TECHNICAL PAPERS
Jul 1, 2008

Sequential Inactivation of Bacillus Subtilis Spores with Ultraviolet Radiation and Iodine

Publication: Journal of Environmental Engineering
Volume 134, Issue 7

Abstract

Bacillus subtilis spores were used as an indicator organism to characterize the effects of UV radiation and iodine, alone and in combination, as disinfectants for water. Spore exposures to UV radiation were conducted in shallow, well-mixed batch reactors under collimated beams. Three (essentially) monochromatic collimated UV sources were used in these experiments, with characteristic emission wavelengths of 222, 254, and 282nm . Iodine exposures were conducted in well-mixed batch reactors. Synergism was demonstrated when UV (at certain doses) and iodine were used as sequential disinfectants; synergism was attributed to UV-induced damage that enhanced the susceptibility of spores to iodine.

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Acknowledgments

The writers would like to acknowledge the NASA Specialized Center for Research and Training (NSCORT) for funding this research and Ushio America, Inc. for providing the excimer lampsNASA.

References

American Public Health Association/American Water Works Association/Water Environment Federation (APHA/AWWA/WEF). (1998). Standard methods for the examination of water and wastewater, 20th Ed., Washington, D.C.
Avery, S. V. (2006). “Microbial cell individuality and the underlying sources of heterogeneity.” Nat. Rev. Microbiol., 4(8), 577–587.
Bailey, G., Karp, F. S., and Sacks, L. E. (1965). “Ultraviolet-absorption spectra of dry bacterial spores.” J. Bacteriol., 89(4), 984–987.
Balaban, N. Q., Merrin, J., Chait, R., Kowalik, L., and Leibler, S. (2004). “Bacterial persistence as a phenotypic switch.” Science, 305(5690), 1622–1625.
Ballaster, N. A., and Malley, J. P. (2004). “Sequential disinfection of adenovirus type 2 with UV-chlorine-chloramine.” J. Am. Water Works Assoc., 96(10), 97–103.
Blatchley, E. R., III, Cole, K. A., and Hamilton, D. (2000). “Analysis of process performance in polychromatic UV disinfection systems.” Water Environment Federation Technical Exhibition and Conference (WEFTEC) 2000, 14–18.
Butkus, M. A., Labare, M. P., Starke, J. A., Moon, K., and Talbot, M. (2004). “Use of aqueous silver to enhance the inactivation of coliphage MS-2 with UV disinfection.” Appl. Environ. Microbiol., 70(5), 2646–2853.
Cho, M., Chung, H., and Yoon, J. (2003). “Quantitative evaluation of the synergistic sequential inactivation of Bacillus subtilis spores with ozone followed by chlorine.” Environ. Sci. Technol., 37(10), 2134–2138.
Cho, M., Kim, J., and Yoon, J. (2006). “Investigating synergism during sequential inactivation of Bacillus subtilis spores with several disinfectants.” Water Res., 40(15), 2911–2920.
Columbo, G. V., and Sauer, R. L. (1987). “Review of water disinfection techniques.” SAE Technical Paper Series, Paper No. 871488, Intersociety Conf. on Environmental Systems, Seattle, 1–5.
Corona-Vasquez, B., Rennecker, J. L., Driedger, A. M., and Mariñas, B. J. (2002). “Sequential inactivation of Cryptosporidium parvum oocysts with chlorine dioxide followed by free chlorine or monochloramine.” Water Res., 36(1), 178–188.
Cortezzo, D. E., Koziol-Dube, K., Setlow, B., and Setlow, P. (2004). “Treatment with oxidizing agents damages the inner membrane of spores of Bacillus subtilis and sensitizes spores to subsequent stress.” J. Appl. Microbiol., 97(4), 838–852.
Cortezzo, D. E., and Setlow, P. (2005). “Analysis of factors that influence the sensitivity of spores of Bacillus subtilis to DNA damaging chemicals.” J. Appl. Microbiol., 98(3), 606–617.
Davidson, J. N. (1965). The biochemistry of nucleic acids, 5th Ed., Methuen, London.
Deutsche Vereinigung das Gas- und Wasserfaches (DVGW). (2003). “UV disinfection devices for drinking water supply—Requirements and testing.” W294-3, Bonn, Germany.
Donnellan, J. E., Jr., and Setlow, R. B. (1965). “Thymine photoproducts but not thymine dimers found in ultraviolet-irradiated bacterial spores.” Science, 149(3681), 308–310.
