Alicyclobacillus acidoterrestris: An increasing threat to the fruit juice industry?

International Journal of Food Science and Technology

Volumn 43, Issue 2, 2008, Pages 250-260

  Walker, Michelle ^a   Phillips, Carol A ^b  

^a Frutarom (UK) Ltd   (United Kingdom)

^b UNIVERSITY OF NORTHAMPTON   (United Kingdom)

Author keywords

Alicyclobacillus acidoterrestris; Alicyclobacillus spp; Control; Detection; Fruit juices

Indexed keywords

ALICYCLOBACILLUS; ALICYCLOBACILLUS ACIDOTERRESTRIS; BACTERIA (MICROORGANISMS);

EID: 38549085623     PISSN: 09505423     EISSN: 13652621     Source Type: Journal    
DOI: 10.1111/j.1365-2621.2006.01427.x     Document Type: Article

References (74)

1. Albuquerque, L., Rainey, F.A., Chung, A.P., et al. (2000). Alicyclobacillus hesperidum sp. nov. and a related genomic species from solfataric soils of Sao Miguel in the Azores. International Journal of Systematic and Evolutionary Microbiology, 50, 451 457.
2. Alpas, H., Alma, L. Bozoglu, F. (2003). Inactivation of Alicyclobacillus acidoterrestris vegetative cells in model system, apple, orange and tomato juices by high hydrostatic pressure. World Journal of Microbiology and Biotechnology, 19, 619 623.
3. Bahceci, K.S., Gokmen, V. Acar, J. (2005). Formation of guaiacol from vanillin by Alicyclobacillus acidoterrestris in apple juice: a model study. European Food Research and Technology, 220, 196 199.
4. Borlinghaus, A. Engel, R. (1997). Alicyclobacillus incidence in commercial apple juice concentrate (AJC) supplies - method development and validation. Fruit Processing, 7, 262 266.
5. Boziaris, I.S. Adams, M.R. (1999). Effect of chelators and nisin produced in situ on inhibition and inactivation of gram negatives. International Journal of Food Microbiology, 53, 105 113.
6. Brock, T.D. Darland, G. (1970). The limits of microbial existence: temperature and pH. Science, 169, 1316 1318.
7. Buzrul, S., Alpas, H. Bozoglu, F. (2005). Use of Weibull frequency distribution model to describe the inactivation of Alicyclobacillus acidoterrestris by high pressure at different temperatures. Food Research International, 38, 151 157.
8. Cerny, G., Hennlich, W. Poralla, K. (1984). Spoilage of fruit juice by bacilli: Isolation and characterization of the spoiling organism. Zeitschrift fur Lebensmitteluntersuchung und Forschung, 179, 224 227.
9. Chang, S.S. Kang, D.H. (2004). Alicyclobacillus spp. in the fruit juice industry: History, characteristics, and current isolation/detection procedures. Critical Reviews In Microbiology, 30, 55 74.
10. Chang, S. Kang, D.-H. (2005). Development of novel Alicyclobacillus spp. isolation medium. Journal of Applied Microbiology, 99, 1051 1060.
11. Chen, S., Tang, Q., Zhang, X., et al. (2006). Isolation and characterization of thermo-acidophilic endospore-forming bacteria from the concentrated apple juice-processing environment. Food Microbiology, 23, 439 445.
12. Connor, C.J., Luo, H., McSpadden Gardener, B.B. Wang, H.H. (2005). Development of a real-time PCR-based system targeting the 16S rRNA gene sequence for rapid detection of Alicyclobacillus spp. in juice products. International Journal of Food Microbiology, 99, 229 235.
13. Cutter, C.N. Siragusa, G.R. (1995). Treatments with nisin and chelators to reduce Salmonella and Escherichia coli on beef. Journal of Food Protection, 57, 1028 1030.
14. Darland, G. Brock, T.D. (1971). Bacillus acidocaldarius sp. nov., acidophilic thermophilic spore-forming bacterium. Journal of General Microbiology, 67, 9 15.
15. Deinhard, G., Blanz, P., Poralla, K. Altan, E. (1987). Bacillus acidoterrestris sp. nov., A new thermotolerant acidophile isolated from different soils. Systematic and Applied Microbiology, 10, 47 53.
16. Del Nobile, M.A., Cannarsi, M., Altieri, C., et al. (2004). Effect of Ag-containing nano-composite active packaging system on survival of Alicyclobacillus acidoterrestris. Journal of Food Science, 69, E379 E383.
17. Delves-Broughton, J. (1993). The use of EDTA to enhance the efficacy of nisin towards gram-negative bacteria. International Biodeterioration and Biodegradation, 32, 87 97.
