Journal Home > Volume 11 , Issue 2
Food Science and Human Wellness 2022, 11(2): 332-340 https://doi.org/10.1016/j.fshw.2021.11.007
Research Article | Open Access | Issue | Published: 25 November 2021

Ciprofloxacin stress changes key enzymes and intracellular metabolites of Lactobacillus plantarum DNZ-4

Show Author's Information Pin Chena,  Xiaoqian Chena,  Wei Yua,  Bo Zhoua,  Lihua Liub,  Yuzhuo Yangc,  Peng Dua,  Libo Liua( ),  Chun Lia( )
Key Laboratory of Dairy Science, Ministry of Education, Food Science College, Northeast Agricultural University, Harbin 150030, China
Institute of Animal Science (IAS), Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, China
National Dairy Product Quality Supervision and Inspection Center, Harbin 150024, China
Keywords:
Metabolism, Ciprofloxacin, Lactobacillus plantarum DNZ-4, Key enzymes
Cite this article:
Chen P, Chen X, Yu W, et al. Ciprofloxacin stress changes key enzymes and intracellular metabolites of Lactobacillus plantarum DNZ-4. Food Science and Human Wellness, 2022, 11(2): 332-340. https://doi.org/10.1016/j.fshw.2021.11.007
Download citation
EndNote(RIS)
BibTeX

518

Views

31

Downloads

Citations

3

Crossref

3

WoS

3

Scopus

0

CSCD

Abstract Full text About this article

Ciprofloxacin (CIP) is an antibiotic used to treat infections caused by bacteria. In this experiment, key enzymes and intracellular metabolites of Lactobacillus plantarum DNZ-4 was researched under CIP stress. The results showed that the activities of hexokinase, pyruvate kinase, β-galactosidase and Na+, K+-ATPase after 1/2 minimum bacteriostatic concentration (MIC) CIP treatment were significantly decreased (P < 0.01). Gas chromatography-mass spectrometry was used to analysis the changes of main metabolites in the cells and principal component analysis and partial least square model were constructed. The results indicated that CIP could cause changes in intracellular fatty acids, carbohydrates and amino acids, and the mechanism of amino acid metabolism under CIP stress was significantly inhibited. L. plantarum DNZ-4 made stress response to CIP by regulating the ratio of saturated fatty acids and unsaturated fats. This experiment revealed the changes of growth and metabolism mechanism of L. plantarum DNZ-4 under CIP stress, which help to provide technical means for the development of effective probiotics preparation products.


menu
Abstract
Full text
Outline
About this article

Ciprofloxacin stress changes key enzymes and intracellular metabolites of Lactobacillus plantarum DNZ-4

Show Author's information Pin Chena, Xiaoqian Chena, Wei Yua, Bo Zhoua, Lihua Liub, Yuzhuo Yangc, Peng Dua, Libo Liua( ), Chun Lia( )
Key Laboratory of Dairy Science, Ministry of Education, Food Science College, Northeast Agricultural University, Harbin 150030, China
Institute of Animal Science (IAS), Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, China
National Dairy Product Quality Supervision and Inspection Center, Harbin 150024, China

Abstract

Ciprofloxacin (CIP) is an antibiotic used to treat infections caused by bacteria. In this experiment, key enzymes and intracellular metabolites of Lactobacillus plantarum DNZ-4 was researched under CIP stress. The results showed that the activities of hexokinase, pyruvate kinase, β-galactosidase and Na+, K+-ATPase after 1/2 minimum bacteriostatic concentration (MIC) CIP treatment were significantly decreased (P < 0.01). Gas chromatography-mass spectrometry was used to analysis the changes of main metabolites in the cells and principal component analysis and partial least square model were constructed. The results indicated that CIP could cause changes in intracellular fatty acids, carbohydrates and amino acids, and the mechanism of amino acid metabolism under CIP stress was significantly inhibited. L. plantarum DNZ-4 made stress response to CIP by regulating the ratio of saturated fatty acids and unsaturated fats. This experiment revealed the changes of growth and metabolism mechanism of L. plantarum DNZ-4 under CIP stress, which help to provide technical means for the development of effective probiotics preparation products.

