Research Progress on Formation, Germination and Control Methods of Bacterial Spores

ZHANG Dongchun; ZHANG Yajuan; SUN Ying; SI Haishan; KANG Yapeng; MA Mengge; WANG Zhixin; NING Yawei

doi:10.13386/j.issn1002-0306.2022110020

Volume 44 Issue 15

Jul. 2023

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Science and Technology of Food Industry > 2023 > 44(15): 463-473. > DOI: 10.13386/j.issn1002-0306.2022110020

ZHANG Dongchun, ZHANG Yajuan, SUN Ying, et al. Research Progress on Formation, Germination and Control Methods of Bacterial Spores[J]. Science and Technology of Food Industry, 2023, 44(15): 463−473. (in Chinese with English abstract). doi: 10.13386/j.issn1002-0306.2022110020.

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Research Progress on Formation, Germination and Control Methods of Bacterial Spores

College of Food Science and Biology, Hebei University of Science and Technology, Shijiazhuang 050000, China

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Received Date: November 01, 2022
Available Online: June 05, 2023

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Abstract

Abstract

Bacterial spores are extremely resistant to various processing techniques attributable to its special structure and physiological processes, and often lead to the spoilage of thermally sterilized food. Therefore, it is of great significance to inactivate spores or control spore germination in the food industry. This review summarizes the structure and the sporulation regulation mechanism in the formation process of bacterial spores, germination process and the factors of spore germination; then reviews the effects and mechanisms of action of some physical technologies (i.e., heat treatment, ultrasonic treatment, high pressure treatment and plasma treatment), chemical technologies (i.e., surfactants and chemical preservatives) and natural bio-antibacterial agents individually or in combination with other treatments against spore. This review is expected to provide reference for the development of safer and more efficient control technology of bacterial spores.
- bacterial spores,
- formation process,
- germination,
- control technologies

