Alicyclobacillus acidoterrestris in pasteurized exotic Brazilian fruit juices: Isolation, genotypic characterization and heat resistance

Food Microbiology

Volumn 27, Issue 8, 2010, Pages 1016-1022

  McKnight, I C ^a   Eiroa, M N U ^a   Sant'Ana, A S ^b   Massaguer, P R ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ALICYCLOBACILLUS; ARTICLE; BEVERAGE; BRAZIL; CHEMISTRY; CLASSIFICATION; FOOD HANDLING; FRUIT; GENETICS; GENOTYPE; HEAT; ISOLATION AND PURIFICATION; MICROBIAL VIABILITY; MICROBIOLOGY; PASSION FRUIT; PHYLOGENY; PINEAPPLE; RANDOM AMPLIFIED POLYMORPHIC DNA; SEASON;

ALICYCLOBACILLUS; ANANAS; BEVERAGES; BRAZIL; FOOD HANDLING; FRUIT; GENOTYPE; HOT TEMPERATURE; MICROBIAL VIABILITY; PASSIFLORA; PHYLOGENY; RANDOM AMPLIFIED POLYMORPHIC DNA TECHNIQUE; SEASONS;

ALICYCLOBACILLUS; ALICYCLOBACILLUS ACIDOTERRESTRIS; ANANAS COMOSUS; PASSIFLORA EDULIS;

EID: 80054072955     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2010.06.010     Document Type: Article

References (65)

