Abstract
Listeria monocytogenes can cause listeriosis in humans through consumption of contaminated food. L. monocytogenes can adapt and grow in a vast array of physiochemical stresses in the food production environment. In this study, we performed a proteomics strategy in order to investigate how L. monocytogenes survives with a simultaneous exposure to low pH, high salinity and low temperature. The results showed that the adaptation processes mainly affected the biochemical pathways related to protein synthesis, oxidative stress, cell wall and nucleotide metabolism. Interestingly, enzymes involved in the carbohydrate metabolism of energy, such as glycolysis and pentose phosphate pathway, were derepressed due to the down-regulation of CodY, a global transcriptional repressor. The down-regulation of CodY, together with the up-regulation of carbohydrate metabolism enzymes, likely leads to the accumulation of pyruvate and further to the activation of fatty acid synthesis pathway. Proteomics profiling offered a better understanding of the physiological responses of this pathogen to adapt to harsh environment and would hopefully contribute to improving the food-processing and storage methods.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agoston R, Soni K, Jesudhasan PR, Russell WK, Mohacsi-Farkas C, Pillai SD (2009) Differential expression of proteins in Listeria monocytogenes under thermotolerance-inducing, heat shock, and prolonged heat shock conditions. Foodborne Pathog Dis 6:1133–1140
Ali V, Nozaki T (2013) Iron–sulphur clusters, their biosynthesis, and biological functions in protozoan parasites. Adv Parasitol 83:1–92
Ayala-Castro C, Saini A, Outten FW (2008) Fe–S cluster assembly pathways in bacteria. Microbiol Mol Biol Rev 72:110–125
Bennett HJ et al (2007) Characterization of relA and codY mutants of Listeria monocytogenes: identification of the CodY regulon and its role in virulence. Mol Microbiol 63:1453–1467
Borezee E, Pellegrini E, Berche P (2000) OppA of Listeria monocytogenes, an oligopeptide-binding protein required for bacterial growth at low temperature and involved in intracellular survival. Infect Immun 68:7069–7077
Bowman JP, Hages E, Nilsson RE, Kocharunchitt C, Ross T (2012) Investigation of the Listeria monocytogenes Scott A acid tolerance response and associated physiological and phenotypic features via whole proteome analysis. J Proteome Res 11:2409–2426
Brown GK, Otero LJ, LeGris M, Brown RM (1994) Pyruvate dehydrogenase deficiency. J Med Genet 31:875–879
Cacace G, Mazzeo MF, Sorrentino A, Spada V, Malorni A, Siciliano RA (2010) Proteomics for the elucidation of cold adaptation mechanisms in Listeria monocytogenes. J Proteomics 73:2021–2030
Cronan JE Jr. Gelmann EP (1975) Physical properties of membrane lipids: biological relevance and regulation. Bacteriol Rev 39:232–256
Cronan JE Jr. Waldrop GL (2002) Multi-subunit acetyl-CoA carboxylases. Prog Lipid Res 41:407–435
de Ortiz Orue Lucana D, Wedderhoff I, Groves MR (2012) ROS-mediated signalling in bacteria: zinc-containing Cys-X-X-Cys redox centres and iron-based oxidative stress. J Signal Transduct 2012:605905
Duche O, Tremoulet F, Namane A, Labadie J, European Listeria Genome C (2002) A proteomic analysis of the salt stress response of Listeria monocytogenes. FEMS Microbiol Lett 215:183–188
Dunny GM, Leonard BA (1997) Cell-cell communication in gram-positive bacteria. Annu Rev Microbiol 51:527–564
Durack J, Ross T, Bowman JP (2013) Characterisation of the transcriptomes of genetically diverse Listeria monocytogenes exposed to hyperosmotic and low temperature conditions reveal global stress-adaptation mechanisms. PLoS One 8:e73603
