Alicyclobacillus

Alicyclobacillus is a genus of Gram-variable, rod-shaped, spore-forming bacteria. The bacteria are able to grow in acidic conditions, while the spores are able to survive typical pasteurization procedures.

Alicyclobacillus
Scientific classification
Domain:
Bacteria
Division:
Firmicutes
Class:
Bacilli
Order:
Bacillales
Family:
Alicyclobacillaceae
Genus:
Alicyclobacillus

Wisotzkey 1992
Species

A. acidiphilus
A. acidocaldarius
A. acidocaldarius subsp. acidocaldarius
A. acidocaldarius subsp. rittmannii
A. acidoterrestris
A. aeris
A. cellulosilyticus[1]
A. contaminans
A. cycloheptanicus
A. dauci[1]
A. disulfidooxidans
A. fastidiosus
A. ferrooxydans
A. fodiniaquatilis[1]
A. herbarius
A. hesperidum
A. kakegawensis
A. macrosporangiidus
A. montanus
A. pomorum
A. sacchari
A. sendaiensis
A. shizuokensis
A. tengchongensis[1]
A. tolerans
A. vulcanalis

Overview

Alicyclobacilli are strictly aerobic, acidophilic, mesophilic to thermophilic, soil-dwelling organisms.[2] Alicyclobacilli are of special interest to the fruit juice canning industry because common pasteurization techniques (92 °C for 10 seconds) do not deactivate the spores;[3] Alicyclobacillus species can have a D95-value of over 8 minutes (requiring treatment of over 8 minutes at 95 °C to kill 90% of spores).[4] When a product is spoiled by Alicyclobacillus, the juice products develop a disinfectant-like odor and/or flavor (due to guaiacol production), but the bacteria do not cause swelling of the package or discoloration of the product,[4] nor is it pathogenic to humans.[5] Alicyclobacilli have been implicated in spoilages of pear, orange, peach, mango, and white grape juice, fruit juice blends, and tomato products.[6] Not all Alicyclobacilli produce guaiacol, and thus not all species are of spoilage concern.[7] A. consociatus and A. pohliae were originally classified in genus Alicyclobacillus, but were later reclassified into the novel genus Effusibacillus in 2014.[8]

Most Alicyclobacillus species optimally grow in the 40-55 °C range.[9] The exceptions include A. acidocaldarius (65 °C),[9] A. aeris (30 °C),[10] A. disulfidooxidans (35 °C),[11][12] and A. ferrooxydans (28 °C).[13] A. acidocaldarius is the most thermotolerant, as is able to grow in temperatures up to 70 °C.[9] A. disulfidooxidans is the only psychrotroph, being able to grow at 4 °C.[11][12] Most species can grow in the pH 2.0-6.0 range, and none have been shown to grow above pH 6.5.[9] A. disulfidooxidans is the most acid-tolerant, and can grow at pH 0.5.[11][12]

Background

The first Alicyclobacillus species was isolated in 1967 from hot springs, and was named Bacillus acidocaldarius. However, it was not until 1982 that the organisms were implicated in the spoilage of apple juice. The next outbreak occurred in 1994, and based on 16S rRNA studies, a separate genus was proposed.[4] The genus name derives from ω-alicyclic fatty acids as the major component in the cellular membrane, and to reflect the previous classification as Bacillus.[9] A. acidoterrestris is considered the most important spoilage species within the genus Alicyclobacillus,[14] but A. acidocaldarius, A. pomorum, and A. herbarius have also been isolated from spoiled product.[15] Soil is a common habitat for species of Alicyclobacillus, and is likely the source for contamination of food products.[9]

Impact

The canning industry works under the assumption that bacterial spores will not germinate at pH values below 4.6, and that acid-tolerant organisms are not very heat resistant. In this case, a low heat pasteurization process is applicable. However, the emergence of Alicyclobacillus as a spoilage organism has led some researchers to advocate using A. acidoterrestris as the reference organism to design pasteurization processes for high acid foods, just as the thermal death time of Clostridium botulinum was used to design the sterilization process for low acid canned foods.[16] High-pressure processing has been shown to be effective at inactivating A. acidoterrestris spores in orange juice.[17] One survey of 8556 samples of fruit and vegetable juices found Alicyclobacillus in 13% of samples,[18] while another study found Alicyclobacillus in 6% out of 180 samples,[19] and another found the bacteria in 14% out of 75 samples.[4]

In The Netherlands in 2013, contamination of raspberry with Alicyclobacillus in pasteurized juices led to a public recall after consumers complained about bad taste and odor.[20]

