AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (880 KB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

Cross-protective effect of acid adaptation on ethanol tolerance in Salmonella Enteritidis

Shoukui HeaBeining YeaZengfeng ZhangaYan CuiaSiyun WangbXianming Shia( )
MOST-USDA Joint Research Center for Food Safety, School of Agriculture and Biology, State Key Lab of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China
Food, Nutrition and Health, Faculty of Land and Food Systems, The University of British Columbia, Vancouver BC V6T 1Z4, Canada

Peer review under responsibility of KeAi Communications Co., Ltd.

Show Author Information

Abstract

Cross protection can undermine the effectiveness of control measures on foodborne pathogens, and therefore brings major implications for food safety. In this work, the capacity of Salmonella Enteritidis to mount ethanol tolerance following acid adaptation was characterized by analysis of cell viability and cell membrane property. It was observed that preadaptation to pH 4.5 significantly (P < 0.05) increased the tolerance of log-phase cells to ethanol; in contrast, stationary-phase cells displayed reduced ethanol tolerance after acid adaptation. However, acid adaptation did not cause cell leakage and morphological change in both log-phase and stationary-phase S. Enteritidis. Fatty acid analysis further revealed that the amount of C14:0, C17:0 cyclo and C19:0 cyclo fatty acids was increased, while that of C and C fatty acids was decreased, respectively, in response to acid adaptation, regardless of bacterial growth phase. Notably, acid adaptation significantly (P < 0.05) increased the proportion of C16:0 fatty acid in log-phase cells, but this effect did not occur in stationary-phase cells. Moreover, exogenous addition of C16:0 fatty acid to stationary-phase acid-adapted cultures was able to enhance bacterial ethanol tolerance. Taken together, C16:0 fatty acid is involved in the growth-phase-dependent protective effect of acid adaptation on ethanol tolerance in S. Enteritidis.

References

[1]

S. He, X. Shi, Microbial food safety in China: past, present, and future, Foodborne Pathog. Dis. 18 (2021) 510-518. https://doi.org/10.1089/fpd.2021.0009.

[2]

S.T. Ngoi, K.L. Thong, Molecular characterization showed limited genetic diversity among Salmonella Enteritidis isolated from humans and animals in Malaysia, Diagn. Micr. Infec. Dis. 77 (2013) 304-311. https://doi.org/10.1016/j.diagmicrobio.2013.09.004.

[3]

S.E. Majowicz, J. Musto, E. Scallan, et al., The global burden of nontyphoidal Salmonella gastroenteritis, Clin. Infect. Dis. 50 (2010) 882-889. https://doi.org/10.1086/650733.

[4]

E.H. Mezal, A. Sabol, M.A. Khan, et al., Isolation and molecular characterization of Salmonella enterica serovar Enteritidis from poultry house and clinical samples during 2010, Food Microbiol. 38 (2014) 67-74. https://doi.org/10.1016/j.fm.2013.08.003.

[5]

M.E. Pearce, N.F. Alikhan, T.J. Dallman, et al., Comparative analysis of core genome MLST and SNP typing within a European Salmonella serovar Enteritidis outbreak, Int. J. Food Microbiol. 274 (2018) 1-11. https://doi.org/10.1016/j.ijfoodmicro.2018.02.023.

[6]

E. Mani-López, H.S. García, A. López-Malo, Organic acids as antimicrobials to control Salmonella in meat and poultry products, Food Res. Int. 45 (2012) 713-721. https://doi.org/10.1016/j.foodres.2011.04.043.

[7]

H.G. Yuk, D.L. Marshall, Adaptation of Escherichia coli O157: H7 to pH alters membrane lipid composition, verotoxin secretion, and resistance to simulated gastric fluid acid, Appl. Environ. Microbiol. 70 (2004) 3500-3505. https://doi.org/10.1128/AEM.70.6.3500-3505.2004.

[8]

D. O'Leary, E.M. McCabe, M.P. McCusker, et al., Acid environments affect biofilm formation and gene expression in isolates of Salmonella enterica Typhimurium DT104, Int. J. Food Microbiol. 206 (2015) 7-16. https://doi.org/10.1016/j.ijfoodmicro.2015.03.030.

[9]

K. Jia, G. Wang, L. Liang, et al., Preliminary transcriptome analysis of mature biofilm and planktonic cells of Salmonella Enteritidis exposure to acid stress, Front. Microbiol. 8 (2017) 1861. https://doi.org/10.3389/fmicb.2017.01861.