1. Association of the Industries of Juices and Nectars from Fruits and Vegetables of the European Union (AIJN), 2007. Alicyclobacillus best practice guideline, incorporating comments from Hague Working Group. 10th. Version 10. p. 28.
2. Al-Qadiri H.M., Lin M., Cavinato A.G., Rasco B.A. Fourier transform infrared spectroscopy, detection and identification of Escherichia coli O157:H7 and Alicyclobacillus strains in apple juice. Int. J. Food Microbiol. 2006, 111:73-80.
3. Bahçeci K.S., Acar J. Modeling the combined effects of pH, temperature and ascorbic acid concentration on the heat resistance of Alicyclobacillus acidoterrestris. Int. J. Food Microbiol. 2007, 120:266-273.
4. Barrios Eguiluz K.I., Salazar-Banda G.R., Funes-Huacca M.E., Alberice J.V., Carrilho E., Spinola MacHado S.A., et al. Sequence-specific electrochemical detection of alicyclobacillus acidoterrestris DNA using electroconductive polymer-modified fluorine tin oxide electrodes. Analyst 2009, 134:314-319.
5. Bevilacqua A., Sinigaglia M., Corbo M.R. Alicyclobacillus acidoterrestris: new methods for inhibiting spore germination. Int. J. Food Microbiol. 2008, 125:103-110.
6. Borlinghaus A., Engel R. Alicyclobacillus incidences in commercial apple juice concentrate (AJC) supplies - method development and validation. Fruit Proc. 1997, 7:262.
7. Carvalho A.A.T., Vanetti M.C.D., Mantovani H.C. Bovicin HC5 reduces thermal resistance of Alicyclobacillus acidoterrestris in acidic mango pulp. J. Appl. Microbiol. 2008, 104:1685-1691.
8. Cerny G., Hennlich W., Poralla K. Fruchtsaftverderb durch bacillen: isolierung und harakterisierung des verderbserregers. Zeitschrift für. Leb. Unt. Forsch 1984, 179:224-227.
9. Chang S.-S., Kang D.-H. Alicyclobacillus spp. in the fruit juice industry: history, characteristics, and current isolation/detection procedures. Crit. Rev. Microbiol. 2004, 30:55-74.
10. Chen S., Tang Q., Zhang X., Zhao G., Hu X., Liao X., Chen F., Wu J., Xiang J. Isolation and characterization of thermo-acidophilic endospore-forming bacteria from the concentrated apple juice-processing environment. Food Microbiol. 2006, 23:439-445.
11. Darland G., Brock T.D. Bacillus acidocaldarius sp. nov., an acidophilic thermophilic spore-forming bacterium. J. Gen. Microbiol. 1971, 67:9-15.
12. Deinhard G., Blanz P., Poralla K., Altan E. Bacillus acidoterrestris sp. nov., a new thermotolerant acidophile isolated from different soils. Syst. Appl. Microbiol. 1987, 10:47-53.
13. Doyle J.J., Doyle J.L. Isolation of plant DNA from fresh tissue. Focus 1990, 12:13-15.
14. Eguchi S.Y., Azuma E.H., Pinhatti M.E.C., Manfio G.P., Variane S. Acidotermophilic sporeforming bacteria (ATSB) in orange juices. Detection methods, ecology and involvement in the deterioration of fruit juices. Part II. Fruit Proc. 2001, 2:55-62.
15. Eguchi S.Y., Azuma E.H., Pinhatti M.E.C., Manfio G.P., Variane S. Acidotermophilic sporeforming bacteria (ATSB) in orange juices. Detection methods, ecology and involvement in the deterioration of fruit juices. Part I. Fruit Proc. 2001, 1:12-18.
16. Eguchi S.Y., Azuma E.H., Pinhatti M.E.C., Manfio G.P., Variane S. Acidotermophilic sporeforming bacteria (ATSB) in orange juices. Detection methods, ecology and involvement in the deterioration of fruit juices. Part III. Fruit Proc. 2001, 3:95-101.
17. Eiroa M.N.U., Junqueira V.C.A., Schmidt F.L. Alicyclobacillus in orange juice: occurrence and heat resistance of spores. J. Food Prot. 1999, 62:883-886.
18. Food and Agriculture Organization Statistics FAOStat 2009, Available at, (accessed 12.08.09). http://faostat.fao.org/site/339/default.aspx.
19. Friedrich L.M., Goodrich-Schneider R., Parish M.E., Danyluk M.D. Mitigation of Alicyclobacillus spp. spores on food contact surfaces with aqueous chlorine dioxide and hypochlorite. Food Microbiol. 2009, 26:936-941.
20. Funes-Huacca M., Regitano L.C.A., Mueller O., Carrilho E. Semiquantitative determination of Alicyclobacillus acidoterrestris in orange juice by reverse-transcriptase polymerase chain reaction and capillary electrophoresis - laser induced fluorescence using microchip technology. Electrophoresis 2004, 25:3860-3864.
21. Gonçalves J.S., Souza S.A.M. Fruta da paixão: panorama econômico do maracujá no Brasil. Inform. Econ. 2006, 36:1-8.
22. Gordon R.E. The Genus Bacillus 1973, Agricultural Hanbook n.427, USDA-ARS, Washington.