18. Delves-Broughton, J. (1997). The food preservative nisin. The Food Technologist, 27, 100 103.
19. De Rosa, M., Gambacorta, A. Minale, L. (1971). Cyclohexane fatty acids from a thermophilic bacterium. Chemical Communications, 1334.
20. De Rosa, M., Gambacorta, A. Bu'Lock, J.D. (1974). Effects of pH and temperature on the fatty acid composition of Bacillus acidocaldarius. Journal of Bacteriology, 117, 212 214.
21. Dufresne, S., Bousquet, J., Bossinot, M. Guay, R. (1996). Sulfobacillus disulfidooxidans sp.nov., a new acidophilic, disulphide-oxidising, gram-positive, spore forming bacterium. International Journal of Systematic Bacteriology, 46, 1056 1064.
22. Duong, H.A. Jensen, N. (2000). Spoilage of iced tea by Alicyclobacillus. Food Australia, 52, 292.
23. Eiroa, M.N.U., Junqueira, V.C.A. Schmidt, F.L. (1999). Alicyclobacillus in orange juice: occurrence and heat resistance of spores. Journal of Food Protection, 62, 883 886.
24. Funes-Huacca, M., Regitano, L.C.D., Mueller, O. Carrilho, E. (2004). Semiquantitative determination of Alicyclobacillus acidoterrestris in orange juice by reverse-transcriptase polymerase chain reaction and capillary electrophoresis - laser induced fluorescence using microchip technology. Electrophoresis, 25, 3860 3864.
25. Gocmen, D., Elston, A., Williams, T., Parish, M. Rouseff, R.L. (2005). Identification of medicinal off-flavours generated by Alicyclobacillus species in orange juice using GC-olfactometry and GC-MS. Letters in Applied Microbiology, 40, 172 177.
26. Goto, K., Matsubara, H., Mochida, K., et al. (2002). Alicyclobacillus herbarius sp nov., a novel bacterium containing omega-cycloheptane fatty acids, isolated from herbal tea. International Journal of Systematic and Evolutionary Microbiology, 52, 109 113.
27. Goto, K., Mochida, K., Asahara, M., Suzuki, M., Kasai, H. Yokota, A. (2003). Alicyclobacillus pomorum sp. nov., a novel thermo-acidophilic, endospore-forming bacterium that does not possess w-alicyclic fatty acids, and emended description of the genus Alicyclobacillus. International Journal of Systematic and Evolutionary Microbiology, 53, 1537 1544.
28. Grande, M.J., Lucas, R., Abriouel, H., et al. (2005). Control of Alicyclobacillus acidoterrestris in fruit juices by enterocin AS-48. International Journal of Food Microbiology, 104, 289 297.
29. Hippchen, B., Röll, A. Poralla, K. (1981). Occurrence in soil of thermophilic Bacilli possessing -cyclohexane fatty acids and hopanoids. Archives in Microbiology, 129, 53 55.
30. Jensen, N. (1999). Alicyclobacillus- a new challenge for the food industry. Food Australia, 51, 33 36.
31. Jensen, N. Whitfield, F.B. (2003). Role of Alicyclobacillus acidoterrestris in the development of a disinfectant taint in shelf-stable fruit juice. Letters in Applied Microbiology, 36, 9 14.
32. Karavaiko, G.I., Bogdanova, T.I., Tourova, T.P., et al. (2005). Reclassification of 'Sulfobacillus thermosulfidooxidans subsp thermotolerans' strain K1 as Alicyclobacillus tolerans sp nov and Sulfobacillus disulfidooxidans Dufresne et al. 1996 as Alicyclobacillus disulfidooxidans comb. nov., and emended description of the genus Alicyclobacillus. International Journal of Systematic and Evolutionary Microbiology, 55, 941 947.
33. Komitopoulou, E., Boziaris, I.S., Davies, E.A., Delves-Broughton, J. Adams, M.R. (1999). Alicyclobacillus acidoterrestris in fruit juices and its control by nisin. International Journal of Food Science and Technology, 34, 81 84.
34. Kusano, K., Yamada, H., Niwa, M. Yamasato, K. (1997). Propionibacterium cyclohexanicum sp. nov., a new acid-tolerant w-cyclohexyl fatty acid-containing propionibacterium isolated from spoiled orange juice. International Journal of Systematic Bacteriology, 47, 825 831.
35. Langworthy, T.A. Mayberry, W.R. (1976). A 1,2,3,4-tetrahydroxy pentane-substituted pentacyclic triterpene from Bacillus acidocaldarius. Biochimica et Biophysica Acta, 431, 570 577.
36. Lee, S.-Y., Dougherty, H.H. Kang, D.-H. (2002). Inhibitory effects of high pressure and heat on Alicyclobacillus acidoterrestris spores in apple juice. Applied and Environmental Microbiology, 68, 4158 4161.
