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Growth phase-associated changes in the transcriptome and proteome of Streptococcus pyogenes

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Abstract

Streptococcus pyogenes is responsible for approximately 500,000 deaths each year worldwide. Many of the associated virulence factors are expressed in a growth phase-dependent manner. To identify growth phase-associated changes in expression on a genomescale, the exponential and stationary phase transcriptomes and proteomes of S. pyogenes strain NZ131 (serotype M49) were compared by using Affymetrix NimbleExpress gene chips and two-dimensional gel electrophoresis. At the transcript level, the expression of 689 genes, representing approximately 40% of the chromosome, differed by twofold or more between the two growth phases. The majority of transcripts that were more abundant in the early-stationary phase encoded proteins involved in energy conversion, transport, and metabolism. At the protein level, an average of 527 and 403 protein spots were detected in the exponential and stationary phases of growth, respectively. Tandem mass spectrometry was used to identify 172 protein spots, 128 of which were growth phase regulated. Enzymes involved in glycolysis and pyruvate metabolism and several stress-responsive proteins were more abundant in the stationary phase of growth. Overall, the results identified growth phase-regulated genes in strain NZ131 and revealed significant post-transcriptional complexity associated with pathogen adaptation to the stationary phase of growth.

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Abbreviations

THY:

Todd-Hewitt yeast extract broth

2-DE:

Two-dimensional gel electrophoresis

References

  • Barnett TC, Bugrysheva JV, Scott JR (2007) Role of mRNA stability in growth phase regulation of gene expression in the group A streptococcus. J Bacteriol 189:1866–1873

    Article  PubMed  CAS  Google Scholar 

  • Beyer-Sehlmeyer G, Kreikemeyer B, Horster A, Podbielski A (2005) Analysis of the growth phase-associated transcriptome of Streptococcus pyogenes. Int J Med Microbiol 295:161–177

    Article  PubMed  CAS  Google Scholar 

  • Carapetis JR, Steer AC, Mulholland EK, Weber M (2005) The global burden of group A streptococcal diseases. Lancet Infect Dis 5:685–694

    Article  PubMed  Google Scholar 

  • Chaussee MS, Phillips ER, Ferretti JJ (1997) Temporal production of streptococcal erythrogenic toxin B (streptococcal cysteine proteinase) in response to nutrient depletion. Infect Immun 65:1956–1959

    PubMed  CAS  Google Scholar 

  • Chaussee MS, Somerville GA, Reitzer L, Musser JM (2003) Rgg coordinates virulence factor synthesis and metabolism in Streptococcus pyogenes. J Bacteriol 185:6016–6024

    Article  PubMed  CAS  Google Scholar 

  • Chaussee MA, Callegari EA, Chaussee MS (2004) Rgg regulates growth phase-dependent expression of proteins associated with secondary metabolism and stress in Streptococcus pyogenes. J Bacteriol 186:7091–7099

    Article  PubMed  CAS  Google Scholar 

  • Chaussee MA, McDowell EJ, Rieck LD, Callegari EA, Chaussee MS (2006) Proteomic analysis of a penicillin-tolerant rgg mutant strain of Streptococcus pyogenes. J Antimicrob Chemother 58(4):752–759

    Article  PubMed  CAS  Google Scholar 

  • Cunningham MW (2000) Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 13:470–511

    Article  PubMed  CAS  Google Scholar 

  • Davies HD et al (1996) Invasive group A streptococcal infections in Ontario, Canada. Ontario Group A Streptococcal Study Group. N Engl J Med 335:547–554

    Article  PubMed  CAS  Google Scholar 

  • Dmitriev AV, McDowell EJ, Kappeler KV, Chaussee MA, Rieck LD, Chaussee MS (2006) The Rgg regulator of Streptococcus pyogenes influences utilization of nonglucose carbohydrates, prophage induction, and expression of the NAD-glycohydrolase virulence operon. J Bacteriol 188:7230–7241

    Article  PubMed  CAS  Google Scholar 

  • Ferretti JJ et al (2001) Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci USA 98:4658–4663

    Article  PubMed  CAS  Google Scholar 

  • Fisher SH (1999) Regulation of nitrogen metabolism in Bacillus subtilis: vive la difference! Mol Microbiol 32:223–232

