Thermosonication damages the inner membrane of Bacillus subtilis spores and impels their inactivation

Food Research International

Volumn 125, Issue , 2019, Pages

  Fan, Lihua ^a   Ismail, Balarabe Bilyaminu ^a   Hou, Furong ^a   Muhammad, Aliyu Idris ^a   Zou, Mingming ^a   Ding, Tian ^a   Liu, Donghong ^a,b  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

Bacillus subtilis spore; Inner membrane; Spore resistance; Thermosonication

Indexed keywords

BACTERIOLOGY; CELL MEMBRANES; PROTEINS; THERMOACOUSTICS; ULTRASONICS;

BACILLUS SUBTILIS; BACILLUS SUBTILIS SPORES; FURTHER UTILIZATION; INNER MEMBRANES; INTRACELLULAR SUBSTANCES; PLASMA MEMBRANE PERMEABILITY; THERMO SONICATIONS; WILD-TYPE STRAIN;

HEAT RESISTANCE;

BACILLUS SUBTILIS; BACTERIAL SPORE; CELL MEMBRANE; FOOD CONTROL; HEAT; INSTRUMENT STERILIZATION; PROCEDURES; RADIATION RESPONSE; ULTRASOUND;

BACILLUS SUBTILIS; CELL MEMBRANE; FOOD MICROBIOLOGY; HOT TEMPERATURE; SONICATION; SPORES, BACTERIAL; STERILIZATION;

EID: 85071342897     PISSN: 09639969     EISSN: 18737145     Source Type: Journal    
DOI: 10.1016/j.foodres.2019.108514     Document Type: Article

References (41)

