1887

Microbiology Society logo

Volume 159, Issue Pt_6

Refinement of the σ regulon through quantitative proteomic analysis Free

Abstract

σ is an alternative σ factor that regulates stress response and virulence genes in the foodborne pathogen . To gain further insight into σ-dependent regulatory mechanisms in , we (i) performed quantitative proteomic comparisons between the parent strain 10403S and an isogenic Δ mutant and (ii) conducted a meta-analysis of published microarray studies on the 10403S σ regulon. A total of 134 genes were found to be significantly positively regulated by σ at the transcriptomic level with >75 % of these genes preceded by putative σ-dependent promoters; 21 of these 134 genes were also found to be positively regulated by σ through proteomics. In addition, 15 proteins were only found to be positively regulated by σ through proteomics analyses, including Lmo1349, a putative glycine cleavage system protein. The lmo1349 gene is preceded by a 5′ UTR that functions as a glycine riboswitch, which suggests regulation of glycine metabolism by σ in . Herein, we propose a model where σ upregulates pathways that facilitate biosynthesis and uptake of glycine, which may then activate this riboswitch. Our data also (i) identified a number of σ-dependent proteins that appear to be encoded by genes that are co-regulated by multiple transcriptional regulators, in particular PrfA, and (ii) found σ-dependent genes and proteins to be overrepresented in the ‘energy metabolism’ role category, highlighting contributions of the σ regulon to energy metabolism as well as a role of PrfA and σ interaction in regulating aspects of energy metabolism in .

  • Received:
  • Accepted:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.066001-0
2013-06-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/6/1109.html?itemId=/content/journal/micro/10.1099/mic.0.066001-0&mimeType=html&fmt=ahah