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References

[1]	SETLOW P, CHRISTIE G. Bacterial spore mRNA-What's up with that?[J]. Frontiers in Microbiology,2020,11:596092. doi: 10.3389/fmicb.2020.596092
[2]	MARTLBAUER E, GRANUM P E. Bacillus cereus toxins[J]. Toxins,2021,13(5):295−295. doi: 10.3390/toxins13050295
[3]	PAREDES-SABJA D, SHEN A, SORG J A. Clostridium difficile spore biology: Sporulation, germination, and spore structural proteins[J]. Trends in Microbiology,2014,22(7):406−416. doi: 10.1016/j.tim.2014.04.003
[4]	SWARGE B, NAFID C, VISCHER N, et al. Investigating synthesis of the MalS malic enzyme during Bacillus subtilis spore germination and outgrowth and the influence of spore maturation and sporulation conditions[J]. mSphere,2020,5(4):e00464−20.
[5]	LOPEZ-GARRIDO J, OJKIC N, KHANNA K, et al. Chromosome translocation inflates Bacillus forespores and impacts cellular morphology[J]. Cell,2018,172(4):758−770. doi: 10.1016/j.cell.2018.01.027
[6]	SHEN A, EDWARDS A N, SARKER M R, et al. Sporulation and germination in clostridial pathogens[J]. Microbiology Spectrum, 2019, 7(6): 10.
[7]	GAUVRY E, MATHOT A-G, COUVERT O, et al. Differentiation of vegetative cells into spores: A kinetic model applied to Bacillus subtilis[J]. Applied and Environmental Microbiology,2019,85(10):e00322−19.
[8]	SøGAARD-ANDERSEN L, MEARLS E B, JACKTER J, et al. Transcription and translation of the sigG gene is tuned for proper execution of the switch from early to late gene expression in the developing Bacillus subtilis spore[J]. PLOS Genetics,2018,14(4):e1007350. doi: 10.1371/journal.pgen.1007350
[9]	WANG S T, SETLOW B, CONLON E M, et al. The forespore line of gene expression in Bacillus subtilis[J]. Journal of Molecular Biology,2006,358(1):16−37. doi: 10.1016/j.jmb.2006.01.059
[10]	KEARNS D B, RAMÍREZ-GUADIANA F H, MEESKE A J, et al. A two-step transport pathway allows the mother cell to nurture the developing spore in Bacillus subtilis[J]. PLOS Genetics,2017,13(9):e1007015. doi: 10.1371/journal.pgen.1007015
[11]	RILEY E P, TRINQUIER A, REILLY M L, et al. Spatiotemporally regulated proteolysis to dissect the role of vegetative proteins during Bacillus subtilis sporulation: Cell-specific requirement of σH and σA[J]. Molecular Microbiology,2018,108(1):45−62. doi: 10.1111/mmi.13916
[12]	SAUJET L, PEREIRA F C, HENRIQUES A O, et al. The regulatory network controlling spore formation in Clostridium difficile[J]. FEMS Microbiology Letters,2014,358(1):1−10. doi: 10.1111/1574-6968.12540
[13]	SWARGE B, ABHYANKAR W, JONKER M, et al. Integrative analysis of proteome and transcriptome dynamics during Bacillus subtilis spore revival[J]. Msphere,2020,5(4):e00463−20.
[14]	WANG Y, DE BOER R, VISCHER N, et al. Visualization of germination proteins in putative Bacillus cereus germinosomes[J]. International Journal of Molecular Sciences, 2020, 21(15): 5198.
[15]	GUPTA S, üSTOK F I, JOHNSON C L, et al. Investigating the functional hierarchy of Bacillus megaterium PV361 spore germinant receptors[J]. Journal of Bacteriology,2013,195(13):3045−3053. doi: 10.1128/JB.00325-13
[16]	SHRESTHA R, SORG J A. Hierarchical recognition of amino acid co-germinants during Clostridioides difficile spore germination[J]. Anaerobe,2018,49:41−47. doi: 10.1016/j.anaerobe.2017.12.001
[17]	RAO L, FEEHERRY F E, GHOSH S, et al. Effects of lowering water activity by various humectants on germination of spores of Bacillus species with different germinants[J]. Food Microbiology,2018,72:112−127. doi: 10.1016/j.fm.2017.11.012
[18]	LIANG D, WANG X, WU X, et al. The effect of high pressure combined with moderate temperature and peptidoglycan fragments on spore inactivation[J]. Food Research International,2021,148:110615. doi: 10.1016/j.foodres.2021.110615
[19]	朱瑶迪, 张佳烨, 李苗云, 等. 不同肽聚糖对肉制品中产气荚膜梭菌芽孢萌发率影响及其定量预测[J]. 农业工程学报,2020,36(4):287−293. [ZHU Yaodi, ZHANG Jiaye, LI Miaoyun, et al. Effect of different peptidoglycan on Clostridium perfringens spores germination and quantitative prediction[J]. Transactions of the Chinese Society of Agricultural Engineering,2020,36(4):287−293. doi: 10.11975/j.issn.1002-6819.2020.04.034 ZHU Yaodi, ZHANG Jiaye, LI Miaoyun, et al. Effect of different peptidoglycan on Clostridium perfringens spores germination and quantitative prediction[J]. Transactions of the Chinese Society of Agricultural Engineering, 2020, 36(4): 287-293. doi: 10.11975/j.issn.1002-6819.2020.04.034
