Daqu fermentation selects for heat-resistant Enterobacteriaceae and bacilli

Applied and Environmental Microbiology

Volumn 84, Issue 21, 2018, Pages

  Wang, Zhiying ^a   Li, Pan ^b,c   Luo, Lixin ^c   Simpson, David J ^a   Gänzle, Michael G ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^c SOUTH CHINA UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

Bacillus; Cronobacter; Daqu; Heat resistance; Locus of heat resistance; SpoVA2mob operon

Indexed keywords

BACILLI; BACTERIOLOGY; FERMENTATION; ORGANIC POLYMERS; POLYMERASE CHAIN REACTION; RNA; SACCHARIFICATION; SPECIFIC HEAT;

BACILLUS AMYLOLIQUEFACIENS; BACILLUS LICHENIFORMIS; CRONOBACTER; DAQU; SOLID-STATE FERMENTATION; SPONTANEOUS FERMENTATION; SPOVA2MOB OPERON; TEMPERATURE PROFILES;

HEAT RESISTANCE;

ANTIMICROBIAL ACTIVITY; BACTERIUM; CEREAL; CHEMICAL REACTION; DNA; FERMENTATION; GENE; GENE EXPRESSION; GENETIC ANALYSIS; HEATING; MICROBIAL ACTIVITY; PROTEIN; SPORE; TEMPERATURE EFFECT;

AVENA; BACILLI (CLASS); BACILLUS (BACTERIUM); BACILLUS AMYLOLIQUEFACIENS; BACILLUS LICHENIFORMIS; BACILLUS SUBTILIS; BACILLUS VELEZENSIS; BACTERIA (MICROORGANISMS); BREVIBACILLUS PARABREVIS; ENTEROBACTERIACEAE;

BACILLUS; BACTERIAL SPORE; CHEMISTRY; CLASSIFICATION; ENTEROBACTERIACEAE; FERMENTATION; FOOD CONTROL; GENETICS; GENOMIC ISLAND; HEAT; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; OPERON; WINE;

BACILLUS; ENTEROBACTERIACEAE; FERMENTATION; FOOD MICROBIOLOGY; GENOMIC ISLANDS; HOT TEMPERATURE; OPERON; SPORES, BACTERIAL; WINE;

EID: 85055073319     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01483-18     Document Type: Article

References (45)