[10]

A. Lianou, G.J.E. Nychas, K.P. Koutsoumanis, Variability in the adaptive acid tolerance response phenotype of Salmonella enterica strains, Food Microbiol. 62 (2017) 99-105. https://doi.org/10.1016/j.fm.2016.10.011.

[11]

S. Hu, Y. Yu, D. Zhou, et al., Global transcriptomic acid tolerance response in Salmonella Enteritidis, LWT-Food Sci. Technol. 92 (2018) 330-338. https://doi.org/10.1016/j.lwt.2018.02.039.

[12]

S. Hu, Y. Yu, Z. Lv, et al., Proteomics study unveils ROS balance in acid-adapted Salmonella Enteritidis, Food Microbiol. 92 (2020) 103585. https://doi.org/10.1016/j.fm.2020.103585.

[13]

B. Ye, S. He, X. Zhou, et al., Response to acid adaptation in Salmonella enterica serovar Enteritidis, J. Food Sci. 84 (2019) 599-605. https://doi.org/10.1111/1750-3841.14465.

[14]

A. Gavriil, A. Thanasoulia, P.N. Skandamis, Sublethal concentrations of undissociated acetic acid may not always stimulate acid resistance in Salmonella enterica sub. enterica serovar Enteritidis phage type 4: implications of challenge substrate associated factors, PLoS One 15 (2020) e0234999. https://doi.org/10.1371/journal.pone.0234999.

[15]

N. Dhowlaghar, Q. Shen, R. Nannapaneni, et al., Survival of acid stress adapted cells of Listeria monocytogenes serotypes 1/2a and 4b in commonly used disinfectants in broth and water models, LWT-Food Sci. Technol. 109 (2019) 201-206. https://doi.org/10.1016/j.lwt.2019.04.007.

[16]

M.L. Chiang, H.C. Chen, C. Wu, et al., Effect of acid adaptation on the environmental stress tolerance of three strains of Vibrio parahaemolyticus, Foodborne Pathog. Dis. 11 (2014) 287-294. https://doi.org/10.1089/fpd.2013.1641.

[17]

S. He, K. Fong, S. Wang, et al., Meat juice contributes to the stability of ethanol adaptation in Salmonella enterica serovar Enteritidis, Food Qual. Saf. 5 (2021) 1-6. https://doi.org/10.1093/fqsafe/fyab017.

[18]

R.A. Wu, H.G. Yuk, D. Liu, et al., Recent advances in understanding the effect of acid-adaptation on the cross-protection to food-related stress of common foodborne pathogens, Crit. Rev. Food Sci. Nutr. (2021) 1-18. https://doi.org/10.1080/10408398.2021.1913570.

[19]

A. Álvarez-Ordóñez, M. Prieto, A. Bernardo, et al., The acid tolerance response of Salmonella spp.: an adaptive strategy to survive in stressful environments prevailing in foods and the host, Food Res. Int. 45 (2012) 482-492. https://doi.org/10.1016/j.foodres.2011.04.002.

[20]

S. He, K. Fong, S. Wang, et al., Ethanol adaptation in foodborne bacterial pathogens, Crit. Rev. Food Sci. Nutr. 61 (2021) 777-787. https://doi.org/10. 1080/10408398.2020.1746628.

[21]

S. He, X. Zhou, C. Shi, et al., Ethanol adaptation induces direct protection and cross-protection against freezing stress in Salmonella enterica serovar Enteritidis, J. Appl. Microbiol. 120 (2016) 697-704. https://doi.org/10.1111/jam.13042.

[22]

R. Dong, X. Qin, S. He, et al., DsrA confers resistance to oxidative stress in Salmonella enterica serovar Typhimurium, Food Control 121 (2021) 107571. https://doi.org/10.1016/j.foodcont.2020.107571.

[23]
M. Sasser, MIDI technical note #101: bacterial identification by gas chromatographic analysis of fatty acids methyl esters (GC-FAME), Netwark, Delaware: MIDI, Inc., 2001.
[24]

X. Qin, R. Dong, S. He, et al., Characterization of the role of ybgC in lysozyme resistance of Salmonella Enteritidis, Food Control 109 (2020) 106732. https://doi.org/10.1016/j.foodcont.2019.106732.

