Identification of guaiacol producing Alicyclobacillus recovered from commercial orange juices distributed in Greek markets
Main Article Content
Keywords
Alicyclobacillus acidoterrestris, orange juice, PCR-RFLP, vdc gene
Abstract
The objective of this work was the isolation and characterization of Alicyclobacillus acidoterrestris strains from orange juice. In all, 72 isolates were recovered from commercial orange juice bought from the Greek market. The isolates were subjected to polymerase chain reaction–restriction fragment length polymorphism (PCR-RFLP) to discriminate them at strain level and A. acidoterrestris types I and II. The restriction patterns of 16S rRNA gene revealed that isolates were categorized in different groups depending on the restriction endonucleases. Moreover, the digestion of the part of vdc operon gene with HphI restriction enzyme successfully differentiated between A. acidoterrestris types I and II. In conclusion, RFLP succeeded in differentiating A. acidoterrestris isolates at strain and type levels.
References
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International Federation of Fruit Juice Producers. 2007. Method on the detection of taint producing Alicyclobacillus in fruit juices. IFU method No. 12, 2004/2007. IFU, Copenhagen, Denmark.
Klijn N., Weerkamp A.H., and de Vos W.M. 1991. Identification of mesophilic lactic acid bacteria by using polymerase chain reaction-amplified variable regions of 16S rRNA and specific DNA probes. Appl Environ Microbiol. 57:3390–3393. 10.1128/aem.57.11.3390-3393.1991
Lusardi C., Previdi M.P., Colla F., Barbieri G., and Bolzoni L. 2000. Ability of Alicyclobacillus strains to spoil fruit juices and nectars. Ind Conserve Italy. 75:151–161.
McKnight I., Eiroa M., Sant’Ana A., and Massaguer P. 2010. Alicyclobacillus acidoterrestris in pasteurized exotic Brazilian fruit juices: isolation, genotypic characterization and heat resistance. Food Microbiol. 27:1016–1022. 10.1016/j.fm.2010.06.010
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Roth K., Rana Y.S., Daeschel D., Kovac J., Worobo R., and Snyder A.B. 2021. Alicyclobacillus mali spp. nov., Alicyclobacillus suci spp. nov., and Alicyclobacillus fructus spp. nov., thermoacidophilic sporeforming bacteria isolated from fruit beverages. Int J Syst Evol Microbiol. 71(9):5016. 10.1099/ijsem.0.005016
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Silva F.V.M., Gibbs P., and Silva C.L.M. 2000. Establishing a new pasteurisation criterion based on Alicyclobacillus acidoterrestris spores for shelf-stable high-acidic fruit products. Fruit Proces. 4:138–141.
Smit Y., Cameron M., Venter P., and Witthuhn R.C. 2011. Alicyclobacillus spoilage and isolation—a review. Food Microbiol. 28:331–349. 10.1016/j.fm.2010.11.008
Sourri P., Doulgeraki A.I., Tassou C.C., and Nychas G.-J.E. 2019. A single enzyme PCR-RFLP assay targeting V1-V3 region of 16S rRNA gene for direct identification of Alicyclobacillus acidoterrestris from other Alicyclobacillus species. J Appl Genet. 60:225–229. 10.1007/s13353-019-00498-8
Sourri P., Tassou C.C., Nychas G.-J.E., and Panagou E.Z. 2022. Fruit juice spoilage by Alicyclobacillus: detection and control methods—a comprehensive review. Foods. 11:747. 10.3390/foods11050747
Thelen K. (2003). Specific rapid detection of Alicyclobacillus by fluorescently labeled gene probes in fruit juices. Fruit Proces. 6:416–418.
Uchida R., and Silva F.V. 2017. Alicyclobacillus acidoterrestris spores inactivation by high pressure combined with mild heat: modeling the effects of temperature and soluble solids. Food Control. 73:426–432. 10.1016/j.foodcont.2016.08.034
Van Luong T.S., Moir C.J., Kaur M., Frank D., Bowman J.P., and Bradbury M.I. 2019. Diversity and guaiacol production of Alicyclobacillus spp. from fruit juice and fruit-based beverages. Int J Food Microbiol. 2:311:108314. 10.1016/j.ijfoodmicro.2019.108314
Vieira M.C., Teixeira A.A., Silva F.M., Gaspar N., and Silva C.L.M. 2002. Alicyclobacillus acidoterrestris spores as a target for Cupuaçu (Theobroma grandiflorum) nectar thermal processing: kinetic parameters and experimental methods. Int J Food Microbiol. 77:71–81. 10.1016/S0168-1605(02)00043-0
Wang Z., Yue T., Yuan Y., Zhang Y., Gao Z., and Cai R. 2021. Targeting the vanillic acid decarboxylase gene for Alicyclobacillus acidoterrestris quantification and guaiacol assessment in apple juices using real time PCR. Int J Food Microbiol. 338:109006. 10.1016/j.ijfoodmicro.2020.109006
Witthuhn R.C., Smit Y., Cameron M., and Venter P. 2011. Isolation of Alicyclobacillus and the influence of different growth parameters. Int J Food Microbiol. 146:63–68. 10.1016/j.ijfoodmicro.2011.02.002
Yamazaki K., Teduka H., Inoue N., and Shinano H. 1996. Specific primers for detection of Alicyclobacillus acidoterrestris by RT-PCR. Lett Appl Microbiol. 23:350–354. 10.1111/j.1472-765X.1996.tb00206.x
Zhang J., Yue T., and Yuan Y. 2013. Alicyclobacillus contamination in the production line of Kiwi products in China. PLoS One. 2-8(7):67704. 10.1371/journal.pone.0067704
Centers for Disease Control and Prevention (CDC). 1999. Outbreak of salmonella serotype Muenchen infections associated with unpasteurized orange juice—United States and Canada, June 1999. MMWR Morb Mortal Wkly Rep. 1999 Jul 16;48(27):582–585. Available at: https://www.cdc.gov/mmwr/preview/mmwrhtml/mm4827a2.htm (accessed: 30 January 2022).
