Inactivation of bacteria and yeast using high-frequency ultrasound treatment

Water Research

Volumn 60, Issue , 2014, Pages 93-104

  Gao, Shengpu ^a,b,c   Hemar, Yacine ^a   Ashokkumar, Muthupandian ^d   Paturel, Sara ^a,b   Lewis, Gillian D ^b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c CHINA NATIONAL INSTITUTE OF STANDARDIZATION   (China)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Aureobasidium pullulans; Bacillus subtilis; Bacteria inactivation; Enterobacter aerogenes; High frequency ultrasound; Staphylococcus epidermidis; Yeast

Indexed keywords

BACTERIA; BACTERIOLOGY; CAVITATION; FREE RADICALS; ULTRASONICS;

ACOUSTIC CAVITATIONS; AUREOBASIDIUM PULLULANS; BACILLUS SUBTILIS; BACTERIA INACTIVATION; ENTEROBACTER AEROGENES; GROWTH PHASE; GROWTH PHASIS; HIGH-FREQUENCY ULTRASOUND; STAPHYLOCOCCUS EPIDERMIDIS; ULTRASOUND TREATMENTS;

YEAST;

FREE RADICAL; HYDROGEN PEROXIDE;

BACTERIUM; FREE RADICAL; GROWTH; HYDROGEN PEROXIDE; ULTRASONICS; YEAST;

ARTICLE; AUREOBASIDIUM PULLULANS; BACILLUS SUBTILIS; BACTERIAL GROWTH; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM INACTIVATION; CONTROLLED STUDY; ENTEROBACTER AEROGENES; FUNGAL PHENOMENA AND FUNCTIONS; FUNGUS GROWTH; GROWTH CURVE; HIGH FREQUENCY ULTRASOUND; NONHUMAN; PRIORITY JOURNAL; STAPHYLOCOCCUS EPIDERMIDIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASOUND; YEAST INACTIVATION; ASCOMYCETES; BACTERIA; MICROBIAL VIABILITY; PHYSIOLOGY; ULTRASTRUCTURE;

ASCOMYCOTA; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; MICROBIAL VIABILITY; MICROSCOPY, ELECTRON, TRANSMISSION; SONICATION;

EID: 84900553648     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2014.04.038     Document Type: Article

References (77)

