BMC Microbiology | |
Protein level identification of the Listeria monocytogenes Sigma H, Sigma L, and Sigma C regulons | |
Martin Wiedmann1  Kathryn J Boor1  Renato H Orsi1  Sana Mujahid1  | |
[1] Department of Food Science, Cornell University, 412 Stocking Hall, Ithaca, NY, USA | |
关键词: Quantitative proteomics; Alternative sigma factors; Listeria monocytogenes; | |
Others : 1143498 DOI : 10.1186/1471-2180-13-156 |
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received in 2013-02-07, accepted in 2013-07-04, 发布年份 2013 | |
【 摘 要 】
Background
Transcriptional regulation by alternative sigma (σ) factors represents an important mechanism that allows bacteria to rapidly regulate transcript and protein levels in response to changing environmental conditions. While the role of the alternative σ factor σB has been comparatively well characterized in L. monocytogenes, our understanding of the roles of the three other L. monocytogenes alternative σ factors is still limited. In this study, we employed a quantitative proteomics approach using Isobaric Tags for Relative and Absolute Quantitation (iTRAQ) to characterize the L. monocytogenes σL, σH, and σC protein regulons. Proteomic comparisons used a quadruple alternative σ factor mutant strain (ΔBCHL) and strains expressing a single alternative σ factor (i.e., σL, σH, and σC; strains ΔBCH, ΔBCL, and ΔBHL) to eliminate potential redundancies between σ factors.
Results
Among the three alternative σ factors studied here, σH provides positive regulation for the largest number of proteins, consistent with previous transcriptomic studies, while σL appears to contribute to negative regulation of a number of proteins. σC was found to regulate a small number of proteins in L. monocytogenes grown to stationary phase at 37°C. Proteins identified as being regulated by multiple alternative σ factors include MptA, which is a component of a PTS system with a potential role in regulation of PrfA activity.
Conclusions
This study provides initial insights into global regulation of protein production by the L. monocytogenes alternative σ factors σL, σH, and σC. While, among these σ factors, σH appears to positively regulate the largest number of proteins, we also identified PTS systems that appear to be co-regulated by multiple alternative σ factors. Future studies should not only explore potential roles of alternative σ factors in activating a “cascade” of PTS systems that potentially regulate PrfA, but also may want to explore the σL and σC regulons under different environmental conditions to identify conditions where these σ factors may regulate larger numbers of proteins or genes.
【 授权许可】
2013 Mujahid et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
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20150329095338853.pdf | 960KB | download | |
Figure 2. | 60KB | Image | download |
Figure 1. | 61KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
【 参考文献 】
- [1]Chaturongakul S, Raengpradub S, Wiedmann M, Boor KJ: Modulation of stress and virulence in Listeria monocytogenes. Trends Microbiol 2008, 16(8):388-396.
- [2]Gray MJ, Zadoks RN, Fortes ED, Dogan B, Cai S, Chen Y, Scott VN, Gombas DE, Boor KJ, Wiedmann M: Listeria monocytogenes isolates from foods and humans form distinct but overlapping populations. Appl Environ Microbiol 2004, 70(10):5833-5841.
- [3]Zhang C, Nietfeldt J, Zhang M, Benson AK: Functional consequences of genome evolution in Listeria monocytogenes: the lmo0423 and lmo0422 genes encode SigmaC and LstR, a lineage II-specific heat shock system. J Bacteriol 2005, 187(21):7243-7253.
- [4]Orsi RH, den Bakker HC, Wiedmann M: Listeria monocytogenes lineages: Genomics, evolution, ecology, and phenotypic characteristics. Int J Med Microbiol 2011, 301(2):79-96.
- [5]O’Byrne CP, Karatzas KA: The role of Sigma B (Sigma B) in the stress adaptations of Listeria monocytogenes: overlaps between stress adaptation and virulence. Adv Appl Microbiol 2008, 65:115-140.
- [6]Oliver HF, Orsi RH, Wiedmann M, Boor KJ: Listeria monocytogenes {Sigma}B has a small core regulon and a conserved role in virulence but makes differential contributions to stress tolerance across a diverse collection of strains. Appl Environ Microbiol 2010, 76(13):4216-4232.