References

  1. Abram F., Su W. L., Wiedmann M., Boor K. J., Coote P., Botting C., Karatzas K. A., O’Byrne C. P.( 2008a). Proteomic analyses of a Listeria monocytogenes mutant lacking σB identify new components of the σB regulon and highlight a role for σB in the utilization of glycerol. Appl Environ Microbiol 74:594–604 [View Article][PubMed]
     [Google Scholar]
  2. Abram F., Starr E., Karatzas K. A., Matlawska-Wasowska K., Boyd A., Wiedmann M., Boor K. J., Connally D., O’Byrne C. P.( 2008b). Identification of components of the sigma B regulon in Listeria monocytogenes that contribute to acid and salt tolerance. Appl Environ Microbiol 74:6848–6858 [View Article][PubMed]
     [Google Scholar]
  3. Bennett H. J., Pearce D. M., Glenn S., Taylor C. M., Kuhn M., Sonenshein A. L., Andrew P. W., Roberts I. S.( 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 [View Article][PubMed]
     [Google Scholar]
  4. Butler E. B., Xiong Y., Wang J., Strobel S. A.( 2011). Structural basis of cooperative ligand binding by the glycine riboswitch. Chem Biol 18:293–298 [View Article][PubMed]
     [Google Scholar]
  5. Chatterjee S. S., Hossain H., Otten S., Kuenne C., Kuchmina K., Machata S., Domann E., Chakraborty T., Hain T.( 2006). Intracellular gene expression profile of Listeria monocytogenes. Infect Immun 74:1323–1338 [View Article][PubMed]
     [Google Scholar]
  6. Chaturongakul S., Boor K. J.( 2004). RsbT and RsbV contribute to σB-dependent survival under environmental, energy, and intracellular stress conditions in Listeria monocytogenes. Appl Environ Microbiol 70:5349–5356 [View Article][PubMed]
     [Google Scholar]
  7. Chaturongakul S., Raengpradub S., Wiedmann M., Boor K. J.( 2008). Modulation of stress and virulence in Listeria monocytogenes. Trends Microbiol 16:388–396 [View Article][PubMed]
     [Google Scholar]
  8. Erion T. V., Strobel S. A.( 2011). Identification of a tertiary interaction important for cooperative ligand binding by the glycine riboswitch. RNA 17:74–84 [View Article][PubMed]
     [Google Scholar]
  9. Fraser K. R., Sue D., Wiedmann M., Boor K., O’Byrne C. P.( 2003). Role of σB in regulating the compatible solute uptake systems of Listeria monocytogenes: osmotic induction of opuC is σB dependent. Appl Environ Microbiol 69:2015–2022 [View Article][PubMed]
     [Google Scholar]
  10. Garner M. R., Njaa B. L., Wiedmann M., Boor K. J.( 2006). Sigma B contributes to Listeria monocytogenes gastrointestinal infection but not to systemic spread in the guinea pig infection model. Infect Immun 74:876–886 [View Article][PubMed]
     [Google Scholar]
  11. Hain T., Hossain H., Chatterjee S. S., Machata S., Volk U., Wagner S., Brors B., Haas S., Kuenne C. T.& other authors ( 2008). Temporal transcriptomic analysis of the Listeria monocytogenes EGD-e σB regulon. BMC Microbiol 8:20 [View Article][PubMed]
     [Google Scholar]
  12. Hegde P. S., White I. R., Debouck C.( 2003). Interplay of transcriptomics and proteomics. Curr Opin Biotechnol 14:647–651 [View Article][PubMed]
     [Google Scholar]
  13. Huang L., Serganov A., Patel D. J.( 2010). Structural insights into ligand recognition by a sensing domain of the cooperative glycine riboswitch. Mol Cell 40:774–786 [View Article][PubMed]
     [Google Scholar]
  14. Joseph B., Mertins S., Stoll R., Schär J., Umesha K. R., Luo Q., Müller-Altrock S., Goebel W.( 2008). Glycerol metabolism and PrfA activity in Listeria monocytogenes. J Bacteriol 190:5412–5430 [View Article][PubMed]
     [Google Scholar]
  15. Kazmierczak M. J., Wiedmann M., Boor K. J.( 2005). Alternative sigma factors and their roles in bacterial virulence. Microbiol Mol Biol Rev 69:527–543 [View Article][PubMed]
     [Google Scholar]
  16. Kim H., Marquis H., Boor K. J.( 2005). σB contributes to Listeria monocytogenes invasion by controlling expression of inlA and inlB. Microbiology 151:3215–3222 [View Article][PubMed]
     [Google Scholar]
  17. Kingsford C. L., Ayanbule K., Salzberg S. L.( 2007). Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. Genome Biol 8:R22 [View Article][PubMed]
     [Google Scholar]
  18. Kwon M., Strobel S. A.( 2008). Chemical basis of glycine riboswitch cooperativity. RNA 14:25–34 [View Article][PubMed]
     [Google Scholar]
  19. Loh E., Gripenland J., Johansson J.( 2006). Control of Listeria monocytogenes virulence by 5′-untranslated RNA. Trends Microbiol 14:294–298 [View Article][PubMed]
     [Google Scholar]
  20. Mandal M., Lee M., Barrick J. E., Weinberg Z., Emilsson G. M., Ruzzo W. L., Breaker R. R.( 2004). A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 306:275–279 [View Article][PubMed]
     [Google Scholar]
  21. Mellin J. R., Cossart P.( 2012). The non-coding RNA world of the bacterial pathogen Listeria monocytogenes. RNA Biol 9:372–378 [View Article][PubMed]
     [Google Scholar]
  22. Mujahid S., Bergholz T. M., Oliver H. F., Boor K. J., Wiedmann M.( 2013). Exploration of the role of the non-coding RNA SbrE in L. monocytogenes stress response. Int J Mol Sci 14:378–393 [View Article][PubMed]
     [Google Scholar]