Chen S., Tang Q., Zhang X., Zhao G., Hu X., Liao X., et al. 2006. Isolation and characterization of thermo-acidophilic endospore-forming bacteria from the concentrated apple juice-processing environment. Food Microbiol. 23:439–445. 10.1016/j.fm.2005.07.005
Dekowska A., Niezgoda J., and Sokolowska B. 2018. Genetic heterogeneity of Alicyclobacillus strains revealed by RFLP analysis of vdc region and rpoB gene. Biomed Res Int. 2018:9608756. 10.1155/2018/9608756
Doerge D.R., Divi R.L., and Churchwell M.I. 1997. Identification of the colored guaiacol oxidation product produced by peroxidases. Anal Biochem. 250:10–17. 10.1006/abio.1997.2191
Durak M.Z., Churey J.J., Danyluk M.D., and Worobo R.W. 2010. Identification and haplotype distribution of Alicyclobacillus spp. from different juices and beverages. Int J Food Microbiol. 142:286–291. 10.1016/j.ijfoodmicro.2010.07.003
Eguchi S., Manfio G., Pinhatti M., Azuma E., and Variane S. 1999. Acidothermophilic sporeforming bacteria (ATSB) in orange juices: detection methods, ecology, and involvement in the deterioration of fruit juices. Brazillian Association of Citrus Exports (CitrusBR), Corpus ID: 166224686, pp. 25–35. https://api.semanticscholar.org/CorpusID:166224686
Eiroa M.N.U., Junqueira V.C.A., and Schmidt F.L. 1999. Alicyclobacillus in orange juice: occurrence and heat resistance of spores. J Food Prot. 62:883–886. 10.4315/0362-028X-62.8.883
Gocmen D., Elston A., Williams T., Parish M., and Rouseff R. 2005. Identification of medicinal off-flavours generated by Alicyclobacillus species in orange juice using GC-olfactometry and GC-MS. Lett Appl Microbiol. 40:172–177. 10.1111/j.1472-765X.2004.01636.x
Gouws P.A., Gie L., Pretorius A., and Dhansay N. 2005. Isolation and identification of Alicyclobacillus acidocaldarius by 16S rDNA from mango juice and concentrate. Int J Food Sci Technol. 40;789–792. 10.1111/j.1365-2621.2005.01006.x
Griffiths M. 2000. The new face of food born illness. Can Meat Sci Assoc. 1:6–9.
Hartyáni P., Dalmadi I., and Knorr D. 2013. Electronic nose investigation of Alicyclobacillus acidoterrestris inoculated apple and orange juice treated by high hydrostatic pressure. Food Control. 32:262–269. 10.1016/j.foodcont.2012.10.035
International Federation of Fruit Juice Producers. 2007. Method on the detection of taint producing Alicyclobacillus in fruit juices. IFU method No. 12, 2004/2007. IFU, Copenhagen, Denmark.
Klijn N., Weerkamp A.H., and de Vos W.M. 1991. Identification of mesophilic lactic acid bacteria by using polymerase chain reaction-amplified variable regions of 16S rRNA and specific DNA probes. Appl Environ Microbiol. 57:3390–3393. 10.1128/aem.57.11.3390-3393.1991
Lusardi C., Previdi M.P., Colla F., Barbieri G., and Bolzoni L. 2000. Ability of Alicyclobacillus strains to spoil fruit juices and nectars. Ind Conserve Italy. 75:151–161.
McKnight I., Eiroa M., Sant’Ana A., and Massaguer P. 2010. Alicyclobacillus acidoterrestris in pasteurized exotic Brazilian fruit juices: isolation, genotypic characterization and heat resistance. Food Microbiol. 27:1016–1022. 10.1016/j.fm.2010.06.010
Molva C., and Baysal A.H. 2015. Evaluation of bioactivity of pomegranate fruit extract against Alicyclobacillus acidoterrestris DSM 3922 vegetative cells and spores in apple juice. LWT. 62:989–995. 10.1016/j.lwt.2015.02.021
Osopale B.A., Witthuhn C.R., Albertyn J., and Oguntoyinbo F.A. 2016. Culture-dependent and independent genomic identification of Alicyclobacillus species in contaminated commercial fruit juices. Food Microbiol. 56:21–28. 10.1016/j.fm.2015.11.014
Pinhatti M.E.M.C., Variane S., Eguchi S.Y., and Manfio G.P. 1997. Detection of Acidothermophilic bacilli in industrialized fruit juices. Fruit Process. 9:350–353.
