi:10.1016/j.tim.2010.10.004
30. Peniche AG, Savidge TC, Dann SM (2013) Recent insights into Clostridium difficile pathogenesis. Curr Opin Infect Dis 26(5):447–53, doi:10.1097/01.qco.0000433318.82618.c6
31. Piggot PJ, Hilbert DW (2004) Sporulation of Bacillus subtilis. Curr Opin Microbiol 7(6):579–86, 10.1016/j.mib.2004.10.001
32. Rastogi VK, Ryan SP, Wallace L, Smith LS, Shah SS, Martin GB (2010) Systematic evaluation of the efficacy of chlorine dioxide in decontamination of building interior surfaces contaminated with anthrax spores. Appl Environ Microbiol 76(10):3343–51, doi:10.1128/AEM. 02668-09
33. Riesenman PJ, Nicholson WL (2000) Role of the spore coat layers in Bacillus subtilis spore resistance to hydrogen peroxide, artificial UV-C, UV-B, and solar UV radiation. Appl Environ Microbiol 66(2):620–6, doi:10.1128/aem. 66.2.620-626.2000
34. Roberts K, Smith CF, Snelling AM, Kerr KG, Banfield KR, Sleigh PA, Beggs CB (2008) Aerial dissemination of Clostridium difficile spores. BMC Infect Dis 8:7, doi:10.1186/1471-2334-8-7
35. Schmid G, Kaufmann A (2002) Anthrax in Europe: its epidemiology, clinical characteristics, and role in bioterrorism. Clin Microbiol Infect 8(8):479–88
36. Schuerger AC, Mancinelli RL, Kern RG, Rothschild LJ, McKay CP (2003) Survival of endospores of Bacillus subtilis on spacecraft surfaces under simulated martian environments: implications for the forward contamination of Mars. Icarus 165(2):253–76, doi:10.1016/s0019-1035(03)00200-8
37. Setlow P (1988) Small, acid-soluble spore proteins of Bacillus species: structure, synthesis, genetics, function, and degradation. Annu Rev Microbiol 42:319–38, doi:10.1146/annurev.mi.42.100188.001535
38. Setlow P (2003) Spore germination. Curr Opin Microbiol 6(6):550–6, doi:10.1016/j.mib.2003.10.001
39. Setlow P (2006) Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J Appl Microbiol 101(3):514–25, doi:10.1111/j.1365-2672.2005.02736.x
40. Setlow B, Atluri S, Kitchel R, Koziol-Dube K, Setlow P (2006) Role of dipicolinic acid in resistance and stability of spores of Bacillus subtilis with or without DNA-protective α/β-Type small acid-soluble proteins. J Bacteriol 188(11):3740–7, doi:10.1128/jb.00212-06
41. Sharma VK, Sohn M (2012) Reactivity of chlorine dioxide with amino acids, peptides, and proteins. Environ Chem Lett 10(3):255–64, doi:10.1007/s10311-012-0355-5
42. Shemesh M, Kolter R, Losick R (2010) The biocide chlorine dioxide stimulates biofilm formation in Bacillus subtilis by activation of the histidine kinase KinC. J Bacteriol 192(24):6352–6, doi:10.1128/JB.01025-10
43. Spotts Whitney EA, Beatty ME, Taylor THJ, Weyant R, Sobel J, Arduino MJ, Ashford DA (2003) Inactivation of Bacillus anthracis spores. Emerg Infect Dis 9(6):623–7
44. Takamatsu H, Watabe K (2002) Assembly and genetics of spore protective structures. Cell Mol Life Sci 59(3):434–44
45. Tauveron G, Slomianny C, Henry C, Faille C (2006) Variability among Bacillus cereus strains in spore surface properties and influence on their ability to contaminate food surface equipment. Int J Food Microbiol 110(3):254–62, doi:10.1016/j.ijfoodmicro.2006.04.027
46. Tirumalai MR, Rastogi R, Zamani N, O’Bryant Williams E, Allen S, Diouf F, Kwende S, Weinstock GM, Venkateswaran KJ, Fox GE (2013) Candidate genes that may be responsible for the unusual resistances exhibited by Bacillus pumilus SAFR-032 spores. PLoS One 8(6):e66012, doi:10.1371/journal.pone.0066012
47. Vaishampayan PA, Rabbow E, Horneck G, Venkateswaran KJ (2012) Survival of Bacillus pumilus spores for a prolonged period of time in real space conditions. Astrobiology 12(5):487–97, doi:10.1089/ast.2011.0738
48. Venkateswaran K, Vaishampayan P, Cisneros J, Pierson D, Rogers S, Perry J (2014) International Space Station environmental microbiome — microbial inventories of ISS filter debris. Appl Microbiol Biotechnol 98(14):6453–66, doi:10.1007/s00253-014-5650-6
49. Warth AD, Strominger JL (1971) Structure of the peptidoglycan from vegetative cell walls of Bacillus subtilis. Biochemistry 10(24):4349–58
50. Warth AD, Strominger JL (1972) Structure of the Peptidoglycan from spores of Bacillus subtilis. Biochemistry 11(8):1389–96
51. Young SB, Setlow P (2003) Mechanisms of killing of Bacillus subtilis spores by hypochlorite and chlorine dioxide. J Appl Microbiol 95(1):54–67
52. Zhao J, Krishna V, Moudgil B, Koopman B (2008) Evaluation of endospore purification methods applied to Bacillus cereus. Sep Purif Technol 61(3):341–7, doi:10.1016/j.seppur.2007.11.002