1. Aadil, R. M., Zeng, X. A., Sun, D.W., Wang, M. S., Liu, Z.W. & Zhang, Z. H. (2015c). Combined effects of sonication and pulsed electric field on selected quality parameters of grapefruit juice. LWT- Food Science and Technology, 62, 890-893.
2. Aadil, R. M., Zeng, X. A., Zhang, Z. H., Sahar, A., Khalil, A. A., Rahman, U. U., Khan, M. & Mehmood, T. (2018). Combined effects of pulsed electric field and ultrasound on bioactive compounds and microbial quality of grapefruit juice. Journal of Food Processing & Preservation, 42, e13507. doi:10.1111/jfpp.13507.
3. Aadil, R. M., Zeng, X. A., Zhang, Z. H., Wang, M. S., Han, Z., Jing, H. & Jabbar, S. (2015a). A potential of ultrasound on minerals, micro-organisms, phenolic compounds and colouring pigments of grapefruit juice. International Journal of Food Science & Technology, 50, 1144-1150.
4. Aadil, R. M., Zeng, X. A., Zhang, Z. H., Wang, M. S., Han, Z., Jing, H. & Jabbar, S. (2015b). Thermosonication: a potential technique that influences the quality of grapefruit juice. International Journal of Food Science & Technology, 50, 1275-1282.
5. Alkaabi, K. M., Abeer, Y., & Ashraf, S. S. (2005). Effect of pH on thermal- and chemical-induced denaturation of GFP. Applied Biochemistry and Biotechnology, 126, 149-156.
6. Black, E. P., Kasia, K. D., Dongsheng, G., Jie, W., Barbara, S., Cortezzo, D. E., Hoover, D. G., & Peter, S. (2005). Factors influencing germination of Bacillus subtilis spores via activation of nutrient receptors by high pressure. Applied and Environmental Microbiology, 71, 5879-5887.
7. Coleman, W. H., Chen, D., Li, Y. Q., Cowan, A. E., & Setlow, P. (2007). How moist heat kills spores of Bacillus subtilis. Journal of Bacteriology, 189, 8458-8466.
8. Coleman, W. H., Zhang, P., Li, Y. Q., & Setlow, P. (2010). Mechanism of killing of spores of Bacillus cereus and Bacillus megaterium by wet heat. Letters in Applied Microbiology, 50, 507-514.
9. Cortezzo, D. E., & Setlow, P. (2005). Analysis of factors that influence the sensitivity of spores of Bacillus subtilis to DNA damaging chemicals. Journal of Applied Microbiology, 98, 606-617.
10. Cowan, A. E., Koppel, D. E., Barbara, S., & Peter, S. (2003). A soluble protein is immobile in dormant spores of Bacillus subtilis but is mobile in germinated spores: implications for spore dormancy. Proceedings of the National Academy of Sciences of the United States of America, 100, 4209-4214.
11. Duarte, A. L. A, Rosário, D. K. A, Oliveira, S. B. S., Souza, H. L. S., Carvalho, R.V., Carneiro, J. C. S., & Bernardes, P. C. (2018). Ultrasound improves antimicrobial effect of sodium dichloroisocyanurate to reduce Salmonella Typhimurium on purple cabbage. International Journal of Food Microbiology, 269, 12-18.
12. Evelyn, E., & Silva, F. V. (2015b). Use of power ultrasound to enhance the thermal inactivation of Clostridium perfringens spores in beef slurry. International Journal of Food Microbiology, 206, 17-23.
13. Evelyn, E., & Silva, F. V. (2018). Differences in the resistance of microbial spores to thermosonication, high pressure thermal processing and thermal treatment alone. Journal of Food Engineering, 222, 292-297.
14. Evelyn, E., & Silva, F. V. M. (2015a). Thermosonication versus thermal processing of skim milk and beef slurry: Modeling the inactivation kinetics of psychrotrophic Bacillus cereus spores. Food Research International, 67, 67-74.
15. Fan, L., Hou, F., Muhammad, A. I., Ruiling, L. V., Watharkar, R. B., Guo, M., Ding, T., & Liu, D. (2019). Synergistic inactivation and mechanism of thermal and ultrasound treatments against Bacillus subtilis spores. Food Research International, 116, 1094-1102.
16. Francis, M. B., & Sorg, J. A. (2016). Detecting cortex fragments during bacterial spore germination. Journal of Visualized Experiments Jove, 112, 1-7.
17. Garcia, M. L., Burgos, J., Sanz, B., & Ordoñez, J. A. (1989). Effect of heat and ultrasonic waves on the survival of two strains of Bacillus subtilis. Journal of Applied Bacteriology, 67, 619-628.
18. Hornstra, L. M., Devries, Y. P., Devos, W. M., Abee, T., & Wellsbennik, M. H. (2005). GerR, a novel ger operon involved in L-alanine- and inosine-initiated germination of Bacillus cereus ATCC 14579. Applied & Environmental Microbiology, 71, 774-781.
19. Khanal, S. N., Anand, S., & Muthukumarappan, K. (2014). Evaluation of high-intensity ultrasonication for the inactivation of endospores of 3 bacillus species in nonfat milk. Journal of Dairy Science, 97, 5952-5963.