37. Lee, S.-Y., Gray, P.M., Dougherty, R.H. Kang, D.-H. (2004). The use of chlorine dioxide to control Alicyclobacillus acidoterrestris spores in aqueous suspension and on apples. International Journal of Food Microbiology, 92, 121.
38. Lee, S.-Y., Dancer, G.I., Chang, S., Rhee, M.-S. Kang, D.-H. (2006). Efficacy of chlorine dioxide gas against Alicyclobacillus acidoterrestris spores on apple surfaces. International Journal of Food Microbiology, 108, 364 368.
39. Lin, M., Al-Holy, M., Chang, S. et al. (2005). Rapid discrimination of Alicyclobacillus strains in apple juice by Fourier transform infrared spectroscopy. International Journal of Food Microbiology, 105, 369 376.
40. Luo, H., Yousef, A.E. Wang, H.H. (2004). A real-time polymerase chain reaction-based method for rapid and specific detection of spoilage Alicyclobacillus spp. in apple juice. Letters in Applied Microbiology, 39, 376 382.
41. Matsubara, H., Goto, K., Matsumura, T., et al. (2002). Alicyclobacillus acidophilus sp.nov., a novel thermo-acidophilic, w-alicyclic fatty acid containing bacterium from acidic beverages. International Journal of Systematic and Evolutionary Microbiology, 52, 1681 1685.
42. Murakami, M., Tedzuka, H. Yamazaki, K. (1998). Thermal resistance of Alicyclobacillus acidoterrestris spores in different buffers and pH. Food Microbiology, 15, 577 582.
43. Nakauma, M., Saito, K., Katayama, T., Tada, M. Todoriki, S. (2004). Radiation-heat synergism for inactivation of Alicyclobacillus acidoterrestris spores in citrus juice. Journal of Food Protection, 67, 2538 2543.
44. Nicolaus, B., Improta, R., Manca, M.C., Lama, L., Esposito, E. Gambacorta, A. (1998). Alicyclobacilli from an unexplored geothermal soil in Antarctica: Mount Rittmann. Polar Biology, 19, 133 141.
45. Oita, S. Kohyama, N. (2002). Antibacterial effect of grape polyphenols against thermoacidophilic bacteria Alicyclobacillus acidoterrestris. Journal of the Japanese Society for Food Science and Technology-Nippon Shokuhin Kagaku Kogaku Kaishi, 49, 555 558.
46. Orr, R.V., Shewfelt, R.L., Huang, C.J., Tefera, S. Beuchat, L.R. (2000). Detection of guaiacol produced by Alicyclobacillus acidoterrestris in apple juice by sensory and chromatographic analyses, and comparison with spore and vegetative cell populations. Journal of Food Protection, 63, 1517 1522.
47. Pettipher, G.L. Osmundson, M.E. (2000). Methods for the detection, enumeration and identification of Alicyclobacillus acidoterrestris. Food Australia, 57, 293 295.
48. Pettipher, G.L., Osmundson, M.E. Murphy, J.M. (1997). Methods for the detection and enumeration of Alicyclobacillus acidoterrestris and investigation of growth and production of taint in fruit juice and fruit juice-containing drinks. Letters in Applied Microbiology, 24, 185 189.
49. Pinhatti, M.E.M.C., Variane, S., Eguchi, S.Y. Manfio, G.P. (1997). Detection of acidothermophilic Bacilli in industrialised fruit juices. Fruit Processing, 7, 185 189.
50. Pontius, A.J., Rushing, J.E. Foegeding, P.M. (1998). Heat resistance of Alicyclobacillus acidoterrestris spores as affected by various pH values and organic acids. Journal of Food Protection, 61, 41 46.
51. Roller, S. (1995). The quest for natural antimicrobials as novel means of food preservation: status report on a European research project. International Biodeterioration and Biodegradation, 36, 333 345.
52. Saxby, M.J. (1996). A survey of chemicals causing taints and off-flavours in foods. In : Food Taints and Off-Flavours edited by M.J. Saxby 2nd edn. Pp. 41 71. London : Blackie Academic and Professional.
53. Silva, F.V.M. Gibbs, P. (2001). Alicyclobacillus acidoterrestris spores in fruit products and design of pasteurization processes. Trends in Food Science and Technology, 12, 68 74.
54. Silva, F.M., Gibbs, P., Vieira, M.C. Silva, C.L.M. (1999). Thermal inactivation of Alicyclobacillus acidoterrestris spores under different temperature, soluble solids and pH conditions for the design of fruit processes. International Journal of Food Microbiology, 51, 95 103.