1. Ahmed F.I.K., Russell C. Synergism between ultrasonic waves and hydrogen peroxide in the killing of micro-organisms. J. Appl. Bacteriol. 1975, 39(1):31-40.
2. Al Bsoul A., Magnin J.P., Commenges-Bernole N., Gondrexon N., Willison J., Petrier C. Effectiveness of ultrasound for the destruction of Mycobacterium sp. strain (6PY1). Ultrason. Sonochem. 2010, 17(1):106-110.
3. Alegria A.E., Lion Y., Kondo T., Riesz P. Sonolysis of aqueous surfactant solutions: probing the interfacial region of cavitation bubbles by spin trapping. J. Phys. Chem. 1989, 93(12):4908-4913.
4. Alliger H. Ultrasonic disruption. Am. Lab. 1975, 10:75-85.
5. Antoniadis A., Poulios I., Nikolakaki E., Mantzavinos D. Sonochemical disinfection of municipal wastewater. J. Hazard. Mater. 2007, 146(3):492-495.
6. Ashokkumar M. The characterization of acoustic cavitation bubbles - an overview. Ultrason. Sonochem. 2011, 18(4):864-872.
7. -. J. Am. Chem. Soc. 1951, 73(4):1842-1843.
8. Butz P., Tauscher B. Emerging technologies: chemical aspects. Food Res. Int. 2002, 35(2-3):279-284.
9. Cabiscol E., Tamarit J., Ros J. Oxidative stress in bacteria and protein damage by reactive oxygen species. Int. Microbiol. 2010, 3(1):3-8.
10. Cheremisinoff N.P., Cheremisinoff P.N. Water Treatment and Waste Recovery: Advanced Technology and Applications 1993, Prentice-Hall, Inc., New Jersey.
11. Chi Z., Wang F., Chi Z., Yue L., Liu G., Zhang T. Bioproducts from Aureobasidium pullulans, a biotechnologically important yeast. Appl. Microbiol. Biotechnol. 2009, 82(5):793-804.
12. Cho M., Chung H., Yoon J. Effect of pH and importance of ozone initiated radical reactions in inactivating Bacillus subtilis spore. Ozone: Sci. Eng. 2002, 24(2):145-150.
13. Collis J., Manasseh R., Liovic P., Tho P., Ooi A., Petkovic-Duran K., Zhu Y. Cavitation microstreaming and stress fields created by microbubbles. Ultrasonics 2010, 50(2):273-279.
14. Cooke W.B. An ecological life history of Aureobasidium pullulans (de Bary) Arnaud. Mycopathol. Mycol. Appl. 1959, 12(1):1-45.
15. Crum L.A. Comments on the evolving field of sonochemistry by a cavitation physicist. Ultrason. Sonochem. 1995, 2(2):S147-S152.
16. Dai Y., Li F., Ge F., Zhu F., Wu L., Yang X. Mechanism of the enhanced degradation of pentachlorophenol by ultrasound in the presence of elemental iron. J. Hazard. Mater. 2006, 137(3):1424-1429.
17. Davies R. Observations on the use of ultrasound waves for the disruption of micro-organisms. Biochim. et Biophys. Acta 1959, 33(2):481-493.
18. Dong Y., Chen S., Wang Z., Peng N., Yu J. Synergy of ultrasound microbubbles and vancomycin against Staphylococcus epidermidis biofilm. J. Antimicrob. Chemother. 2013, 68(4):816-826.
19. Drakopoulou S., Terzakis S., Fountoulakis M.S., Mantzavinos D., Manios T. Ultrasound-induced inactivation of gram-negative and gram-positive bacteria in secondary treated municipal wastewater. Ultrason. Sonochem. 2009, 16(5):629-634.
20. Earnshaw R.G., Appleyard J., Hurst R.M. Understanding physical inactivation processes: combined preservation opportunities using heat, ultrasound and pressure. Int. J. Food Microbiol. 1995, 28(2):197-219.
21. Gao S., Lewis G.D., Ashokkumar M., Hemar Y. Inactivation of microorganisms by low-frequency high-power ultrasound: 1. Effect of growth phase and capsule properties of the bacteria. Ultrason. Sonochem. 2014, 21(1):446-453.
22. Gao S., Lewis G.D., Ashokkumar M., Hemar Y. Inactivation of microorganisms by low-frequency high-power ultrasound: 2. A simple model for the inactivation mechanism. Ultrason. Sonochem. 2014, 21(1):454-460.
23. Gniewosz M., Duszkiewicz-Reinhard W. Comparative studies on pullulan synthesis, melanin synthesis and morphology of white mutant Aureobasidium pullulans B-1 and parent strain A.p.-3. Carbohydr. Polym. 2008, 72(3):431-438.
24. Grimont F., Grimont P.D. The Prokaryotes 2006, 197-214. Springer, New York. M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, E. Stackebrandt (Eds.).
25. Harvey E.N., Loomis A.L. The destruction of Luminous bacteria by high frequency sound waves. J. Bacteriol. 1929, 17(5):373-376.
26. He Y., Vinodgopal K., Ashokkumar M., Grieser F. Sonochemical synthesis of ruthenium nanoparticles. Res. Chem. Intermed. 2006, 32(8):709-715.
27. Hoog G.S. Evolution of black yeasts: possible adaptation to the human host. Anton. van Leeuwen. 1993, 63(2):105-109.