Roth K., Rana Y.S., Daeschel D., Kovac J., Worobo R., and Snyder A.B. 2021. Alicyclobacillus mali spp. nov., Alicyclobacillus suci spp. nov., and Alicyclobacillus fructus spp. nov., thermoacidophilic sporeforming bacteria isolated from fruit beverages. Int J Syst Evol Microbiol. 71(9):5016. 10.1099/ijsem.0.005016
Silva F., and Gibbs P. 2001. Alicyclobacillus acidoterrestris spores in fruit products and design of pasteurization processes. Trends Food Sci Technol. 12:68–74. 10.1016/S0924-2244(01)00070-X
Silva F.V.M., Gibbs P., and Silva C.L.M. 2000. Establishing a new pasteurisation criterion based on Alicyclobacillus acidoterrestris spores for shelf-stable high-acidic fruit products. Fruit Proces. 4:138–141.
Smit Y., Cameron M., Venter P., and Witthuhn R.C. 2011. Alicyclobacillus spoilage and isolation—a review. Food Microbiol. 28:331–349. 10.1016/j.fm.2010.11.008
Sourri P., Doulgeraki A.I., Tassou C.C., and Nychas G.-J.E. 2019. A single enzyme PCR-RFLP assay targeting V1-V3 region of 16S rRNA gene for direct identification of Alicyclobacillus acidoterrestris from other Alicyclobacillus species. J Appl Genet. 60:225–229. 10.1007/s13353-019-00498-8
Sourri P., Tassou C.C., Nychas G.-J.E., and Panagou E.Z. 2022. Fruit juice spoilage by Alicyclobacillus: detection and control methods—a comprehensive review. Foods. 11:747. 10.3390/foods11050747
Thelen K. (2003). Specific rapid detection of Alicyclobacillus by fluorescently labeled gene probes in fruit juices. Fruit Proces. 6:416–418.
Uchida R., and Silva F.V. 2017. Alicyclobacillus acidoterrestris spores inactivation by high pressure combined with mild heat: modeling the effects of temperature and soluble solids. Food Control. 73:426–432. 10.1016/j.foodcont.2016.08.034
Van Luong T.S., Moir C.J., Kaur M., Frank D., Bowman J.P., and Bradbury M.I. 2019. Diversity and guaiacol production of Alicyclobacillus spp. from fruit juice and fruit-based beverages. Int J Food Microbiol. 2:311:108314. 10.1016/j.ijfoodmicro.2019.108314
Vieira M.C., Teixeira A.A., Silva F.M., Gaspar N., and Silva C.L.M. 2002. Alicyclobacillus acidoterrestris spores as a target for Cupuaçu (Theobroma grandiflorum) nectar thermal processing: kinetic parameters and experimental methods. Int J Food Microbiol. 77:71–81. 10.1016/S0168-1605(02)00043-0
Wang Z., Yue T., Yuan Y., Zhang Y., Gao Z., and Cai R. 2021. Targeting the vanillic acid decarboxylase gene for Alicyclobacillus acidoterrestris quantification and guaiacol assessment in apple juices using real time PCR. Int J Food Microbiol. 338:109006. 10.1016/j.ijfoodmicro.2020.109006
Witthuhn R.C., Smit Y., Cameron M., and Venter P. 2011. Isolation of Alicyclobacillus and the influence of different growth parameters. Int J Food Microbiol. 146:63–68. 10.1016/j.ijfoodmicro.2011.02.002
Yamazaki K., Teduka H., Inoue N., and Shinano H. 1996. Specific primers for detection of Alicyclobacillus acidoterrestris by RT-PCR. Lett Appl Microbiol. 23:350–354. 10.1111/j.1472-765X.1996.tb00206.x
Zhang J., Yue T., and Yuan Y. 2013. Alicyclobacillus contamination in the production line of Kiwi products in China. PLoS One. 2-8(7):67704. 10.1371/journal.pone.0067704
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May 24, 2024
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Sourri, P., Dekowska, A., E. Nychas, G.-J., C. Tassou, C., & Doulgeraki, A. (2024). Identification of guaiacol producing Alicyclobacillus recovered from commercial orange juices distributed in Greek markets (J. Bucka-Kolendo , Trans.). Italian Journal of Food Science, 36(2), 205-215. https://doi.org/10.15586/ijfs.v36i2.2476
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How to Cite
Sourri, P., Dekowska, A., E. Nychas, G.-J., C. Tassou, C., & Doulgeraki, A. (2024). Identification of guaiacol producing Alicyclobacillus recovered from commercial orange juices distributed in Greek markets (J. Bucka-Kolendo , Trans.). Italian Journal of Food Science, 36(2), 205-215. https://doi.org/10.15586/ijfs.v36i2.2476