    Article  PubMed  CAS  Google Scholar 

  • Folio P, Chavant P, Chafsey I, Belkorchia A, Chambon C, Hebraud M (2004) Two-dimensional electrophoresis database of Listeria monocytogenes EGDe proteome and proteomic analysis of mid-log and stationary growth phase cells. Proteomics 4:3187–3201

    Article  PubMed  CAS  Google Scholar 

  • Giard JC, Rince A, Capiaux H, Auffray Y, Hartke A (2000) Inactivation of the stress- and starvation-inducible gls24 operon has a pleiotrophic effect on cell morphology, stress sensitivity, and gene expression in Enterococcus faecalis. J Bacteriol 182:4512–4520

    Article  PubMed  CAS  Google Scholar 

  • Gibson CM, Mallett TC, Claiborne A, Caparon MG (2000) Contribution of NADH oxidase to aerobic metabolism of Streptococcus pyogenes. J Bacteriol 182:448–455

    Article  PubMed  CAS  Google Scholar 

  • Graham MR et al (2006) Analysis of the transcriptome of group A Streptococcus in mouse soft tissue infection. Am J Pathol 169:927–942

    Article  PubMed  CAS  Google Scholar 

  • Guillot A, Gitton C, Anglade P, Mistou MY (2003) Proteomic analysis of Lactococcus lactis, a lactic acid bacterium. Proteomics 3:337–354

    Article  PubMed  CAS  Google Scholar 

  • Harder W, Dijkhuizen L (1983) Physiological responses to nutrient limitation. Annu Rev Microbiol 37:1–23

    Article  PubMed  CAS  Google Scholar 

  • Helmann JD, Moran CP (2002) RNA polymerases and sigma factors. ASM Press, Washington DC

    Google Scholar 

  • Hew CM, Korakli M, Vogel RF (2006) Expression of virulence-related genes by Enterococcus faecalis in response to different environments. Syst Appl Microbiol 30(4):257–267

    Article  PubMed  Google Scholar 

  • Hua Q, Yang C, Oshima T, Mori H, Shimizu K (2004) Analysis of gene expression in Escherichia coli in response to changes of growth-limiting nutrient in chemostat cultures. Appl Environ Microbiol 70:2354–2366

    Article  PubMed  CAS  Google Scholar 

  • Johansson BP, Levander F, von Pawel-Rammingen U, Berggard T, Bjorck L, James P (2005) The protein expression of Streptococcus pyogenes is significantly influenced by human plasma. J Proteome Res 4:2302–2311

    Article  PubMed  CAS  Google Scholar 

  • Jungblut PR et al (2000) Comparative proteome analysis of Helicobacter pylori. Mol Microbiol 36:710–725

    Article  PubMed  CAS  Google Scholar 

  • Kang CM, Abbott DW, Park ST, Dascher CC, Cantley LC, Husson RN (2005) The Mycobacterium tuberculosis serine/threonine kinases PknA and PknB: substrate identification and regulation of cell shape. Genes Dev 19:1692–1704

    Article  PubMed  CAS  Google Scholar 

  • Kreikemeyer B, McIver KS, Podbielski A (2003) Virulence factor regulation and regulatory networks in Streptococcus pyogenes and their impact on pathogen-host interactions. Trends Microbiol 11:224–232

    PubMed  CAS  Google Scholar 

  • Lee KJ, Bae SM, Lee MR, Yeon SM, Lee YH, Kim KS (2006) Proteomic analysis of growth phase-dependent proteins of Streptococcus pneumoniae. Proteomics 6:1274–1282

    Article  PubMed  CAS  Google Scholar 

  • Len AC, Harty DW, Jacques NA (2004) Stress-responsive proteins are upregulated in Streptococcus mutans during acid tolerance. Microbiology 150:1339–1351

    Article  PubMed  CAS  Google Scholar 

  • Lithgow JK, Hayhurst EJ, Cohen G, Aharonowitz Y, Foster SJ (2004) Role of a cysteine synthase in Staphylococcus aureus. J Bacteriol 186:1579–1590

    Article  PubMed  CAS  Google Scholar 

  • Lyon WR, Madden JC, Levin JC, Stein JL, Caparon MG (2001) Mutation of luxS affects growth and virulence factor expression in Streptococcus pyogenes. Mol Microbiol 42:145–157