Keywords: Metabolism, Ciprofloxacin, Lactobacillus plantarum DNZ-4, Key enzymes

References(37)

[1]

H.A. Seddik, F. Bendali, F. Gancel, et al., Lactobacillus plantarum and its probiotic and food potentialities, Probiotics & Antimicro. Prot. 31 (2017) 88-93. https://doi.org/10.1007/s12602-017-9264-z.
DOI Google Scholar
[2]

M. Kleerebezem, P. Hols, J. Hugenholtz, Lactic acid bacteria as a cell factory: rerouting of carbon metabolism in Lactococcus lactis by metabolic engineering, Enzyme Microb. Technol. 26 (2000) 840-848. https://doi.org/10.1016/S0141-0229(00)00180-0.
DOI Google Scholar
[3]

M.V. Arasu, N.A. Aldhabi, S. Ilavenil, et al., In vitro importance of probiotic Lactobacillus plantarum related to medical field, Saudi J. Biol. Sci. 23 (2016) 372-389. https://doi.org/10.1016/j.sjbs.2015.09.022.
DOI Google Scholar
[4]

W. Wang, J. He, D. Pan, et al., Metabolomics analysis of Lactobacillus plantarum ATCC 14917 adhesion activity under initial acid and alkali stress, PLoS One 13 (2018) 447-489. https://doi.org/10.1371/journal.pone.0196231.
DOI Google Scholar
[5]

D.M. Campoli-Richards, J.P. Monk, A. Price, et al., Ciprofloxacin, Drugs 35 (1988) 373-447.
DOI Google Scholar
[6]

R. Davis, A. Markham, J. Balfour, Ciprofloxacin. An updated review of its pharmacology, therapeutic efficacy and tolerability, Drugs 51 (1986) 1019-1074. https://doi.org/10.2165/00003495-199651060-00010.
DOI Google Scholar
[7]

J. Machuca, E. Recacha, A. Briales, et al., Cellular response to ciprofloxacin in low-level quinolone-resistant Escherichia coli, Front. Microbiol. 8 (2017) 483-492. https://doi.org/10.3389/fmicb.2017.01370.
DOI Google Scholar
[8]

D.I. Andersson, D. Hughes, Microbiological effects of sublethal levels of antibiotics, Nat. Rev. Microbiol. 12 (2014) 465-478. https://doi.org/10.1038/nrmicro3270.
DOI Google Scholar
[9]

R.N. Klitgaard, J. Bimal, G. Luca, et al., DNA damage repair and drug efflux as potential targets for reversing low or intermediate ciprofloxacin resistance in E. coli K-12, Front. Microbiol. 9 (2018) 1438-1467. https://doi.org/10.3389/fmicb.2018.01438.
DOI Google Scholar
[10]

R.J. Carman, M.A. Woodburn, Effects of low levels of ciprofloxacin on a chemostat model of the human colonic microflora, Regul. Toxicol. Pharmacol. 33 (2001) 276-284. https://doi.org/10.1006/rtph.2001.1473.
DOI Google Scholar
[11]

J. Weigelt, L.D. Mcbroomcerajewski, M. Schapira, et al., Erratum to: 'structural genomics and drug discovery: all in the family, Curr. Opin. Chem. Biol. 13 (2009) 132.
DOI Google Scholar
[12]

S. Rochfort, Metabolomics reviewed: a new "omics" platform technology for systems biology and implications for natural products research, J. Nat. Prod. 68 (2005) 1813-1820. https://doi.org/10.1021/np050255w.
DOI Google Scholar
[13]