1. Doyle MP, Buchanan RL (ed). 2012. Food microbiology: fundamentals and frontiers. ASM Press, Washington, DC
2. Liu Y, Gill A, McMullen L, Gänzle MG. 2015. Variation in heat and pressure resistance of verotoxigenic and nontoxigenic Escherichia coli. J Food Prot 78:111-120. https://doi.org/10.4315/0362-028X.JFP-14-267
3. Esty J, Meyer K. 1922. The heat resistance of the spores of B. botulinus and allied anaerobes. XI. J Infect Dis 36:650-664. https://doi.org/10 .1093/infdis/31.6.650
4. Dlusskaya E, McMullen L, Gänzle M. 2011. Characterization of an extremely heat-resistant Escherichia coli obtained from a beef processing facility. J Appl Microbiol 110:840-849. https://doi.org/10.1111/j.1365-2672.2011.04943.x
5. Margosch D, Ehrmann MA, Buckow R, Heinz V, Vogel RF, Gänzle MG. 2006. High-pressure-mediated survival of Clostridium botulinum and Bacillus amyloliquefaciens endospores at high temperature. Appl Environ Microbiol 72: 3476-3481. https://doi.org/10.1128/AEM.72.5.3476-3481.2006
6. Berendsen EM, Boekhorst J, Kuipers OP, Wells-Bennik MH. 2016. A mobile genetic element profoundly increases heat resistance of bacterial spores. ISME J 10:2633-2642. https://doi.org/10.1038/ismej.2016.59
7. Mercer RG, Zheng J, Garcia-Hernandez R, Ruan L, Gänzle MG, McMullen LM. 2015. Genetic determinants of heat resistance in Escherichia coli. Front Microbiol 6:932. https://doi.org/10.3389/fmicb.2015.00932
8. Berendsen EM, Koning RA, Boekhorst J, de Jong A, Kuipers OP, Wells-Bennik MH. 2016. High-level heat resistance of spores of Bacillus amyloliquefaciens and Bacillus licheniformis results from the presence of a spoVA operon in a Tn1546 transposon. Front Microbiol 7:1912. https:// doi.org/10.3389/fmicb.2016.01912
9. Krawczyk AO, Berendsen EM, de Jong A, Boekhorst J, Wells-Bennik MH, Kuipers OP, Eijlander RT. 2016. A transposon present in specific strains of Bacillus subtilis negatively affects nutrient-and dodecylamine-induced spore germination. Environ Microbiol 18:4830-4846. https://doi.org/10 .1111/1462-2920.13386
10. Kort R, O'Brien AC, Van Stokkum IH, Oomes SJ, Crielaard W, Hellingwerf KJ, Brul S. 2005. Assessment of heat resistance of bacterial spores from food product isolates by fluorescence monitoring of dipicolinic acid release. Appl Environ Microbiol 71:3556-3564. https://doi.org/10.1128/ AEM.71.7.3556-3564.2005
11. Tovar-Rojo F, Chander M, Setlow B, Setlow P. 2002. The products of the spoVA operon are involved in dipicolinic acid uptake into developing spores of Bacillus subtilis. J Bacteriol 184:584-587. https://doi.org/10 .1128/JB.184.2.584-587.2002
12. Mercer RG, Walker BD, Yang X, McMullen LM, Gänzle MG. 2017. The locus of heat resistance (LHR) mediates heat resistance in Salmonella enterica, Escherichia coli and Enterobacter cloacae. Food Microbiol 64:96-103. https://doi.org/10.1016/j.fm.2016.12.018
13. Li H, Gänzle M. 2016. Some like it hot: heat resistance of Escherichia coli in food. Front Microbiol 7:1763. https://doi.org/10.3389/fmicb .2016.01763
14. Mercer R, Nguyen O, Ou Q, McMullen L, Gänzle MG. 2017. Functional analysis of genes comprising the locus of heat resistance in Escherichia coli. Appl Environ Microbiol 83:e01400-17. https://doi.org/10.1128/AEM .01400-17
15. Lee C, Franke KB, Kamal SM, Kim H, Lünsdorf H, Jäger J, Nimtz M, Trček J, Jänsch L, Bukau B. 2018. Stand-alone ClpG disaggregase confers superior heat tolerance to bacteria. Proc Natl Acad Sci U S A 115: E273-E282. https://doi.org/10.1073/pnas.1712051115
16. Sadiq FA, Li Y, Liu T, Flint S, Zhang G, Yuan L, Pei Z, He G. 2016. The heat resistance and spoilage potential of aerobic mesophilic and thermophilic spore forming bacteria isolated from Chinese milk powders. Int J Food Microbiol 238:193-201. https://doi.org/10.1016/j.ijfoodmicro.2016 .09.009
17. Zhi S, Banting G, Li Q, Edge TA, Topp E, Sokurenko M, Scott C, Braithwaite S, Ruecker NJ, Yasui Y. 2016. Evidence of naturalized stress-tolerant strains of Escherichia coli in municipal wastewater treatment plants. Appl Environ Microbiol 82:5505-5518. https://doi.org/10.1128/AEM.00143-16
18. Ma A, Chui L. 2017. Identification of heat resistant Escherichia coli by qPCR for the locus of heat resistance. J Microbiol Methods 133:87-89. https://doi.org/10.1016/j.mimet.2016.12.019
19. Xiu L, Kunliang G, Hongxun Z. 2012. Determination of microbial diversity in Daqu, a fermentation starter culture of Maotai liquor, using nested PCR-denaturing gradient gel electrophoresis. World J Microbiol Biotechnol 28:2375-2381. https://doi.org/10.1007/s11274-012-1045-y
20. Li P, Lin W, Liu X, Wang X, Luo L. 2016. Environmental factors affecting microbiota dynamics during traditional solid-state fermentation of Chinese Daqu starter. Front Microbiol 7:1237. https://doi.org/10.3389/fmicb .2016.01237
21. Xiao C, Lu ZM, Zhang XJ, Wang ST, Ao L, Shen CH, Shi JS, Xu ZH. 2017. Bio-heat is a key environmental driver shaping the microbial community of medium-temperature Daqu. Appl Environ Microbiol, 83:e01550-17. https://doi.org/10.1128/AEM.01550-17
22. Wang HY, Gao YB, Fan QW, Xu Y. 2011. Characterization and comparison of microbial community of different typical Chinese liquor Daqus by PCR-DGGE. Lett Appl Microbiol 53:134-140. https://doi.org/10.1111/j .1472-765X.2011.03076.x