Gottardi, W. (1999). “Iodine and disinfection: Theoretical study on the mode of action, efficiency, stability and analytical aspects in the aqueous system.” Archives of Pharmacy, 332(5), 151–157.
Gottardi, W. (2001). “Iodine and iodine compounds.” Disinfection, sterilization, and preservation, 5th Ed., Chap. 8, S. S. Block, ed., Lippincott Williams & Wilkins, Philadelphia, 159–183.
Kashinkunti, R. D., Linden, K. G., Shin, G., Metz, D. H., Sobsey, M. D., Moran, M. C., and Samuelson, A. M. (2004). “Investigating multibarrier inactivation for Cincinnati-UV, by-products and biostability.” J. Am. Water Works Assoc., 96(6), 114–127.
Kearns, D., and Losick, R. (2005). “Cell population heterogeneity during growth of Bacillus subtilis.” Genes Dev., 19(24), 3083–3094.
Keren, I., Shah, D., Spoering, A., Kaldalu, N., and Lewis, K. (2004). “Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli.” J. Bacteriol., 186(24), 8172–8180.
Koivunen, J., and Heinonen-Tanski, H. (2005). “Inactivation of enteric microorganisms with chemical disinfectants, UV irradiation and combined chemical/UV treatments.” Water Res., 39(8), 1519–1526.
Kruse, C. W., Hsu, Y., Griffiths, A. C., and Stringer, R. (1970). “Halogen action on bacteria, viruses and protozoa.” Proc., National Specialty Conf. on Disinfection, ASCE, Amherst, Mass., 113–136.
Kussell, E., Kishony, R., Balaban, N. Q., and Leibler, S. (2005). “Bacterial persistence: A model of survival in changing environments.” Genetics, 169(4), 1807–1814.
Larson, M., and Mariñas, B. (2003). “Inactivation of Bacillus subtilis spores with ozone and monochloramine.” Water Res., 37(4), 833–844.
Levin, B. R. (2004). “Noninherited resistance to antibiotics.” Science, 305(5690), 1578–1579.
Levin, B. R., and Rozen, D. E. (2006). “Noninherited antibiotic resistance.” Nat. Rev. Microbiol., 4(7), 556–562.
Mamane-Gravetz, H., Linden, K. G., Cabaj, A., and Sommer, R. (2005). “Spectral sensitivity of Bacillus subtilis spores and MS2 coliphage for validation testing of ultraviolet reactors for water disinfection.” Environ. Sci. Technol., 39(20), 7845–7852.
McMonigal, K., Braverman, K. E., Dunn, J. T., Stanbury, J. B., and Wear, M. (2000). “Thyroid function changes related to use of iodinated water in the US space program.” Aviat., Space Environ. Med., 71(11), 1120–1125.
Miller, C., Thomsen, L. E., Gaggero, C., Mosseri, R., Ingmer, H., and Cohen, S. N. (2004). “SOS response induction by B-Lactams and bacterial defense against antibiotic lethality.” Science, 305(5690), 1629–1630.
Miyata, S., Kozuka, S., Yasuda, Y., Chen, Y. H., Moriyama, R., Tochikubo, K., and Makino, S. (1997). “Localization of germination-specific spore-lytic enzymes in Clostridium perfringens S40 spores detected by immunoelectron microscopy.” FEMS Microbiol. Lett., 152(2), 243–247.
Nicholson, W. L., Munakata, N., Horneck, G., Melosh, N. J., and Setlow, P. (2000). “Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments.” Microbiol. Mol. Biol. Rev., 64(3), 548–572.
Nicholson, W. L., and Setlow, P. (1990). “Sporulation, germination, and outgrowth.” Molecular biological methods for Bacillus, Wiley, Sussex, U.K., 391–450.
Österreichisches Normungsinstitut (ONORM). (2001). “Plants for disinfection of water using ultraviolet radiation: Requirements and testing. 1: Low pressure mercury lamp plants.” ÖNORM M5873–1 E, Vienna, Austria.
Österreichisches Normungsinstitut (ONORM). (2003). “Plants for disinfection of water using ultraviolet radiation: Requirements and testing. 2: Medium pressure mercury lamp plants.” ÖNORM M5873-2 E, Vienna, Austria.
Pennell, K. G. (2005). “Sequential water disinfection using UV irradiation and iodination for long-term space missions.” Ph.D. thesis, Purdue Univ., West Lafayette, Ind.
Pennell, K. G., Aronson, A. I., and Blatchley, E. R., III. (2008). “Phenotypic persistence and external shielding ultraviolet radiation inactivation kinetic model.” J. Appl. Microbiol.,104(4), 1192–1202.
Pierson, D. L. (2001) “Microbial contamination of spacecraft.” Gravitational and Space Biology Bulletin, 14(2), 1–6.
Rahn, R. O. (1993). “Technical note: Use of potassium iodide as a chemical actinometer.” J. Photochem. Photobiol., A, 58(6), 874–880.