    Article  PubMed  CAS  Google Scholar 

  • Malke H, Steiner K, McShan WM, Ferretti JJ (2006) Linking the nutritional status of Streptococcus pyogenes to alteration of transcriptional gene expression: the action of CodY and RelA. Int J Med Microbiol 296:259–275

    Article  PubMed  CAS  Google Scholar 

  • Neely MN, Lyon WR, Runft DL, Caparon M (2003) Role of RopB in growth phase expression of the SpeB cysteine protease of Streptococcus pyogenes. J Bacteriol 185:5166–5174

    Article  PubMed  CAS  Google Scholar 

  • Neijssel OM, Snoep JL, Teixeira de Mattos MJ (1997) Regulation of energy source metabolism in streptococci. Soc Appl Bacteriol Symp Ser 26:12S-19S

    PubMed  CAS  Google Scholar 

  • Neuner JM, Hamel MB, Phillips RS, Bona K, Aronson MD (2003) Diagnosis and management of adults with pharyngitis. A cost-effectiveness analysis. Ann Intern Med 139:113–122

    PubMed  Google Scholar 

  • Reva ON et al (2006) Functional genomics of stress response in Pseudomonas putida KT2440. J Bacteriol 188:4079–4092

    Article  PubMed  CAS  Google Scholar 

  • Shelburne SA 3rd, Sumby P, Sitkiewicz I, Granville C, DeLeo FR, Musser JM (2005) Central role of a bacterial two-component gene regulatory system of previously unknown function in pathogen persistence in human saliva. Proc Natl Acad Sci USA 102:16037–16042

    Article  PubMed  CAS  Google Scholar 

  • Steiner K, Malke H (2000) Life in protein-rich environments: the relA-independent response of Streptococcus pyogenes to amino acid starvation. Mol Microbiol 38:1004–1016

    Article  PubMed  CAS  Google Scholar 

  • Voyich JM et al (2003) Genome-wide protective response used by group A Streptococcus to evade destruction by human polymorphonuclear leukocytes. Proc Natl Acad Sci USA 100:1996–2001

    Article  PubMed  CAS  Google Scholar 

  • Wick LM, Quadroni M, Egli T (2001) Short- and long-term changes in proteome composition and kinetic properties in a culture of Escherichia coli during transition from glucose-excess to glucose-limited growth conditions in continuous culture and vice versa. Environ Microbiol 3:588–599

    Article  PubMed  CAS  Google Scholar 

  • Wilkins JC, Homer KA, Beighton D (2002) Analysis of Streptococcus mutans proteins modulated by culture under acidic conditions. Appl Environ Microbiol 68:2382–2390

    Article  PubMed  CAS  Google Scholar 

  • Woodbury RL, Wang X, Moran CP Jr (2006) Sigma X induces competence gene expression in Streptococcus pyogenes. Res Microbiol 157:851–856

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Emily McDowell for completing the quantitative RT-PCR assays. This work was supported by NIAID/NIH grant RO1 AIO52147 to M.S.C and NIH Grant Number 2 P20 RR016479 from the INBRE Program of the National Center for Research Resources.

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Authors and Affiliations

  1. Division of Basic Biomedical Sciences, The Sanford School of Medicine of the University of South Dakota, Lee Medical Building, 414 East Clark Street, Vermillion, SD, 57069-2390, USA

    Michelle A. Chaussee, Alexander V. Dmitriev, Eduardo A. Callegari & Michael S. Chaussee

  2. Department of Molecular Microbiology, Institute of Experimental Medicine, Saint-Petersburg, Russia

    Alexander V. Dmitriev

Authors
  1. Michelle A. Chaussee
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  2. Alexander V. Dmitriev
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  3. Eduardo A. Callegari
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  4. Michael S. Chaussee
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Correspondence to Michael S. Chaussee.

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Communicated by Erko Stackebrandt.

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Chaussee, M.A., Dmitriev, A.V., Callegari, E.A. et al. Growth phase-associated changes in the transcriptome and proteome of Streptococcus pyogenes . Arch Microbiol 189, 27–41 (2008). https://doi.org/10.1007/s00203-007-0290-1

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  • DOI: https://doi.org/10.1007/s00203-007-0290-1

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