23. Krawczyk AO, de Jong A, Omony J, Holsappel S, Wells-Bennik MH, Kuipers OP, Eijlander RT. 2017. Spore heat activation requirements and germination responses correlate with sequences of germinant receptors and with the presence of a specific spoVA2mob operon in foodborne strains of Bacillus subtilis. Appl Environ Microbiol 83:e03122-16. https:// doi.org/10.1128/AEM.03122-16
24. Nazarowec-White M, Farber JM. 1997. Thermal resistance of Enterobacter sakazakii in reconstituted dried-infant formula. Lett Appl Microbiol 24: 9-13. https://doi.org/10.1046/j.1472-765X.1997.00328.x
25. Yan Q, Fanning S. 2015. Strategies for the identification and tracking of Cronobacter species: an opportunistic pathogen of concern to neonatal health. Front Pediatr 3:38. https://doi.org/10.3389/fped.2015.00038
26. Tall BD, Gangiredla J, Gopinath GR, Yan Q, Chase HR, Lee B, Hwang S, Trach L, Park E, Yoo Y, Chung T. 2015. Development of a customdesigned, pan genomic DNA microarray to characterize strain-level diversity among Cronobacter spp. Front Pediatr 3:36. https://doi.org/10 .3389/fped.2015.00036
27. Li P, Aflakpui FWK, Yu H, Luo L, Lin WT. 2015. Characterization of activity and microbial diversity of typical types of Daqu for traditional Chinese vinegar. Ann Microbiol 65:2019-2027. https://doi.org/10.1007/s13213-015-1040-2
28. Li P, Liang H, Lin WT, Feng F, Luo L. 2015. Microbiota dynamics associated with environmental conditions and potential roles of cellulolytic communities in traditional Chinese cereal starter solid-state fermentation. Appl Environ Microbiol 81:5144-5156. https://doi.org/10.1128/AEM .01325-15
29. Jaradat ZW, Al Mousa W, Elbetieha A, Al Nabulsi A, Tall BD. 2014. Cronobacter spp.-opportunistic food-borne pathogens. A review of their virulence and environmental-adaptive traits. J Med Microbiol 63: 1023-1037
30. Mardaneh J, Soltan-Dallal MM. 2014. Isolation and identification of E. cowanii from powdered infant formula in NICU and determination of antimicrobial susceptibility of isolates. Iran J Pediatr 24:261
31. Marti R, Muniesa M, Schmid M, Ahrens CH, Naskova J, Hummerjohann J. 2016. Heat-resistant Escherichia coli as potential persistent reservoir of extended-spectrum β-lactamases and Shiga toxin-encoding phages in dairy. J Dairy Sci 99:8622-8632. https://doi.org/10.3168/jds.2016-11076
32. Feeney A, Johnston CD, Govender R, O'Mahony J, Coffey A, Sleator RD. 2014. Analysis of the role of the Cronobacter sakazakii ProP homologues in osmotolerance. Gut Pathog 6:15. https://doi.org/10 .1186/1757-4749-6-15
33. Breeuwer P. 2014. Adaptation of pathogenic microorganisms to dry conditions: the microbiological safety of low water activity foods and spices, p 37-48. In Gurtler JB, Doyle MP, Kornacki JL (ed), Food microbiology and food safety. Springer, New York, NY
34. Pleitner A, Zhai Y, Winter R, Ruan L, McMullen LM, Gänzle MG. 2012. Compatible solutes contribute to heat resistance and ribosome stability in Escherichia coli AW1.7. Biochim Biophys Acta 1824:1351-1357. https:// doi.org/10.1016/j.bbapap.2012.07.007
35. Bond WW, Favero MS. 1977. Bacillus xerothermodurans sp. nov., a species forming endospores extremely resistant to dry heat. Int J Syst Bacteriol 27:157-160
36. Liang H, Zhang C, Shao C, Peng X, Liang L, Su J, Li C. 2015. A DGGE marker-mediated fast monitoring of bacterial diversity and comprehensive identification of high-temperature Daqu starter. J Food Sci 80: 1519-1525. https://doi.org/10.1111/1750-3841.13144
37. den Besten HM, Berendsen EM, Wells-Bennik MH, Straatsma H, Zwietering MH. 2017. Two complementary approaches to quantify variability in heat resistance of spores of Bacillus subtilis. Int J Food Microbiol 253: 48-53. https://doi.org/10.1016/j.ijfoodmicro.2017.04.014
38. Esteban MD, Conesa R, Huertas JP, Palop A. 2015. Effect of thymol in heating and recovery media on the isothermal and non-isothermal heat resistance of Bacillus spores. Food Microbiol 48:35-40. https://doi.org/ 10.1016/j.fm.2014.11.016
39. Berendsen EM, Zwietering MH, Kuipers OP, Wells-Bennik MH. 2015. Two distinct groups within the Bacillus subtilis group display significantly different spore heat resistance properties. Food Microbiol 45:18-25. https://doi.org/10.1016/j.fm.2014.04.009
40. Weibull W. 1951. A statistical distribution function of wide applicability. J Appl Mech 18:293-297
41. Peleg M, Cole M. 2000. Estimating the survival of Clostridium botulinum spores during heat treatments. J Food Prot 63:190-195. https://doi.org/ 10.4315/0362-028X-63.2.190
42. Mathys A, Heinz V, Schwartz FH, Knorr D. 2007. Impact of agglomeration on the quantitative assessment of Bacillus stearothermophilus heat inactivation. J Food Eng 81:380-387. https://doi.org/10.1016/j .jfoodeng.2006.11.012
43. Gänzle MG. 2015. Lactic metabolism revisited: metabolism of lactic acid bacteria in food fermentations and food spoilage. Curr Opin Food Sci 2:106-117. https://doi.org/10.1016/j.cofs.2015.03.001
44. Eden PA, Schmidt TM, Blakemore RP, Pace NR. 1991. Phylogenetic analysis of Aquaspirillum magnetotacticum using polymerase chain reaction-amplified 16S rRNA-specific DNA. Int J Syst Bacteriol 41: 324-325
45. Mafart P, Couvert O, Gaillard S, Leguérinel I. 2002. On calculating sterility in thermal preservation methods: application of the Weibull frequency distribution model. Int J Food Microbiol 72:107-113. https://doi.org/10 .1016/S0168-1605(01)00624-9