Y. Hu, S. Zhang, Z. Xu, et al. 4-Quinolone hybrids and their antibacterial activities, Eur. J. Med. Chem. 141 (2017) 335-345. https://doi.org/10.1016/j.ejmech.2017.09.050.
DOI Google Scholar
[14]

S. Correia, M. Hebraud, I. Chafsey, et al., Comparative subproteomic analysis of clinically acquired fluoroquinolone resistance and ciprofloxacin stress in Salmonella Typhimurium DT104B, Proteom. Clin. Appl. 11 (2017) 1600-1607. https://doi.org/10.1002/prca.201600107.
DOI Google Scholar
[15]

W. Li, S. Zhang, X. Wang, et al., Systematically integrated metabonomic-proteomic studies of Escherichia coli under ciprofloxacin stress, J. Proteomics 179 (2018) 61-70. https://doi.org/10.1016/j.jprot.2018.03.002.
DOI Google Scholar
[16]

B. Shan, Y. Cai, J.D. Brooks, et al., Antibacterial properties of Polygonum cuspidatum roots and their major bioactive constituents, Food Chem. 109 (2008) 530-537. https://doi.org/10.1016/j.foodchem.2007.12.064.
DOI Google Scholar
[17]

I.B. Pavlova, D.A. Bannikova, A.B. Kononenko, et al., Electron microscopy study of interaction of lactic acid bacteria with pathogenic microorganisms, Russ. Agricult. Sci. 39 (2013) 179-183. https://doi.org/10.3103/S106836741302016X.
DOI Google Scholar
[18]

J.L. Brunelle, R. Green, Coomassie blue staining, Methods Enzymol. 541 (2014) 161-167.
Google Scholar
[19]

D.C. Hooper, G.A. Jacoby, Topoisomerase inhibitors: fluoroquinolone mechanisms of action and resistance, Cold Spring Harb. Perspect. Med. 6 (2016) 189-196. https://doi.org/10.1101/cshperspect.a025320.
DOI Google Scholar
[20]
T. Dorr, K. Lewis, M. Vulic, SOS response induces persistence to fluoroquinolones in Escherichia coli, PLoS Genet. 5 (2009) 647-665. https://doi.org/110.1371/journal.pgen.1000760.
[21]

S.M. Smith, R.H.K. Eng, Activity of ciprofloxacin against methicillin-resistant Staphylococcus aureus, Antimicrob. Agents Chemother. 27 (1985) 688-691. https://doi.org/10.1128/AAC.27.5.688.
DOI Google Scholar
[22]

B. Nanduri, M.L. Lawrence, C.R. Boyle, et al., Effects of subminimum inhibitory concentrations of antibiotics on the pasteurella multocida proteome: a systems approach, Comp. Funct. Genomics. 5 (2006) 572-580. https://doi.org/10.1021/pr050360r.
DOI Google Scholar
[23]

D.J. Cabral, J.I. Wurster, P. Belenky, Antibiotic persistence as a metabolic adaptation: stress, metabolism, the host, and new directions, Antimicrob. Agents Chemother. 11 (2018) 14-28. https://doi.org/10.3390/ph11010014.
DOI Google Scholar
[24]

J.L. Brown, S. Koorajian, J. Katze, et al., β-Galactosidase, J. Biol. Chem. 241 (1966) 2826-2831.
DOI Google Scholar
[25]

M.V. Tselevych, S.M. Mandzynets, D.I. Sanahursky, Effect of antibiotics on Na(+), K(+)-ATP-ase activity of the membranes in the Misgurnus fossilis L. embryos, Fiziol Zh. 50 (2004) 64-68.
Google Scholar
[26]

R. Zemelman, M.A. Mondaca, A. Neira, et al., Bacterial cell characteristics that contribute to antibiotic resistance, Arch. Med. Vet. 13 (1980) 233-245.
Google Scholar
[27]