28. Hua I., Thompson J.E. Inactivation of Escherichia coli by sonication at discrete ultrasonic frequencies. Water Res. 2000, 34(15):3888-3893.
29. Huertas A., Barbeau B., Desjardins C., Galarza A., Figueroa M., Toranzos G. Evaluation of Bacillus subtilis and coliphage MS2 as indicators of advanced water treatment efficiency. Water Sci. Technol. 2003, 47(3):255-259.
30. Hughes R., Kilvington S. Comparison of hydrogen peroxide contact lens disinfection systems and solutions against Acanthamoeba polyphaga. Antimicrob. Agents Chemother. 2001, 45(7):2038-2043.
31. Imhoff J. Bergey's Manual of Systematic Bacteriology 2005, 587-850. Springer, New York. D. Brenner, N. Krieg, J. Staley, G. Garrity, D. Boone, P. Vos, M. Goodfellow, F. Rainey, K.-H. Schleifer (Eds.).
32. Imlay J.A., Linn S. Bimodal pattern of killing of DNA-repair-defective or anoxically grown Escherichia coli by hydrogen peroxide. J. Bacteriol. 1986, 166(2):519-527.
33. Joyce E., Al-Hashimi A., Mason T.J. Assessing the effect of different ultrasonic frequencies on bacterial viability using flow cytometry. J. Appl. Microbiol. 2011, 110(4):862-870.
34. Joyce E., Mason T.J., Phull S.S., Lorimer J.P. The development and evaluation of electrolysis in conjunction with power ultrasound for the disinfection of bacterial suspensions. Ultrason. Sonochem. 2003, 10(4-5):231-234.
35. Joyce E., Phull S.S., Lorimer J.P., Mason T.J. The development and evaluation of ultrasound for the treatment of bacterial suspensions. A study of frequency, power and sonication time on cultured Bacillus species. Ultrason. Sonochem. 2003, 10(6):315-318.
36. Jyoti K.K., Pandit A.B. Hybrid cavitation methods for water disinfection: simultaneous use of chemicals with cavitation. Ultrason. Sonochem. 2003, 10(4-5):255-264.
37. 2 yield) and bubble dynamics: frequency and power effects. Ultrason. Sonochem. 2008, 15(2):143-150.
38. Katsikogianni M., Spiliopoulou I., Dowling D.P., Missirlis Y.F. Adhesion of slime producing Staphylococcus epidermidis strains to PVC and diamond-like carbon/silver/fluorinated coatings. J. Mater. Sci. Mater. Med. 2006, 17(8):679-689.
39. Kikuchi T., Uchida T. Calorimetric method for measuring high ultrasonic power using water as a heating material. J. Phys. Conf. Ser. 2011, 279:012012.
40. Klis F.M. Review: cell wall assembly in yeast. Yeast 1994, 10(7):851-869.
41. Koda S., Kimura T., Kondo T., Mitome H. A standard method to calibrate sonochemical efficiency of an individual reaction system. Ultrason. Sonochem. 2003, 10(3):149-156.
42. Koda S., Miyamoto M., Toma M., Matsuoka T., Maebayashi M. Inactivation of Escherichia coli and Streptococcus mutans by ultrasound at 500kHz. Ultrason. Sonochem. 2009, 16(5):655-659.
43. Kumar V., Bhardwaj Y.K., Sabharwal S., Mohan H. The role of radiolytically generated species in radiation-induced polymerization of vinylbenzyltrimethylammonium chloride (VBT) in aqueous solution: steady-state and pulse radiolysis study. J. Radiat. Res. 2003, 44(2):161-169.
44. Leighton T.G. The Acoustic Bubble 1994, Academic Press, San Diego.
45. Liu L., Yuan Y., Li F.B., Feng C.H. In-situ Cr(VI) reduction with electrogenerated hydrogen peroxide driven by iron-reducing bacteria. Bioresour. Technol. 2011, 102(3):2468-2473.
46. Mason T.J. Sonochemistry: the uses of ultrasound in chemistry 1990, The Royal Society of Chemistry Press, Cambridge.
47. Mason T.J., Joyce E., Phull S.S., Lorimer J.P. Potential uses of ultrasound in the biological decontamination of water. Ultrason. Sonochem. 2003, 10(6):319-323.
48. Mason T.J., Riera E., Vercet A., Lopez-Buesa P. Emerging Technologies for Food Processing 2005, 323-351. Elsevier Academic Press, California. D.W. Sun (Ed.).
49. Mead E.L., Sutherland R.G., Verrall R.E. The effect of ultrasound on water in the presence of dissolved gases. Can. J. Chem. 1976, 54(7):1114-1120.
50. Miles A.A., Misra S.S., Irwin J.O. The estimation of the bactericidal power of the blood. J. Hyg. 1938, 38(6):732-749.
51. O'Donnell C.P., Tiwari B.K., Bourke P., Cullen P.J. Effect of ultrasonic processing on food enzymes of industrial importance. Trends Food Sci. Technol. 2010, 21(7):358-367.
52. Olvera M., Eguia A., Rodriguez O., Chong E., Pillai S.D., Ilangovan K. Inactivation of Cryptosporidium parvum oocysts in water using ultrasonic treatment. Bioresour. Technol. 2008, 99(6):2046-2049.