20. Li, J., Ding, T., Liao, X., Chen, S., Ye, X., & Liu, D. (2017b). Synergetic effects of ultrasound and slightly acidic electrolyzed water against Staphylococcus aureus evaluated by flow cytometry and electron microscopy. Ultrasonics Sonochemstry, 38, 711-719.
21. Li, J., Suo, Y., Liao, X., Ahn, J., Liu, D., Chen, S., Ye, X., & Ding, T. (2017a). Analysis of Staphylococcus aureus cell viability, sublethal injury and death induced by synergistic combination of ultrasound and mild heat. Ultrasonics Sonochemistry, 39, 101-110.
22. Liao X., Muhammad, A., Chen, S., Hu, Y., Ye, X., Liu, D., Ding, T. (2018). Spore inactivation induced by cold plasma. Critical Reviews in Food Science & Nutrition, 58, 1-11.
23. Logan, N. A. (2012). Bacillus and relatives in foodborne illness. Journal of Applied Microbiology, 112, 417-429.
24. Luu, S., Cruz-Mora, J., Setlow, B., Feeherry, F. E., Doona, C. J., & Setlow, P. (2015). The effects of heat activation on Bacillus spore germination, with nutrients or under high pressure, with or without various germination proteins. Applied & Environmental Microbiology, 81, 2927-2938.
25. Moeller, R., Horneck, G., Rettberg, P., Mollenkopf, H. J., Stackebrandt, E., Nicholson, W. L. (2006). A method for extracting RNA from dormant and germinating Bacillus subtilis strain 168 endospores. Current Microbiology, 53, 227-231.
26. Paidhungat, M., Ragkousi, K., & Setlow, P. (2001). Genetic requirements for induction of germination of spores of Bacillus subtilis by Ca2+-dipicolinate. Journal of Bacteriology, 183, 4886-4893.
27. Pinzón, P. A., Scholl, G., Nagarajan, R., Mello, C. M., & Camesano, T. A. (2010). Atomic force microscopy study of germination and killing of Bacillus atrophaeus spores. Journal of Molecular Control, 22, 373-379.
28. Rao, L., Zhao, F., Wang, Y., Chen, F., Hu, X., & Liao, X. (2016). Investigating the inactivation mechanism of Bacillus subtilis spores by high pressure CO2. Frontiers in Microbiology, 7, 1-12
29. Roobab, U., Aadil, R. M., Madni, G. M., & Alaa, E. B. (2018). The impact of nonthermal technologies on the microbiological quality of juices: A review. Comprehensive Reviews in Food Science and Food Safety, 17, 437-457.
30. Setlow, B., Korza, G., Blatt, K. M. S., Fey, J. P., & Setlow, P. (2016). Mechanism of Bacillus subtilis spore inactivation by and resistance to supercritical CO2 plus peracetic acid. Journal of Applied Microbiology, 120, 57-69.
31. Setlow, B., Melly, E., & Setlow, P. (2001). Properties of spores of Bacillus subtilis blocked at an intermediate stage in spore germination. Journal of Bacteriology, 183, 4894-4899.
32. Setlow, B., & Setlow, P. (1996). Role of DNA repair in Bacillus subtilis spore resistance. Journal of Bacteriology, 178, 3486-3495.
33. Setlow, P. (2014). Spore resistance properties. Microbiology Spectrum, 2, 1-13.
34. Stocks, S. M. (2010). Mechanism and use of the commercially available viability stain, baclight. Cytometry Part A, 62, 189-195.
35. Ugarte, R. E., Feng, H., Martin, S. E., Cadwallader, K. R., & Robinson, S. (2006). Inactivation of Escherichia coli with power ultrasound in apple cider. Journal of Food Science, 71, 102-108.
36. Wang, Z., Xiufang, B.I., Xiang, R., Chen, L., Feng, X., Zhou, M., Che, Z. (2018). Inactivation of Escherichia coli by ultrasound combined with nisin. Journal of Food Protection, 81, 993-1000.
37. Wordon, B. A., Mortimer, B., & Mcmaster, L. D. (2012). Comparative real-time analysis of Saccharomyces cerevisiae cell viability, injury and death induced by ultrasound (20 kHz) and heat for the application of hurdle technology. Food Research International, 47, 134-139.
38. Wu, X., Narsimhan, G. (2017). Synergistic effect of low power ultrasonication on antimicrobial activity of melittin against Listeria monocytogenes. LWT-Food Science and Technology, 75, 578-581.
39. Yi, X., & Setlow, P. (2010). Studies of the commitment step in the germination of spores of Bacillus species. Journal of Bacteriology, 192, 3424-3433.
40. Young, S. B., & Setlow, P. (2010). Mechanisms of killing of Bacillus subtilis spores by hypochlorite and chlorine dioxide. Journal of Applied Microbiology, 95, 54-67.
41. Zia, S., Khan, M. R., Zeng, X. A., Sehrish, Shabbir, M. A. & Aadil, R. M. (2019). Combined effect of microwave and ultrasonication treatments on the quality and stability of sugarcane juice during cold storage. International Journal of Food Science & Technology, doi:10.1111/ijfs.14167.