S. Even, N.D. Lindley, P. Loubière, et al., Dynamic response of catabolic pathways to autoacidification in Lactococcus lactis: transcript profiling and stability in relation to metabolic and energetic constraints, Mol. Microbiol. 45 (2002) 58-78. https://doi.org/10.1046/j.1365-2958.2002.03086.x.
DOI Google Scholar
[28]

W.N. Konings, J.S. Lolkema, H. Bolhuis, et al., The role of transport processes in survival of lactic acid bacteria, energy transduction and multidrug resistance, Anton. Leeuw. Int. J. G. 71 (1997) 117-128. https://doi.org/10.1023/a:1000143525601.
DOI Google Scholar
[29]

L.N. Churkina, Z.P. Vasiurenko, V.V. Smirnov, et al., Effect of antibiotic AL-87 on the fatty acid composition of microorganisms in different taxonomic groups, Antibiotiki. 28 (1983) 489-502.
Google Scholar
[30]

V.V. Smirnov, L.N. Churkina, Z.P. Vasiurenko, Antibiotic AL-87 induction of changes in the fatty acid composition of phospholipids and neutral lipids in a sensitive strain of Staphylococcus aureus 209P, Antibiot Chemother. 33 (1988) 440-448.
Google Scholar
[31]

E.P. Feofilova, A.I. Usov, I.S. Mysyakina, et al., Trehalose: chemical structure, biological functions, and practical application, Microbiology 83 (2014) 184-194. https://doi.org/10.1134/S0026261714020064.
DOI Google Scholar
[32]

M.F. Roberts, Inositol in bacteria and archaea, Sub-cell Biochem. 39 (2006) 103-133.
DOI Google Scholar
[33]

M. Fernández, M. Zúñiga, Amino acid catabolic pathways of lactic acid bacteria, Crit. Rev. Microbiol. 32 (2006) 155-174. https://doi.org/10.1080/10408410600880643.
DOI Google Scholar
[34]

D. Banerjee, D. Parmar, N. Bhattacharya, et al., A scalable metabolite supplementation strategy against antibiotic resistant pathogen Chromobacterium violaceum induced by NAD+/NADH+ imbalance, BMC Syst. Biol. 11 (2017) 51-64. https://doi.org/10.1186/s12918-017-0427-z.
DOI Google Scholar
[35]

P. Belenky, J.D. Ye, C.B. Porter, et al., Bactericidal antibiotics induce toxic metabolic perturbations that lead to cellular damage, Cell Rep. 13 (2015) 968-980. https://doi.org/10.1016/j.celrep.2015.09.059.
DOI Google Scholar
[36]

B. Zhang, S.M. Halouska, C.E. Schiaffo, et al., NMR analysis of a stress response metabolic signaling network, J. Proteome Res. 10 (2011) 3743-3754. https://doi.org/10.1021/pr200360w.
DOI Google Scholar
[37]

K.K. Suresh, S.D. Bhosale, H.V. Thulasiram, et al., Comparative and chemical proteomic approaches reveal gatifloxacin deregulates enzymes involved in glucose metabolism, J. Toxicol. Sci. 36 (2011) 787-796. https://doi.org/10.2131/jts.36.787.
DOI Google Scholar
Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 08 July 2020
Revised: 04 November 2020
Accepted: 19 January 2021
Published: 25 November 2021
Issue date: March 2022

Copyright

© 2022 Beijing Academy of Food Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd.

Acknowledgements

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Grant No. 31671874), National Key Research and Development Project (2018YFD0502404), Natural Science Foundation of Heilongjiang Province of China (Grant No.C2018022) and Academic Backbone Plan of Northeast Agricultural University (Grant No. 18XG27) and Research Fund for Key Laboratory of Dairy Science, Ministry of Education, Heilongjiang Province, China (2015KLDSOF-07), and the Project of Young Innovative Talents of Colleges and Universities (UNPYSCT-2016149).

Rights and permissions

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

Return