53. 2 photocatalysis, sonolysis and UV-C irradiation. Catal. Today 2007, 129(1-2):136-142.
54. Petri B., Watts R., Teel A., Huling S., Brown R. Situ Chemical Oxidation for Groundwater Remediation 2011, 33-88. Springer, New York. R.L. Siegrist, M. Crimi, T.J. Simpkin (Eds.).
55. Phull S.S., Newman A.P., Lorimer J.P., Pollet B., Mason T.J. The development and evaluation of ultrasound in the biocidal treatment of water. Ultrason. Sonochem. 1997, 4(2):157-164.
56. Riesz P., Berdahl D., Christman C.L. Free radical generation by ultrasound in aqueous and nonaqueous solutions. Environ. Health Perspect. 1985, 64:233-252.
57. Riesz P., Kondo T. Free radical formation induced by ultrasound and its biological implications. Free Radic. Biol. Med. 1992, 13(3):247-270.
58. Russell N.J. Bacterial membranes: the effects of chill storage and food processing. An overview. Int. J. Food Microbiol. 2002, 79(1-2):27-34.
59. Sala F.J., Burgos J., Condon S., Lopez P., Raso J. New Methods of Food Preservation 1995, 176-204. Blackie Academic & Professional, London. G.W. Gould (Ed.).
60. Salleh-Mack S.Z., Roberts J.S. Ultrasound pasteurization: the effects of temperature, soluble solids, organic acids and pH on the inactivation of Escherichia coli ATCC 25922. Ultrason. Sonochem. 2007, 14:323-329.
61. Salton M.R.J. The relationship between the nature of the cell wall and the gram stain. J. Gen. Microbiol. 1963, 30(2):223-235.
62. Sapers G.M., Sites J.E. Efficacy of 1% hydrogen peroxide wash in decontaminating apples and cantaloupe melons. J. Food Sci. 2003, 68(5):1793-1797.
63. Schleifer K.-H. Bergey's Manual of Systematic Bacteriology 2009, 19-1317. Springer, New York. P. Vos, G. Garrity, D. Jones, N. Krieg, W. Ludwig, F. Rainey, K.-H. Schleifer, W. Whitman (Eds.).
64. Semenov I.A., Ulyanov B.A., Kulov N.N. Effect of ultrasound on the dissolution of carbon dioxide in water. Theor. Found. Chem. Eng. 2011, 45(1):21-25.
65. Singer A.J., Coby C.T., Singer A.H., Thode H.C., Tortora G.T. The effects of low-frequency ultrasound on Staphylococcus epidermidis. Curr. Microbiol. 1999, 38(3):194-196.
66. Soria A.C., Villamiel M. Effect of ultrasound on the technological properties and bioactivity of food: a review. Trends Food Sci. Technol. 2010, 21(7):323-331.
67. Supeno, Kruus P. Sonochemical formation of nitrate and nitrite in water. Ultrason. Sonochem. 2000, 7(3):109-113.
68. Thangavadivel K., Megharaj M., Smart R.S., Lesniewski P.J., Naidu R. Application of high frequency ultrasound in the destruction of DDT in contaminated sand and water. J. Hazard. Mater. 2009, 168(2-3):1380-1386.
69. Urzi C., De Leo F., Lo Passo C., Criseo G. Intra-specific diversity of Aureobasidium pullulans strains isolated from rocks and other habitats assessed by physiological methods and by random amplified polymorphic DNA (RAPD). J. Microbiol. Methods 1999, 36(1-2):95-105.
70. Walker J.T., Bradshaw D.J., Fulford M.R., Marsh P.D. Microbiological evaluation of a range of disinfectant products to control mixed-species biofilm contamination in a laboratory model of a dental unit water system. Appl. Environ. Microbiol. 2003, 69(6):3327-3332.
71. Wang J., Chen C. Biosorbents for heavy metals removal and their future. Biotechnol. Adv. 2009, 27(2):195-226.
72. Warner C.L., Bruckner-Lea C.J., Grate J.W., Straub T., Posakony G.J., Valentine N., Ozanich R., Bond L.J., Matzke M.M., Dockendorff B., Valdez C., Valdez P., Owsley S. A flow-through ultrasonic lysis module for the disruption of bacterial spores. J. Assoc. Lab. Autom. 2009, 14(5):277-284.
73. Weissler A. Formation of hydrogen peroxide by ultrasonic waves: free radicals. J. Am. Chem. Soc. 1959, 81(5):1077-1081.
74. Wingender J., Flemming H. Contamination potential of drinking water distribution network biofilms. Water Sci. Technol. 2004, 49(11):277-286.
75. Wolfe R.L., Stewart M.H., Liang S., Mcguire M.J. Disinfection of model indicator organisms in a drinking water pilot plant by using PEROXONE. Appl. Environ. Microbiol. 1989, 55(9):2230-2241.
76. Wu J., Nyborg W.L. Ultrasound, cavitation bubbles and their interaction with cells. Adv. Drug. Deliv. Rev. 2008, 60(10):1103-1116.
77. Zalar P., Gostincar C., de Hoog G.S., Ursic V., Sudhadham M., Gunde-Cimerman N. Redefinition of Aureobasidium pullulans and its varieties. Stud. Mycol. 2008, 61:21-38.