[20]	YAMAMOTO K. Food processing by high hydrostatic pressure[J]. Bioscience, Biotechnology, and Biochemistry,2017,81(4):672−679. doi: 10.1080/09168451.2017.1281723
[21]	SONI A, OEY I, SILCOCK P, et al. Impact of temperature, nutrients, pH and cold storage on the germination, growth and resistance of Bacillus cereus spores in egg white[J]. Food Research International,2018,106:394−403. doi: 10.1016/j.foodres.2018.01.006
[22]	徐茜茜. 酸土脂环酸芽孢杆菌 (Alicyclobacillus acidoterrestris) 芽孢形成及低pH条件下芽孢萌发的蛋白组学研究[D]. 新乡: 河南科技学院, 2017 XU Xixi. Study on spore formation and proteomics of spore germination atlow pH in Alicyclobacillus acidoterrestris[D]. Xinxiang: Henan Institute of Science and Technology, 2017.
[23]	SETLOW P. Spores of Bacillus subtilis: Their resistance to and killing by radiation, heat and chemicals[J]. Journal of Applied Microbiology,2006,101(3):514−525. doi: 10.1111/j.1365-2672.2005.02736.x
[24]	ROZALI S N, MILANI E A, DEED R C, et al. Bacteria, mould and yeast spore inactivation studies by scanning electron microscope observations[J]. International Journal of Food Microbiology,2017,263:17−25. doi: 10.1016/j.ijfoodmicro.2017.10.008
[25]	SCHOTTROFF F, PYATKOVSKYY T, REINEKE K, et al. Mechanisms of enhanced bacterial endospore inactivation during sterilization by ohmic heating[J]. Bioelectrochemistry,2019,130:107338. doi: 10.1016/j.bioelechem.2019.107338
[26]	JUNEJA V K, OSORIA M, HWANG C A, et al. Thermal inactivation of Bacillus cereus spores during cooking of rice to ensure later safety of boudin[J]. Lwt,2020,122:108955. doi: 10.1016/j.lwt.2019.108955
[27]	CONDÓN-ABANTO S, ARROYO C, áLVAREZ I, et al. Application of ultrasound in combination with heat and pressure for the inactivation of spore forming bacteria isolated from edible crab (Cancer pagurus)[J]. International Journal of Food Microbiology,2016,223:9−16. doi: 10.1016/j.ijfoodmicro.2016.02.001
[28]	ANSARI J A, ISMAIL M, FARID M. Investigation of the use of ultrasonication followed by heat for spore inactivation[J]. Food and Bioproducts Processing,2017,104:32−39. doi: 10.1016/j.fbp.2017.04.005
[29]	BUHR T L, MINTER Z A, KENNIHAN N L, et al. Combining spore germination and heat inactivation to decontaminate materials contaminated with Bacillus anthracis spores[J]. Journal of Applied Microbiology,2020,128(1):124−137. doi: 10.1111/jam.14474
[30]	李素, 张顺亮, 任双, 等. 芽孢诱导技术在中温香肠加工中的应用[J]. 肉类研究,2017,31(12):6−10. [LI Su, ZHANG Shunliang, REN Shuang, et al. Application of spore induction technology in the processing of medium temperature sausage[J]. Meat Research,2017,31(12):6−10. LI Su, ZHANG Shunliang, REN Shuang, et al. Application of spore induction technology in the processing of medium temperature sausage[J]. Meat Research, 2017, 31(12): 6-10.
[31]	FAN L, ISMAIL B B, HOU F, et al. Thermosonication damages the inner membrane of Bacillus subtilis spores and impels their inactivation[J]. Food Research International,2019,125:108514. doi: 10.1016/j.foodres.2019.108514
[32]	FAN L, ISMAIL B B, HOU F, et al. Thermosonication pretreatment enhances the killing of germinated Bacillus spores adhered to stainless steel surface[J]. Lwt,2021,136:110248. doi: 10.1016/j.lwt.2020.110248
[33]	WANG L, XIA Q, LI Y. Label free-based proteomic analysis of proteins in Bacillus cereus spores regulated by high pressure processing and slightly acidic electrolyzed water treatment[J]. Food Control,2018,90:392−400. doi: 10.1016/j.foodcont.2018.03.015
[34]	孙静, 张津瑜, 胡小松, 等. 超高压导致芽孢亚致死损伤进而提高芽孢热敏感性[J]. 食品科技,2017(10):313−317. [SUN Jing, ZHANG Jinyu, HU Xiaosong, et al. Ultrahigh pressure processing enhances spore thermal sensitivity by causing sub-lethal damage to spores[J]. Food Science and Technology,2017(10):313−317. doi: 10.13684/j.cnki.spkj.2017.10.059 SUN Jing, ZHANG Jinyu, HU Xiaosong, et al. Ultrahigh pressure processing enhances spore thermal sensitivity by causing sub-lethal damage to spores[J]. Food Science and Technology, 2017, (10): 313-317. doi: 10.13684/j.cnki.spkj.2017.10.059