Rahn, R. O. (1997). “Technical note: Potassium iodide as a chemical actinometer for 254nm radiation: Use of iodate as an electron scavenger.” J. Photochem. Photobiol., A, 66(4), 450–455.
Rahn, R. O., Stefan, M. I., Bolton, J. R., Goren, E., Shaw, P., and Lykke, K. R. (2003). “Technical note: Quantum yield of the iodide-iodate chemical actinometer: Dependence on wavelength and concentration.” J. Photochem. Photobiol., A, 78(2), 146–152.
Rennecker, J. L., Driedger, A. M., Rubin, S. A., and Mariñas, B. J. (2000). “Synergy in sequential inactivation of cryptosporidium parvum with ozone/free chlorine and ozone/monochloramine.” Water Res., 34(17), 4121–4130.
Rose, R., Setlow, B., Monroe, A., Mallozzi, M., Driks, A., and Setlow, P. (2007). “Comparison of the properties of Bacillus subtilis spores made in liquid or on agar plates.” J. Appl. Microbiol., 103(3), 691–699.
Sarasanandarajah, S., Kunnil, J., Bronk, B. V., and Reinisch, L. (2005). “Two-dimensional multiwavelength fluorescence spectra of dipicolinic acid and calcium dipicolinate.” Appl. Opt., 44(7), 1182–1187.
Schaeffer, A. B., and Fulton, M. (1933). “A simplified method of staining endospores.” Science, 77, 194.
Schaeffer, P., Millet, J., and Aubert, J. P. (1965). “Catabolic repression of bacterial sporulation.” Proc. Natl. Acad. Sci. U.S.A., 54(3), 704–711.
Setlow, P. (2006). “Spores of Bacillus subtilis: Their resistance to and killing by radiation, heat and chemicals.” J. Appl. Microbiol., 101(3), 514–525.
Setlow, R. B. (1966). “Cyclobutane-type pyrimidine dimers in polynucleotides.” Science, 153(3734), 379–386.
Sharpless, C. M., and Linden, K. G. (2001). “UV photolysis of nitrate: Effects of natural organic matter and dissolved inorganic carbon and implications for UV water disinfection.” Environ. Sci. Technol., 35(14), 2949–2955.
Shen, C., Fang, S., Bergstrom, D. E., and Blatchley, E. R., III. (2005). “ (E) -5-[2-(methoxycarbonyl)ethenyl]Cytidine as a chemical actinometer for germicidal UV radiation.” Environ. Sci. Technol., 39(10), 3826–3832.
Slieman, T. A., and Nicholson, W. L. (2000). “Artificial and solar UV radiation induces strand breaks and cyclobutane pyrimidine dimers in Bacillus subtilis spore DNA.” Appl. Environ. Microbiol., 66(1), 199–205.
Tennen, R., Setlow, B., Davis, K. L., Loshon, C. A., and Setlow, P. (2000). “Mechanisms of killing of spores of Bacillus subtilis by iodine, glutaraldehyde, and nitrous acid.” J. Appl. Microbiol., 89(2), 330–338.
USEPA. (2006). “UV disinfection guidance manual for the long term. 2: Enhanced surface water treatment rule.” EPA 815-R-06-007, Washington, D.C.
Varghese, H. A. (1976). “5-Thyminyl-5,6-dihydrothymine from DNA irradiated with ultraviolet light.” Biochem. Biophys. Res. Commun., 38(3), 484–490.
Williams, N. D., and Russell, A. D. (1993). “Revival of Bacillus subtilis spores from biocide-induced injury in the germination process.” J. Appl. Bacteriol., 75(1), 76–81.
Wolff, J. (1969). “Iodide goiter and the pharmacologic effects of excess iodide.” Am. J. Med., 47(1), 101–124.
Wyatt, L. R., and Waites, W. M. (1975) “The effect of chlorine on spores of Clostridium bifermentans, Bacillus subtilis, and Bacillus cereus.” J. Gen. Microbiol., 89(2), 337–344.

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Published In

Go to Journal of Environmental Engineering
Journal of Environmental Engineering
Volume 134Issue 7July 2008
Pages: 513 - 520

History

Received: Jun 5, 2006
Accepted: Dec 21, 2007
Published online: Jul 1, 2008
Published in print: Jul 2008

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Authors

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Kelly G. Pennell, M.ASCE
Post-Doctoral Research Associate, Division of Engineering, Brown Univ., 182 Hope St., Box D, Providence, RI 02912.
Zorana Naunovic
Environmental Engineer, CDM, One Cambridge Pl., 50 Hampshire St., Cambridge, MA 02139.
Ernest R. Blatchley III, A.M.ASCE
Professor, School of Civil Engineering, Purdue Univ., 550 Stadium Mall Dr., West Lafayette, IN 47907 (corresponding author). E-mail: [email protected]

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