  23. Nielsen J. S., Olsen A. S., Bonde M., Valentin-Hansen P., Kallipolitis B. H.( 2008). Identification of a sigma B-dependent small noncoding RNA in Listeria monocytogenes. J Bacteriol 190:6264–6270 [View Article][PubMed]
     [Google Scholar]
  24. O’Byrne C. P., Karatzas K. A.( 2008). The role of sigma B (σB) in the stress adaptations of Listeria monocytogenes: overlaps between stress adaptation and virulence. Adv Appl Microbiol 65:115–140 [View Article][PubMed]
     [Google Scholar]
  25. Oliver H. F., Orsi R. H., Ponnala L., Keich U., Wang W., Sun Q., Cartinhour S. W., Filiatrault M. J., Wiedmann M., Boor K. J.( 2009). 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 10:641 [View Article][PubMed]
     [Google Scholar]
  26. Oliver H. F., Orsi R. H., Wiedmann M., Boor K. J.( 2010). Listeria monocytogenes σB 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 76:4216–4232 [View Article][PubMed]
     [Google Scholar]
  27. Ollinger J., Bowen B., Wiedmann M., Boor K. J., Bergholz T. M.( 2009). Listeria monocytogenes σB modulates PrfA-mediated virulence factor expression. Infect Immun 77:2113–2124 [View Article][PubMed]
     [Google Scholar]
  28. Palmer M. E., Chaturongakul S., Wiedmann M., Boor K. J.( 2011). The Listeria monocytogenes σB regulon and its virulence-associated functions are inhibited by a small molecule. MBio 2:e00241-11 [View Article][PubMed]
     [Google Scholar]
  29. Phan T. T., Schumann W.( 2007). Development of a glycine-inducible expression system for Bacillus subtilis. J Biotechnol 128:486–499 [View Article][PubMed]
     [Google Scholar]
  30. Picard F., Dressaire C., Girbal L., Cocaign-Bousquet M.( 2009). Examination of post-transcriptional regulations in prokaryotes by integrative biology. C R Biol 332:958–973 [View Article][PubMed]
     [Google Scholar]
  31. Premaratne R. J., Lin W. J., Johnson E. A.( 1991). Development of an improved chemically defined minimal medium for Listeria monocytogenes. Appl Environ Microbiol 57:3046–3048[PubMed]
     [Google Scholar]
  32. Raengpradub S., Wiedmann M., Boor K. J.( 2008). Comparative analysis of the sigma B-dependent stress responses in Listeria monocytogenes and Listeria innocua strains exposed to selected stress conditions. Appl Environ Microbiol 74:158–171 [View Article][PubMed]
     [Google Scholar]
  33. Sherman E. M., Esquiaqui J., Elsayed G., Ye J. D.( 2012). An energetically beneficial leader-linker interaction abolishes ligand-binding cooperativity in glycine riboswitches. RNA 18:496–507 [View Article][PubMed]
     [Google Scholar]
  34. Sleator R. D., Wemekamp-Kamphuis H. H., Gahan C. G., Abee T., Hill C.( 2005). A PrfA-regulated bile exclusion system (BilE) is a novel virulence factor in Listeria monocytogenes. Mol Microbiol 55:1183–1195 [View Article][PubMed]
     [Google Scholar]
  35. Stauffer G. V.( 1996). Biosynthesis of serine, glycine, and one-carbon units. Escherichia Coli and Salmonella: Cellular and Molecular Biology506–513 Neidhardt F. C., Curtiss R. III, Ingraham J. L., Lin E. C. C., Low K. B., Magasanik B., Reznikoff W. S., Riley M., Schaechter M., Umbarger H. E. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  36. Sue D., Boor K. J., Wiedmann M.( 2003). σB-dependent expression patterns of compatible solute transporter genes opuCA and lmo1421 and the conjugated bile salt hydrolase gene bsh in Listeria monocytogenes. Microbiology 149:3247–3256 [View Article][PubMed]
     [Google Scholar]
  37. Toledo-Arana A., Dussurget O., Nikitas G., Sesto N., Guet-Revillet H., Balestrino D., Loh E., Gripenland J., Tiensuu T.& other authors ( 2009). The Listeria transcriptional landscape from saprophytism to virulence. Nature 459:950–956 [View Article][PubMed]
     [Google Scholar]
  38. van Schaik W., Abee T.( 2005). The role of σB in the stress response of Gram-positive bacteria – targets for food preservation and safety. Curr Opin Biotechnol 16:218–224 [View Article][PubMed]
     [Google Scholar]
  39. Ward T. J., Ducey T. F., Usgaard T., Dunn K. A., Bielawski J. P.( 2008). Multilocus genotyping assays for single nucleotide polymorphism-based subtyping of Listeria monocytogenes isolates. Appl Environ Microbiol 74:7629–7642 [View Article][PubMed]
     [Google Scholar]
  40. Wiedmann M., Arvik T. J., Hurley R. J., Boor K. J.( 1998). General stress transcription factor sigmaB and its role in acid tolerance and virulence of Listeria monocytogenes. J Bacteriol 180:3650–3656[PubMed]
     [Google Scholar]
  41. Williams T., Joseph B., Beier D., Goebel W., Kuhn M.( 2005). Response regulator DegU of Listeria monocytogenes regulates the expression of flagella-specific genes. FEMS Microbiol Lett 252:287–298 [View Article][PubMed]
     [Google Scholar]
  42. Zhang W., Li F., Nie L.( 2010). Integrating multiple ‘omics’ analysis for microbial biology: application and methodologies. Microbiology 156:287–301 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.066001-0
Loading
Refinement of the Listeria monocytogenes σB regulon through quantitative proteomic analysis
Microbiology 159, 1109 (2013); https://doi.org/10.1099/mic.0.066001-0
/content/journal/micro/10.1099/mic.0.066001-0
/content/journal/micro/10.1099/mic.0.066001-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error