23. Goto K., Matsubara H., Mochida K., Matsubara T., Hara Y., Niwa M., Yamasato K. Alicyclobacillus herbarius sp. nov., a novel bacterium containing omega-cycloheptane fatty acids, isolated from herbal tea. Int. J. Syst. Evol. Microbiol. 2002, 52:109-113.
24. Goto K., Mochida K., Asahara M., Suzuki M., Kasai H., Yokota A. Alicyclobacillus pomorum sp. nov., a novel thermo-acidophilic, endospore-forming bacterium that does not possess-alicyclic fatty acids, and emended description of the genus Alicyclobacillus. Int. J. Syst. Evol. Microbiol. 2003, 53:1537-1544.
25. Goto K., Mochida K., Kato Y., Asahara M., Fujita R., Na S.-Y., Kasai H., Yokota A. Proposal of six species of moderately thermophilic, acidophilic, endospore-forming bacteria: alicyclobacillus contaminans sp. nov., Alicyclobacillus fastidiosus sp. nov., Alicyclobacillus kakegawensis sp. nov., Alicyclobacillus macrosporangiidus sp. nov., Alicyclobacillus sacchari sp. nov. and Alicyclobacillus shizuokensis sp. nov. Int. J. Syst. Evol. Microbiol. 2007, 57:1276-1285.
26. Goto K., Nishibori A., Wasada Y., Furuhata K., Fukuyama M., Hara M. Identification of thermo-acidophilic bacteria isolated from the soil of several japanese fruit orchards. Lett. Appl. Microbiol. 2008, 46:289-294.
27. Gouws P.A., Gie L., Pretorius A., Dhansay N. Isolation and identification of alicyclobacillus acidocaldarius by 16S rDNA from mango juice and concentrate. Int. J. Food Sci. Technol. 2005, 40:789-792.
28. Groenewald W.H., Gouws P.A., Witthuhn R.C. Isolation, identification and typification of Alicyclobacillus acidoterrestris and Alicyclobacillus acidocaldarius strains from orchard soil and the fruit processing environment in South Africa. Food Microbiol. 2009, 26:71-76.
29. Hassimotto N.M.A., Genovese Maria Inês, Lajolo F.M. Antioxidant capacity of Brazilian fruit, vegetables and commercially-frozen fruit pulps. J. Food Compos. Anal. 2009, 22:394-396.
30. Hoffman-Ribani R., Huber L.S., Rodriguez-Amaya D.B. Flavonols in fresh and processed Brazilian fruits. J. Food Compos. Anal. 2009, 22:263-268.
31. Jeyaram K., Singh W.M., Premarani T., Devi A.R., Chanu K.S., Talukdar N.C., Singh M.R. Molecular identification of dominant microflora associated with 'Hawaijar'-a traditional fermented soybean (Glycine max (L.)) food of Manipur, India. Int. J. Food Microbiol. 2008, 122:259-268.
32. Lee S.-Y., Gray P.M., Dougherty R.H., Kang D.-H. The use of chlorine dioxide to control Alicyclobacillus acidoterrestris spores in aqueous suspension and on apples. Int. J. Food Microbiol. 2004, 92:121-127.
33. Lee S.-Y., Dancer G.I., Chang S., Rhee M.-S., Kang D.-H. Efficacy of chlorine dioxide gas against Alicyclobacillus acidoterrestris spores on apple surfaces. Int. J. Food Microbiol. 2006, 108:364-368.
34. Leguèrinel I., Couvert O., Mafart P. Modeling the influence of the incubation temperature upon the estimated heat resistance of heated bacillus spores. Lett. Appl. Microbiol. 2006, 43:17-21.
35. Lin M., Al-Holy M., Chang S.-S., Huang Y., Cavinato A.G., Kang D.-H., Rasco B.A. Rapid discrimination of Alicyclobacillus strains in apple juice by Fourier transform infrared spectroscopy. Int. J. Food Microbiol. 2005, 105:369-376.
36. Luo H., Yousef A.E., Wang H.H. A real-time polymerase chain reaction-based method for rapid and specific detection of spoilage Alicyclobacillus spp. in apple juice. Lett. Appl. Microbiol. 2004, 39:376-382.
37. Matsubara H., Goto K., Matsumura T., Mochida K., Iwaki M., Niwa M., Yamasato K. Alicyclobacillus acidiphilus sp. nov., a novel thermo-acidophilic, omega-alicyclic fatty acid-containing bacterium isolated from acidic beverages. Int. J. Syst. Evol. Microbiol. 2002, 52:1681-1685.
38. McIntyre S., Ikawa J.Y., Parkinson N., Haglund J., Lee J. Characterization of an acidophilic Bacillus strain isolated from shelf-stable juices. J. Food Prot. 1995, 58:319-321.
39. Oliveira A.O., Lopes R.B., Cabral F.B., Eberlin M.N. Volatile compounds from pitanga fruit (Eugenia uniflora L.). Food Chem. 2006, 99:1-5.
40. Orr R.V., Beuchat L.R. Efficacy of disinfectants in killing spores of Alicyclobacillus acidoterrestris and performance of media for supporting colony development by survivors. J. Food Prot. 2000, 63:1117-1122.
41. Palop A., Alvarez I., Raso J., Condon S. Heat resistance of Alicyclobacillus acidocaldarius in water, various buffers, and orange juice. J. Food Prot. 2000, 63:1377-1380.