[25]

M.L. Chiang, C.C Chou, Survival of Vibrio parahaemolyticus under environmental stresses as influenced by growth phase and pre-adaptation treatment, Food Microbiol. 26 (2009) 391-395. https://doi.org/10.1016/j.fm.2009.01.005.

[26]

Y. Yang, M.I. Kadim, W.J. Khoo, et al., Membrane lipid composition and stress/virulence related gene expression of Salmonella Enteritidis cells adapted to lactic acid and trisodium phosphate and their resistance to lethal heat and acid stress, Int. J. Food Microbiol. 191 (2014) 24-31. https://doi.org/10.1016/j.ijfoodmicro.2014.08.034.

[27]

A. Alvarez-Ordonez, A. Fernandez, M. Lopez, et al., Relationship between membrane fatty acid composition and heat resistance of acid and cold stressed Salmonella senftenberg CECT 4384, Food Microbiol. 26 (2009) 347-353. https://doi.org/10.1016/j.fm.2008.11.002.

[28]

M.L. Chiang, W.L. Ho, C.C. Chou, Response of Vibrio parahaemolyticus to ethanol shock, Food Microbiol. 23 (2006) 461-467. https://doi.org/10.1016/j.fm.2005.07.001.

[29]

Y. Yoon, H. Lee, S. Lee, et al., Membrane fluidity-related adaptive response mechanisms of foodborne bacterial pathogens under environmental stresses, Food Res. Int. 72 (2015) 25-36. https://doi.org/10.1016/j.foodres.2015.03.016.

[30]

H. Mizoguchi, S. Hara, Ethanol-induced alterations in lipid composition of Saccharomyces cerevisiae in the presence of exogenous fatty acid, J. Ferment. Bioeng. 83 (1997) 12-16. https://doi.org/10.1016/S0922-338X(97)87319-9.

[31]

M. Ghareib, K.A. Youssef, A.A. Khalil, Ethanol tolerance of Saccharomyces cerevisiae and its relationship to lipid content and composition, Folia Microbiol. 33 (1988) 447-452. https://doi.org/10.1007/BF02925769.

[32]

M.L. Chiang, W.L. Ho, C.C. Chou, Ethanol shock changes the fatty acid profile and survival behavior of Vibrio parahaemolyticus in various stress conditions, Food Microbiol. 25 (2008) 359-365. https://doi.org/10.1016/j.fm.2007.10.002.

[33]

T.N. Dinh, K. Nagahisa, T. Hirasawa, et al., Adaptation of Saccharomyces cerevisiae cells to high ethanol concentration and changes in fatty acid composition of membrane and cell size, PLoS One 3 (2008) e2623. https://doi.org/10.1371/journal.pone.0002623.

[34]

L.H. Luo, P.S. Seo, J.W. Seo, et al., Improved ethanol tolerance in Escherichia coli by changing the cellular fatty acids composition through genetic manipulation, Biotechnol. Lett. 31 (2009) 1867-1871. https://doi.org/10.1007/s10529-009-0092-4.

[35]

A. Lianou, K.P. Koutsoumanis, Evaluation of the strain variability of Salmonella enterica acid and heat resistance, Food Microbiol. 34 (2013) 259-267. https://doi.org/10.1016/j.fm.2012.10.009.

[36]

A. Lianou, G.J.E. Nychas, K.P. Koutsoumanis, Variability in the adaptive acid tolerance response phenotype of Salmonella enterica strains, Food Microbiol. 62 (2017) 99-105. https://doi.org/10.1016/j.fm.2016.10.011.

[37]

S. Tamber, Population-wide survey of Salmonella enterica response to high-pressure processing reveals a diversity of responses and tolerance mechanisms, Appl. Environ. Microbiol. 84 (2018) 1-12. https://doi.org/10.1128/AEM.01673-17.

Food Science and Human Wellness
Pages 1402-1407
Cite this article:
He S, Ye B, Zhang Z, et al. Cross-protective effect of acid adaptation on ethanol tolerance in Salmonella Enteritidis. Food Science and Human Wellness, 2023, 12(4): 1402-1407. https://doi.org/10.1016/j.fshw.2022.10.033

518

Views

33

Downloads

5

Crossref

5

Web of Science

5

Scopus

0

CSCD

Altmetrics

Received: 30 November 2021
Revised: 28 December 2021
Accepted: 12 February 2022
Published: 18 November 2022
© 2023 Beijing Academy of Food Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return