[35]	LIAO X, MUHAMMAD A I, CHEN S, et al. Bacterial spore inactivation induced by cold plasma[J]. Critical Reviews in Food Science and Nutrition,2019,59(16):2562−2572. doi: 10.1080/10408398.2018.1460797
[36]	LIAO X, BAI Y, MUHAMMAD A I, et al. The application of plasma-activated water combined with mild heat for the decontamination of Bacillus cereus spores in rice (Oryza sativa L. ssp. japonica)[J]. Journal of Physics D:Applied Physics,2019,53(6):064003.
[37]	SILVA D R G, HADDAD G B S, DE MOURA A P, et al. Safe cured meat using gamma radiation: Effects on spores of Clostridium sporogenes and technological and sensorial characteristics of low nitrite cooked ham[J]. Lwt,2021,137:110392. doi: 10.1016/j.lwt.2020.110392
[38]	KANG J W, HONG H N, KANG D H. Application of a krypton-chlorine excilamp to control Alicyclobacillus acidoterrestris spores in apple juice and identification of its sporicidal mechanism[J]. Applied and Environmental Microbiology,2020,86(11):e00159−20.
[39]	TAYLOR W, CAMILLERI E, CRAFT D L, et al. DNA damage kills bacterial spores and cells exposed to 222-Nanometer UV radiation[J]. Applied and Environmental Microbiology,2020,86(8):e03039−19.
[40]	TREMARIN A, BRANDãO T R S, SILVA C L M. Application of ultraviolet radiation and ultrasound treatments for Alicyclobacillus acidoterrestris spores inactivation in apple juice[J]. LWT-Food Science and Technology,2017,78:138−142. doi: 10.1016/j.lwt.2016.12.039
[41]	CLAIR G, ESBELIN J, MALLEA S, et al. The spore coat is essential for Bacillus subtilis spore resistance to pulsed light, and pulsed light treatment eliminates some spore coat proteins[J]. International Journal of Food Microbiology,2020,323:108592. doi: 10.1016/j.ijfoodmicro.2020.108592
[42]	SONI A, OEY I, SILCOCK P, et al. Effect of pulsed electric field with moderate heat (80 ℃) on inactivation, thermal resistance and differential gene expression in B. cereus spores[J]. Journal of Food Processing and Preservation,2020,44(7):e14503.
[43]	LUONG T S V, MOIR C, CHANDRY P S, et al. Combined high pressure and heat treatment effectively disintegrates spore membranes and inactivates Alicyclobacillus acidoterrestris spores in acidic fruit juice beverage[J]. Innovative Food Science & Emerging Technologies,2020,66:102523.
[44]	董鹏. 高压均质对细菌营养体与芽孢的杀菌效果及机制研究[D]. 北京: 中国农业大学, 2016 DONG Peng. Inactivation mechanisms of vegetative microorganisms and bacterial spores by high pressure homogenization[D]. Beijing: China Agricultural University, 2016.
[45]	刘月. HPTS结合溶菌酶灭活枯草杆菌芽孢的作用研究[D]. 银川: 宁夏大学, 2022 LIU Yue. Study on the combined effects of HPTS and lysozyme on the inactivation of Bacillus subtilis spores[D]. Yinchuan: Ningxia University, 2022.
[46]	RAO L, WANG Y, CHEN F, et al. High pressure CO₂ reduces the wet heat resistance of Bacillus subtilis spores by perturbing the inner membrane[J]. Innovative Food Science & Emerging Technologies,2020,60:102291.
[47]	EVELYN, SILVA F V M. Differences in the resistance of microbial spores to thermosonication, high pressure thermal processing and thermal treatment alone[J]. Journal of Food Engineering,2018,222:292−297. doi: 10.1016/j.jfoodeng.2017.11.037
[48]	MOKASHI S, KANAAN J, CRAFT D L, et al. Killing of bacterial spores by dodecylamine and its effects on spore inner membrane properties[J]. Journal of Applied Microbiology,2020,129(6):1511−1522. doi: 10.1111/jam.14732
[49]	DONG W, GREEN J, KORZA G, et al. Killing of spores of Bacillus species by cetyltrimethylammonium bromide[J]. Journal of Applied Microbiology,2019,126(5):1391−1401. doi: 10.1111/jam.14242
[50]	HIROKADO R, NOMA S, SOH N, et al. Inactivation of Bacillus subtilis spores by carbonation with glycerin fatty acid esters[J]. Food Science and Technology Research,2018,24(3):455−463. doi: 10.3136/fstr.24.455
[51]	VELUGOTI P R, KUMAR S, BOHRA L K, et al. Inhibition of germination and outgrowth of Clostridium perfringens spores by buffered calcium, potassium and sodium citrates in cured and non-cured injected pork during cooling[J]. Lwt,2020,123(C):109074.