- [7]Chaturongakul S, Raengpradub S, Palmer ME, Bergholz TM, Orsi RH, Hu Y, Ollinger J, Wiedmann M, Boor KJ: Transcriptomic and phenotypic analyses identify coregulated, overlapping regulons among PrfA, CtsR, HrcA, and the alternative sigma factors SigmaB, SigmaC, SigmaH, and SigmaL in Listeria monocytogenes. Appl Environ Microbiol 2011, 77(1):187-200.
- [8]Chaturongakul S, Boor KJ: RsbT and RsbV contribute to SigmaB-dependent survival under environmental, energy, and intracellular stress conditions in Listeria monocytogenes. Appl Environ Microbiol 2004, 70(9):5349-5356.
- [9]Wemekamp-Kamphuis HH, Wouters JA, de Leeuw PP, Hain T, Chakraborty T, Abee T: Identification of sigma factor Sigma B-controlled genes and their impact on acid stress, high hydrostatic pressure, and freeze survival in Listeria monocytogenes EGD-e. Appl Environ Microbiol 2004, 70(6):3457-3466.
- [10]Fraser KR, Sue D, Wiedmann M, Boor K, O’Byrne CP: Role of SigmaB in regulating the compatible solute uptake systems of Listeria monocytogenes: osmotic induction of opuC is SigmaB dependent. Appl Environ Microbiol 2003, 69(4):2015-2022.
- [11]Becker LA, Evans SN, Hutkins RW, Benson AK: Role of Sigma(B) in adaptation of Listeria monocytogenes to growth at low temperature. J Bacteriol 2000, 182(24):7083-7087.
- [12]Moorhead SM, Dykes GA: Influence of the sigB gene on the cold stress survival and subsequent recovery of two Listeria monocytogenes serotypes. Int J Food Microbiol 2004, 91(1):63-72.
- [13]Chan YC, Hu Y, Chaturongakul S, Files KD, Bowen BM, Boor KJ, Wiedmann M: Contributions of two-component regulatory systems, alternative sigma factors, and negative regulators to Listeria monocytogenes cold adaptation and cold growth. J Food Prot 2008, 71(2):420-425.
- [14]Oliver HF, Orsi RH, Ponnala L, Keich U, Wang W, Sun Q, Cartinhour SW, Filiatrault MJ, Wiedmann M, Boor KJ: Deep RNA sequencing of L. monocytogenes reveals overlapping and extensive stationary phase and Sigma B-dependent transcriptomes, including multiple highly transcribed noncoding RNAs. BMC Genomics 2009, 10:641-2164-10-641.
- [15]Abram F, Starr E, Karatzas KA, Matlawska-Wasowska K, Boyd A, Wiedmann M, Boor KJ, Connally D, O’Byrne CP: Identification of components of the Sigma B regulon in Listeria monocytogenes that contribute to acid and salt tolerance. Appl Environ Microbiol 2008, 74(22):6848-6858.
- [16]Abram F, Su WL, Wiedmann M, Boor KJ, Coote P, Botting C, Karatzas KA, O’Byrne CP: Proteomic analyses of a Listeria monocytogenes mutant lacking SigmaB identify new components of the SigmaB regulon and highlight a role for SigmaB in the utilization of glycerol. Appl Environ Microbiol 2008, 74(3):594-604.
- [17]Rea RB, Gahan CG, Hill C: Disruption of putative regulatory loci in Listeria monocytogenes demonstrates a significant role for Fur and PerR in virulence. Infect Immun 2004, 72(2):717-727.
- [18]Mattila M, Somervuo P, Rattei T, Korkeala H, Stephan R, Tasara T: Phenotypic and transcriptomic analyses of Sigma L-dependent characteristics in Listeria monocytogenes EGD-e. Food Microbiol 2012, 32(1):152-164.