42. Parish M.E., Goodrich R.M. Recovery of presumptive Alicyclobacillus strains from orange fruit surfaces. J. Food Prot. 2005, 68:2196-2200.
43. Pena W.E.L., Massaguer P.R. Microbial modeling of Alicyclobacillus acidoterrestris CRA 7152 growth in orange juice with nisin added. J. Food Prot. 2006, 69:1904-1912.
44. Pettipher G.L., Osmundson M.E., Murphy J.M. Methods for the detection and enumeration of Alicyclobacillus acidoterrestris and investigation of growth and production of taint on fruit juice and fruit juice-containing drink. Lett. Appl. Microbiol. 1997, 24:185-189.
45. Pinhatti M.E.M.C., Variane S., Eguchi S.Y., Manfio G.P. Detection of acidothermophilic bacilli in industrialized fruit juices. Fruit Proc. 1997, 9:350-353.
46. Podolak R., Elliott P.H., Taylor B.J., Kurana A., Black D.G. Destruction of Alicyclobacillus acidoterrestris spores in apple juice on stainless steel surfaces by chemical disinfectants. J. Food Prot. 2009, 72:510-514.
47. Pontius A.J., Rushing J.E., Foegeding P.M. Heat resistance of Alicyclobacillus acidoterrestris spores as affected by various pH values and organic acids. J. Food Prot. 1998, 61:41-46.
48. Previdi M.P., Colla P., Vicini E. Characterization of Alicyclobacillus, a spore-forming thermophilic acidophilic bacterium. Indust. Conserve 1995, 70:128-132.
49. Rodrigues S., Barbosa M.F., Ferreira J.O., Reyes A., Massaguer P.R. Building of an Orange washing pilot plant machine to evaluate superficial disinfection of Orange fruits against Alicyclobacillus acidoterrestris. Alim. Cienc. Ing. 2007, 16:332-334.
50. Rohlf F.J. NTSYSpc Version 2.0: User's Guide 1998, Applied Biostatistics Inc.
51. Ronimus R.S., Parker L.E., Morgan H.W. The utilization of RAPD-PCR for identifying thermophilic and mesophilic Bacillus species. FEMS Microbiol. Lett. 1997, 147:75-79.
52. Rosso V.V., Mercadante A.Z. Identification and quantification of carotenoids, by HPLC-PDA-MS/MS, from Amazonian fruits. J. Agric. Food Chem. 2007, 55:5062-5072.
53. Spinelli A.C.N., Sant'Ana A.S., Rodrigues-Junior S., Massaguer P.R. Influence of different storage temperatures on Alicyclobacillus acidoterrestris CRA7152 growth in hot-filled orange juice. Appl. Environ. Microbiol. 2009, 137:295-298.
54. Spinelli A.C.N., Sant'Ana A.S., Pacheco-Sanchez C.P., Massaguer P.R. Influence of the hot-fill water-spray-cooling process after continuous pasteurization on the number of decimal reductions and on Alicyclobacillus acidoterrestris CRA 7152 growth in orange juice stored at 35 °C. Int. J. Food Microbiol. 2010, 137:295-298.
55. Splittstoesser D.F., Churey J.J., Lee C.Y. Growth characteristics of aciduric sporeforming bacilli isolated from fruit juices. J. Food Prot. 1994, 57:1080-1083.
56. Splittstoesser D.F., Lee C.Y., Churey J.J. Control of Alicyclobacillus in the juice industry. Dairy Food Environ. Sanit. 1998, 18:1-5.
57. Stumbo C.R. Thermobacteriology in Food Processing 1973, Academic Press, New York, 329 pp. (ISBN-13: 9780126753523).
58. Torriani S., Clementi F., Vancanneyt M., Hoste B., Dellaglio F., Kersters K. Differentiation of Lactobacillus plantarum, L. pentosus and L. paraplantarum species by RAPD-PCR and AFLP. Syst. Appl. Microbiol. 2001, 24:554-560.
59. Tribst A.A.L., Sant'Ana A.S., Massaguer P.R. Review: microbiological quality and safety of fruit juices: past, present and future perspectives. Crit. Rev. Microbiol. 2009, 35:310-339.
60. Walls I., Chuyate R. Alicyclobacillus - historical perspective and preliminary characterization study. Dairy Food Environ. Sanit. 1998, 18:499-503.
61. Walls I., Chuyate R. Isolation of Alicyclobacillus acidoterrestris from fruit juices. J. AOAC Int. 2000, 83:1115-1120.
62. Wisotzkey J.D., Jurtshuk P., George J.R., Fox E., Deinhard G., Poralla K. 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. Int. J. Syst. Bacteriol. 1992, 42:263-269.
63. Yamazaki K., Kawai Y., Inoue N., Shinano H. Influence of sporulation medium and divalent ions on the heat resistance of Alicyclobacillus acidoterrestris spores. Lett. Appl. Microbiol. 1997, 25:153-156.
64. Yamazaki K., Okubo T., Inoue N., Shinano H. Randomly amplified polymorphic DNA (RAPD) for rapid identification of the spoilage bacterium Alicyclobacillus acidoterrestris. Biosci. Biotechnol. Biochem. 1997, 61:1016-1018.
65. Zanatta C.F., Mercadante A.Z. Carotenoid composition from the Brazilian tropical fruit camu-camu (Myrciaria dubia). Food Chem. 2007, 101:1543-1549.