[52]	CAYEMITTE P E, GERLIANI N, RAYMOND P, et al. Study of the impacts of electro-activated solutions of calcium lactate, calcium ascorbate and their equimolar mixture combined with moderate heat treatments on the spores of Bacillus cereus ATCC 14579 under model conditions and in fresh salmon[J]. International Journal of Food Microbiology,2021,358:109285. doi: 10.1016/j.ijfoodmicro.2021.109285
[53]	GHOSH S, JOSEPH G, KORZA G, et al. Effects of the microbicide ceragenin CSA-13 on and properties of Bacillus subtilis spores prepared on two very different media[J]. Journal of Applied Microbiology,2019,127(1):109−120. doi: 10.1111/jam.14300
[54]	SUDHAUS N, NAGENGAST H, PINA-PÉREZ M C, et al. Effectiveness of a peracetic acid-based disinfectant against spores of Bacillus cereus under different environmental conditions[J]. Food Control,2014,39:1−7. doi: 10.1016/j.foodcont.2013.09.063
[55]	章中, 杨宏伟, 胡济美, 等. 化学物质辅助超高压处理对枯草杆菌芽孢的作用[J]. 中国食品学报,2015,15(5):47−53. [ZHANG Zhong, YANG Hongwei, HU Jimei, et al. Effect of high pressure processing assisted with chemicals on the spores of Bacillus subtilis[J]. Journal of Chinese Institute of Food Science and Technology,2015,15(5):47−53. doi: 10.16429/j.1009-7848.2015.05.007 ZHANG Zhong, YANG Hongwei, HU Jimei, et al. Effect of high pressure processing assisted with chemicals on the spores of Bacillus subtilis[J]. Journal of Chinese Institute of Food Science and Technology, 2015, 15(05): 47-53. doi: 10.16429/j.1009-7848.2015.05.007
[56]	SETLOW B, KORZA G, BLATT K M, et al. Mechanism of Bacillus subtilis spore inactivation by and resistance to supercritical CO₂ plus peracetic acid[J]. Journal of Applied Microbiology,2016,120(1):57−69. doi: 10.1111/jam.12995
[57]	DONG W, LI S, CAMILLERI E, et al. Accumulation and release of rare earth ions by spores of Bacillus species and the location of these ions in spores[J]. Applied and Environmental Microbiology,2019,85(17):e00956−19.
[58]	DONG W, SETLOW P. Fluoride movement into and out of Bacillus spores and growing cells and effects of fluoride accumulation on spore properties[J]. Journal of Applied Microbiology,2019,126(2):503−515. doi: 10.1111/jam.14155
[59]	LÜ R, MUHAMMAD A I, ZOU M, et al. Hurdle enhancement of acidic electrolyzed water antimicrobial efficacy on Bacillus cereus spores using ultrasonication[J]. Applied Microbiology and Biotechnology,2020,104(10):4505−4513. doi: 10.1007/s00253-020-10393-6
[60]	FU Y, LIANG L, DENG S, et al. Novel spore lytic enzyme from a Bacillus phage leading to spore killing[J]. Enzyme and Microbial Technology,2020,142:109698. doi: 10.1016/j.enzmictec.2020.109698
[61]	ZHAO S, HAN J, BIE X, et al. Purification and characterization of Plantaricin JLA-9: A novel bacteriocin against Bacillus spp. produced by Lactobacillus plantarum JLA-9 from Suan-Tsai, a traditional Chinese fermented cabbage[J]. Journal of Agricultural and Food Chemistry,2016,64(13):2754−64. doi: 10.1021/acs.jafc.5b05717
[62]	CETIN-KARACA H, NEWMAN M C. Antimicrobial efficacy of phytochemicals against Bacillus cereus in reconstituted infant rice cereal[J]. Food Microbiology,2018,69:189−195. doi: 10.1016/j.fm.2017.08.011
[63]	MODUGNO C, KMIHA S, SIMONIN H, et al. High pressure sensitization of heat-resistant and pathogenic foodborne spores to nisin[J]. Food Microbiol,2019,84:103244. doi: 10.1016/j.fm.2019.103244
[64]	RAO L, WANG Y, CHEN F, et al. The synergistic effect of high pressure CO₂ and nisin on inactivation of Bacillus subtilis spores in aqueous solutions[J]. Frontiers in Microbiology,2016,7:1507.
[65]	CHO W I, CHUNG M S. Antimicrobial effect of a combination of herb extract and organic acid against Bacillus subtilis spores[J]. Food Science and Biotechnology,2017,26(5):1423−1428. doi: 10.1007/s10068-017-0164-5
[66]	ZHANG C, YANG G, SHEN P, et al. Inactivation mechanism of slightly acidic electrolyzed water on Bacillus cereus spores[J]. Food Microbiology,2022,103:103951. doi: 10.1016/j.fm.2021.103951
[67]	SHU Q, NIU Y, ZHAO W, et al. Antibacterial activity and mannosylerythritol lipids against vegetative cells and spores of Bacillus cereus[J]. Food Control,2019,106:106711. doi: 10.1016/j.foodcont.2019.106711

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