- [19]Okada Y, Okada N, Makino S, Asakura H, Yamamoto S, Igimi S: The sigma factor RpoN (sigma54) is involved in osmotolerance in Listeria monocytogenes. FEMS Microbiol Lett 2006, 263(1):54-60.
- [20]Raimann E, Schmid B, Stephan R, Tasara T: The alternative sigma factor Sigma(L) of L. monocytogenes promotes growth under diverse environmental stresses. Foodborne Pathog Dis 2009, 6(5):583-591.
- [21]Robichon D, Gouin E, Debarbouille M, Cossart P, Cenatiempo Y, Hechard Y: The rpoN (sigma54) gene from Listeria monocytogenes is involved in resistance to mesentericin Y105, an antibacterial peptide from Leuconostoc mesenteroides. J Bacteriol 1997, 179(23):7591-7594.
- [22]Arous S, Buchrieser C, Folio P, Glaser P, Namane A, Hebraud M, Hechard Y: Global analysis of gene expression in an rpoN mutant of Listeria monocytogenes. Microbiology 2004, 150(Pt 5):1581-1590.
- [23]Mujahid S, Orsi RH, Vangay P, Boor KJ, Wiedmann M: Refinement of the Listeria monocytogenes σB regulon through quantitative proteomic analysis. Microbiology 2013. in press
- [24]Archambaud C, Nahori MA, Pizarro-Cerda J, Cossart P, Dussurget O: Control of Listeria Superoxide Dismutase by phosphorylation. J Biol Chem 2006, 281(42):31812-31822.
- [25]Ake FM, Joyet P, Deutscher J, Milohanic E: Mutational analysis of glucose transport regulation and glucose-mediated virulence gene repression in Listeria monocytogenes. Mol Microbiol 2011, 81(1):274-293.
- [26]Craig J, Venter Institute Comprehensive Microbial Resourcehttp://cmr.jcvi.org webcite
- [27]Dons L, Eriksson E, Jin Y, Rottenberg ME, Kristensson K, Larsen CN, Bresciani J, Olsen JE: Role of Flagellin and the two-component CheA/CheY system of Listeria monocytogenes in host cell invasion and virulence. Infect Immun 2004, 72(6):3237-3244.
- [28]Cacace G, Mazzeo MF, Sorrentino A, Spada V, Malorni A, Siciliano RA: Proteomics for the elucidation of cold adaptation mechanisms in Listeria monocytogenes. J Proteomics 2010, 73(10):2021-2030.
- [29]Mascher T, Hachmann AB, Helmann JD: Regulatory overlap and functional redundancy among Bacillus subtilis extracytoplasmic function sigma factors. J Bacteriol 2007, 189(19):6919-6927.
- [30]Stoll R, Goebel W: The major PEP-phosphotransferase systems (PTSs) for glucose, mannose and cellobiose of Listeria monocytogenes, and their significance for extra- and intracellular growth. Microbiology 2010, 156(Pt 4):1069-1083.
- [31]Keseler IM, Collado-Vides J, Santos-Zavaleta A, Peralta-Gil M, Gama-Castro S, Muniz-Rascado L, Bonavides-Martinez C, Paley S, Krummenacker M, Altman T, Kaipa P, Spaulding A, Pacheco J, Latendresse M, Fulcher C, Sarker M, Shearer AG, Mackie A, Paulsen I, Gunsalus RP, Karp PD: EcoCyc: a comprehensive database of Escherichia coli biology. Nucleic Acids Res 2011, 39(Database issue):D583-D590. http://biocyc.org/ECOLI/new-image?object=GALACTITOLCAT-PWY webcite
- [32]Dalet K, Cenatiempo Y, Cossart P, Hechard Y, European Listeria Genome Consortium: A Sigma(54)-dependent PTS permease of the mannose family is responsible for sensitivity of Listeria monocytogenes to mesentericin Y105. Microbiology 2001, 147(Pt 12):3263-3269.
- [33]Mujahid S, Bergholz TM, Oliver HF, Boor KJ, Wiedmann M: Exploration of the role of the non-Coding RNA SbrE in L. monocytogenes stress response. Int J Mol Sci 2012, 14(1):378-393.