Farber JM, Peterkin PI (1991) Listeria monocytogenes, a food-borne pathogen. Microbiol Rev 55:476–511
Gandhi M, Chikindas ML (2007) Listeria: a foodborne pathogen that knows how to survive. Int J Food Microbiol 113:1–15
Giotis ES, Muthaiyan A, Blair IS, Wilkinson BJ, McDowell DA (2008) Genomic and proteomic analysis of the Alkali-Tolerance Response (AlTR) in Listeria monocytogenes 10403S. BMC Microbiol 8:102
Ignatova M et al (2013) Two-dimensional fluorescence difference gel electrophoresis analysis of Listeria monocytogenes submitted to a redox shock. J Proteomics 79:13–27
Johnson DC, Dean DR, Smith AD, Johnson MK (2005) Structure, function, and formation of biological iron–sulfur clusters. Annu Rev Biochem 74:247–281
Jones PM, George AM (2004) The ABC transporter structure and mechanism: perspectives on recent research. Cell Mol Life Sci 61:682–699
Li SJ, Cronan JE Jr (1992) The genes encoding the two carboxyltransferase subunits of Escherichia coli acetyl-CoA carboxylase. J Biol Chem 267:16841–16847
Loiseau L, Ollagnier-de-Choudens S, Nachin L, Fontecave M, Barras F (2003) Biogenesis of Fe–S cluster by the bacterial Suf system: SufS and SufE form a new type of cysteine desulfurase. J Biol Chem 278:38352–38359
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Lushchak VI (2011) Adaptive response to oxidative stress: bacteria, fungi, plants and animals. Comp Biochem Physiol Toxicol Pharmacol 153:175–190
Lynch M, Painter J, Woodruff R, Braden C, Centers for Disease C, Prevention (2006) Surveillance for foodborne-disease outbreaks—United States, 1998–2002. Morb Mortal Wkly Rep Surveill Summ 55:1–42
Majerczyk CD et al (2010) Direct targets of CodY in Staphylococcus aureus. J Bacteriol 192:2861–2877
Mead PS et al (1999) Food-related illness and death in the United States. Emerg Infect Dis 5:607–625
Neuhoff V, Arold N, Taube D, Ehrhardt W (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9:255–262
Phan-Thanh L, Gormon T (1997) Stress proteins in Listeria monocytogenes. Electrophoresis 18:1464–1471
Pittman JR, Buntyn JO, Posadas G, Nanduri B, Pendarvis K, Donaldson JR (2014) Proteomic analysis of cross protection provided between cold and osmotic stress in Listeria monocytogenes. J Proteome Res 13:1896–1904
Rhee SG (2006) Cell signaling. H2O2, a necessary evil for cell signaling. Science 312:1882–1883
Takahashi Y, Tokumoto U (2002) A third bacterial system for the assembly of iron–sulfur clusters with homologs in archaea and plastids. J Biol Chem 277:28380–28383
Tong L (2005) Acetyl-coenzyme A carboxylase: crucial metabolic enzyme and attractive target for drug discovery. Cell Mol Life Sci 62:1784–1803
Wollers S et al (2010) Iron–sulfur (Fe–S) cluster assembly: the SufBCD complex is a new type of Fe–S scaffold with a flavin redox cofactor. J Biol Chem 285:23331–23341
Acknowledgments
We are grateful to Prof. Hai-hong Wang, the School of Life Sciences, South China Agricultural University, for discussion and experimental helping in fatty acid analysis and critical reading of the manuscript. We also thank Prof. Jian-zhong Liu, the School of Life Sciences, SunYat-sen University, for helping in 2-DE experiments. This work was supported by the Joint Funds of Natural Science Foundation of China and Guangdong Province (No. U1031003) and NSFC (No. 30970123).
Conflict of interest
The authors have declared no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Erko Stackebrandt.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
He, L., Deng, QL., Chen, Mt. et al. Proteomics analysis of Listeria monocytogenes ATCC 19115 in response to simultaneous triple stresses. Arch Microbiol 197, 833–841 (2015). https://doi.org/10.1007/s00203-015-1116-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-015-1116-1