References
  1. Parte, A.C. "Alicyclobacillus". LPSN.
  2. Chang, Su-Sen; Kang, Dong-Hyun (29 September 2008). "Alicyclobacillus spp. in the Fruit Juice Industry: History, Characteristics, and Current Isolation/Detection Procedures". Critical Reviews in Microbiology. 30 (2): 55–74. doi:10.1080/10408410490435089. PMID 15239380.
  3. Alicyclobacillus, the Beverage Industry and the BioSys Rapid Microbiology. Retrieved 2010-12-22
  4. Eiroa, M. E. U.; Junqueira, V. C. A.; Schmidt, F. L. (August 1999). "Alicyclobacillus in Orange Juice: Occurrence and Heat Resistance of Spores". Journal of Food Protection. 62 (8): 883–886. doi:10.4315/0362-028X-62.8.883. PMID 10456741.
  5. Silva, Filipa V.M; Gibbs, Paul (February 2001). "Alicyclobacillus acidoterrestris spores in fruit products and design of pasteurization processes". Trends in Food Science & Technology. 12 (2): 68–74. doi:10.1016/S0924-2244(01)00070-X.
  6. Groenewald, W; Gouws, P; Witthuhn, R (February 2009). "Isolation, identification and typification of Alicyclobacillus acidoterrestris and Alicyclobacillus acidocaldarius strains from orchard soil and the fruit processing environment in South Africa". Food Microbiology. 26 (1): 71–76. doi:10.1016/j.fm.2008.07.008. PMID 19028308.
  7. Chang, S.S.; Park, S.H.; Kang, D.H. (June 2013). "Development of novel agar media for isolating guaiacol producing Alicyclobacillus spp". International Journal of Food Microbiology. 164 (1): 1–6. doi:10.1016/j.ijfoodmicro.2013.03.015. PMID 23587706.
  8. Watanabe, M.; Kojima, H.; Fukui, M. (23 May 2014). "Proposal of Effusibacillus lacus gen. nov., sp. nov., and reclassification of Alicyclobacillus pohliae as Effusibacillus pohliae comb. nov. and Alicyclobacillus consociatus as Effusibacillus consociatus comb. nov". International Journal of Systematic and Evolutionary Microbiology. 64 (Pt 8): 2770–2774. doi:10.1099/ijs.0.055814-0. PMID 24860109. S2CID 45473585.
  9. Pornpukdeewattana, Soisuda; Jindaprasert, Aphacha; Massa, Salvatore (7 February 2019). "Alicyclobacillus spoilage and control - a review". Critical Reviews in Food Science and Nutrition. 60 (1): 108–122. doi:10.1080/10408398.2018.1516190. PMID 30729793.
  10. Guo, X; You, X.-Y; Liu, L.-J; Zhang, J.-Y; Liu, S.-J; Jiang, C.-Y (2009). "Alicyclobacillus aeris sp. nov., a novel ferrous- and sulfur-oxidizing bacterium isolated from a copper mine". International Journal of Systematic and Evolutionary Microbiology. 59 (10): 2415–2420. doi:10.1099/ijs.0.008870-0. PMID 19622665.
  11. Dufresne, S; Bousquet, J; Boissinot, M; Guay, R (1996). "Sulfobacillus disulfidooxidans sp. nov., a New Acidophilic, Disulfide-Oxidizing, Gram-Positive, Spore-Forming Bacterium". International Journal of Systematic Bacteriology. 46 (4): 1056–1064. doi:10.1099/00207713-46-4-1056. PMID 8863435.
  12. Karavaiko, G. I (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 (2): 941–947. doi:10.1099/ijs.0.63300-0. PMID 15774689.
  13. Jiang, C.-Y; Liu, Y; Liu, Y.-Y; You, X.-Y; Guo, X; Liu, S.-J (2008). "Alicyclobacillus ferrooxydans sp. nov., a ferrous-oxidizing bacterium from solfataric soil". International Journal of Systematic and Evolutionary Microbiology. 58 (12): 2898–2903. doi:10.1099/ijs.0.2008/000562-0. PMID 19060079.
  14. Spinelli, A. C. N. F.; Sant'Ana, A. S.; Rodrigues-Junior, S.; Massaguer, P. R. (2 October 2009). "Influence of Different Filling, Cooling, and Storage Conditions on the Growth of Alicyclobacillus acidoterrestris CRA7152 in Orange Juice". Applied and Environmental Microbiology. 75 (23): 7409–7416. doi:10.1128/AEM.01400-09. PMC 2786409. PMID 19801469.
  15. McKnight, I.C.; Eiroa, M.N.U.; Sant’Ana, A.S.; Massaguer, P.R. (December 2010). "Alicyclobacillus acidoterrestris in pasteurized exotic Brazilian fruit juices: Isolation, genotypic characterization and heat resistance". Food Microbiology. 27 (8): 1016–1022. doi:10.1016/j.fm.2010.06.010. PMID 20832679.
  16. Silva, F. V. M.; Gibbs, P. (10 August 2010). "Target Selection in Designing Pasteurization Processes for Shelf-Stable High-Acid Fruit Products". Critical Reviews in Food Science and Nutrition. 44 (5): 353–360. doi:10.1080/10408690490489251. PMID 15540648.
  17. Silva, Filipa V.M.; Tan, Eng Keat; Farid, Mohammed (October 2012). "Bacterial spore inactivation at 45–65 °C using high pressure processing: Study of Alicyclobacillus acidoterrestris in orange juice". Food Microbiology. 32 (1): 206–211. doi:10.1016/j.fm.2012.04.019. PMID 22850395.
  18. Oteiza, Juan Martìn; Ares, Gastón; Sant'Ana, Anderson S.; Soto, Silvina; Giannuzzi, Leda (December 2011). "Use of a multivariate approach to assess the incidence of Alicyclobacillus spp. in concentrate fruit juices marketed in Argentina: Results of a 14-year survey". International Journal of Food Microbiology. 151 (2): 229–234. doi:10.1016/j.ijfoodmicro.2011.09.004. PMID 21962940.
  19. Danyluk, Michelle D.; Friedrich, Loretta M.; Jouquand, Celine; Goodrich-Schneider, Renee; Parish, Mickey E.; Rouseff, Russell (May 2011). "Prevalence, concentration, spoilage, and mitigation of Alicyclobacillus spp. in tropical and subtropical fruit juice concentrates". Food Microbiology. 28 (3): 472–477. doi:10.1016/j.fm.2010.10.008. PMID 21356453.
  20. Graanoogst, Audrey. (2013-09-19) Contaminated fruit juice Wicky recalled. NLTimes.nl. Retrieved 2014-05-03.
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