55. Simbahan, J., Drijber, R. Blum, P. (2004). Alicyclobacillus vulcanalis sp nov., a thermophilic, acidophilic bacterium isolated from Coso Hot Springs, California, USA. International Journal of Systematic and Evolutionary Microbiology, 54, 1703 1707.
56. Splittstoesser, D.F., Churey, J.J. Lee, C.Y. (1994). Growth characteristics of aciduric spore forming bacilli isolated from fruit juices. Journal of Food Protection, 57, 1080 1083.
57. Splittstoesser, D.F., Lee, C.Y. Churey, J.J. (1998). Control of Alicyclobacillus in the juice industry. Dairy, Food and Environment Sanitation, 18, 1 5.
58. Suzuki, K., Saito, K., Kawaguchi, A., Okuda, S. Komagata, K. (1981). Occurrence of w-cyclohexyl fatty acids in Curtobacterium pusillum strains. Journal of General and Applied Microbiology, 27, 261 266.
59. Tsuruoka, N., Isono, Y., Shida, O., Hemmi, H., Nayayama, T. Nishino, T. (2003). Alicyclobacillus sendaiensis sp. nov., a novel acidophilic, slightly acidphilic species isolated from soil in Sendai, Japan. International Journal of Systematic and Evolutionary Microbiology, 53, 1081 1084.
60. Uchino, F. Doi, S. (1967). Acido-thermophilic bacteria from thermal waters. Agricultural and Biological Chemistry, 31, 817 822.
61. Vieira, M.C., Teixeira, A.A., Silva, F.M., Gaspar, N. Silva, C.L.M. (2002). Alicyclobacillus acidoterrestris spores as a target for Cupuacu (Theobroma grandiflorum) nectar thermal processing: kinetic parameters and experimental methods. International Journal of Food Microbiology, 77, 71 81.
62. Walker, M. Phillips, C.A. (2005). The effect of intermittent shaking, headspace and temperature on the growth of Alicyclobacillus acidoterrestris in stored apple juice. International Journal of Food Science and Technology, 40, 557 562.
63. Walls, I. Chuyate, R. (1998). Alicyclobacillus- historical perspective and preliminary characterisation study. Dairy, Food and Environmental Sanitation, 18, 499 503.
64. Walls, I. Chuyate, R. (2000). Spoilage of fruit juices by Alicyclobacillus acidoterrestris. Food Australia, 52, 286.
65. Whitfield, F.B., Last, J.H., Shaw, K.J. Tindale, C.T. (1988). 2,6-Dibromophenol: the cause of an iodoform-like off-flavour in some Australian crustacea. Journal of the Science of Food and Agriculture, 46, 29 42.
66. Wisse, C.A. Parish, M.E. (1998). Isolation and enumeration of sporeforming, thermo-acidophilic, rod-shaped bacteria from citrus processing environments. Dairy, Food and Environmental Sanitarians, 18, 504 509.
67. Wisotzkey, J.D., Jurtshuk, P., Fox, G.E., Deinhard, G. Poralla, K. (1992). Comparative sequence analyses on the 16S rRNA (rDNA) of Bacillus acidocaldarius, Bacillus acidoterrestris and Bacillus cycloheptanicus and proposal for creation of a new genus, Alicyclobacillus gen. nov. International Journal of Systematic Bacteriology, 42, 263 269.
68. Yamazaki, K., Teduka, H. Shinano, H. (1996a). Isolation and identification of Alicyclobacillus acidoterrestris from acidic beverages. Bioscience, Biotechnology and Biochemistry, 60, 543 545.
69. Yamazaki, K., Teduka, H., Inoue, N. Shinano, H. (1996b). Specific primers for the detection of Alicyclobacillus acidoterrestris by RT-PCR. Letters in Applied Microbiology, 23, 350 354.
70. Yamazaki, K., Okubo, T., Inoue, N. Shinano, H. (1997). Randomly amplified polymorphic DNA (RAPD) for rapid identification of the spoilage bacterium Alicyclobacillus acidoterrestris. Bioscience Biotechnology and Biochemistry, 61, 1016 1018.
71. Yamazaki, K., Murakami, M., Kawai, Y., Inoue, N. Matsuda, T. (2000). Use of nisin for inhibition of Alicyclobacillus acidoterrestris in acidic drinks. Food Microbiology, 17, 315 320.
72. Yeh, J.Y., Hoogetoorn, E. Chen, J.R. (2004). Influence of calcium lactate on the fate of spoilage and pathogenic microorganisms in orange juice. Journal of Food Protection, 67, 1429 1432.
73. Young, W.F., Horth, H., Crane, R., Ogden, T. Arnott, M. (1996). Taste and odour threshold concentrations of potential potable water contaminants. Water Research, 30, 331 340.
74. Zierler, B., Siegmund, B. Pfannhauser, W. (2004). Determination of off-flavour compounds in apple juice caused by microorganisms using headspace solid phase microextraction-gas chromatography-mass spectrometry. Analytica Chimica Acta, 520, 3 11.