Advertisement

Current Microbiology

, Volume 65, Issue 1, pp 35–43 | Cite as

Carbon Catabolite Control is Important for Listeria monocytogenes Biofilm Formation in Response to Nutrient Availability

  • Qingchun Zhou
  • Xiaoqin Feng
  • Qiang Zhang
  • Feifei Feng
  • Xiaojiao Yin
  • Junli Shang
  • Huiping Qu
  • Qin LuoEmail author
Article

Abstract

The foodborne pathogen Listeria monocytogenes has the ability to develop biofilm in food-processing environment, which becomes a major concern for the food safety. The biofilm formation is strongly influenced by the availability of nutrients and environmental conditions, and particularly enhanced in poor minimal essential medium (MEM) containing glucose rather than in rich brain heart infusion (BHI) broth. To gain better insight into the conserved protein expression profile in these biofilms, the proteomes from biofilm- and planktonic-grown cells from MEM with 50 mM glucose or BHI were compared using two-dimensional polyacrylamide gel electrophoresis followed by MALDI-TOF/TOF analysis. 47 proteins were successfully identified to be either up (19 proteins) or down (28 proteins) regulated in the biofilm states. Most (30 proteins) of them were assigned to the metabolism functional category in cluster of orthologous groups of proteins. Among them, up-regulated proteins were mainly associated with the pentose phosphate pathway and glycolysis, whereas a key enzyme CitC involved in tricarboxylic acid cycle was down-regulated in biofilms compared to the planktonic states. These data implicate the importance of carbon catabolite control for L. monocytogenes biofilm formation in response to nutrient availability.

Keywords

Minimal Essential Medium Pentose Phosphate Pathway Brain Heart Infusion Brain Heart Infusion Broth Planktonic State 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was funded by the National Natural Science Foundation of China (30970111), Excellent Youth Foundation of Hubei Scientific Committee (No. 2009CDA124) and CCNU Project (No. CCNU09Y01001).

References

  1. 1.
    Behari J, Youngman P (1998) A homolog of CcpA mediates catabolite control in Listeria monocytogenes but not carbon source regulation of virulence genes. J Bacteriol 180:6316–6324PubMedGoogle Scholar
  2. 2.
    Chandra H, Basir S, Gupta M, Banerjee N (2010) Glutamine synthetase encoded by glnA-1 is necessary for cell wall resistance and pathogenicity of Mycobacterium bovis. Microbiology 156:3669–3677PubMedCrossRefGoogle Scholar
  3. 3.
    Chang Y, Gu W, Fischer N, McLandsborough L (2012) Identification of genes involved in Listeria monocytogenes biofilm formation by mariner-based transposon mutagenesis. Appl Microbiol Biotechnol 93(5):2051–2062PubMedCrossRefGoogle Scholar
  4. 4.
    Djordjevic D, Wiedmann M, McLandsborough L (2002) Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl Environ Microbiol 68:2950–2958PubMedCrossRefGoogle Scholar
  5. 5.
    Dumas E, Desvaux M, Chambon C, Hébraud M (2009) Insight into the core and variant exoproteomes of Listeria monocytogenes species by comparative subproteomic analysis. Proteomics 9:3136–3155PubMedCrossRefGoogle Scholar
  6. 6.
    Fujita Y (2009) Carbon catabolite control of the metabolic network in Bacillus subtilis. Biosci Biotechnol Biochem 73:245–259PubMedCrossRefGoogle Scholar
  7. 7.
    Gandhi M, Chikindas M (2007) Listeria: a foodborne pathogen that knows how to survive. Int J Food Microbiol 113:1–15PubMedCrossRefGoogle Scholar
  8. 8.
    Helloin E, Jansch L, Phan-Thanh L (2003) Carbon starvation survival of Listeria monocytogenes in planktonic state and in biofilm: a proteomic study. Proteomics 3:2052–2064PubMedCrossRefGoogle Scholar
  9. 9.
    Lemon K, Higgins D, Kolter R (2007) Flagellar motility is critical for Listeria monocytogenes biofilm formation. J Bacteriol 189:4418–4424PubMedCrossRefGoogle Scholar
  10. 10.
    Mertins S, Joseph B, Goetz M, Ecke R, Seidel G, Sprehe M, Hillen W, Goebel W, Müller-Altrock S (2007) Interference of components of the phosphoenolpyruvate phosphotransferase system with the central virulence gene regulator PrfA of Listeria monocytogenes. J Bacteriol 189:473–490PubMedCrossRefGoogle Scholar
  11. 11.
    Nguyen P, Abranches J, Phan T, Marquis R (2002) Repressed respiration of oral streptococci grown in biofilms. Curr Microbiol 44:262–266PubMedCrossRefGoogle Scholar
  12. 12.
    O’Toole G, Kaplan H, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79PubMedCrossRefGoogle Scholar
  13. 13.
    Premaratne R, Lin W, Johnson E (1991) Development of an improved chemically defined minimal medium for Listeria monocytogenes. Appl Environ Microbiol 57:3046–3048PubMedGoogle Scholar
  14. 14.
    Resch A, Leicht S, Saric M, Pásztor L, Jakob A, Götz F, Nordheim A (2006) Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling. Proteomics 6:1867–1877PubMedCrossRefGoogle Scholar
  15. 15.
    Riedel C, Monk I, Casey P, Waidmann M, Gahan C, Hill C (2009) AgrD-dependent quorum sensing affects biofilm formation, invasion, virulence and global gene expression profiles in Listeria monocytogenes. Mol Microbiol 71:1177–1189PubMedCrossRefGoogle Scholar
  16. 16.
    Sadykov M, Hartmann T, Mattes T, Hiatt M, Jann N, Zhu Y, Ledala N, Landmann R, Herrmann M, Rohde H, Bischoff M, Somerville G (2011) CcpA coordinates central metabolism and biofilm formation in Staphylococcus epidermidis. Microbiology 157:3458–3468PubMedCrossRefGoogle Scholar
  17. 17.
    Seidl K, Goerke C, Wolz C, Mack D, Berger-Bächi B, Bischoff M (2008) Staphylococcus aureus CcpA affects biofilm formation. Infect Immun 76:2044–2050PubMedCrossRefGoogle Scholar
  18. 18.
    Stoll R, Mertins S, Joseph B, Müller-Altrock S, Goebel W (2008) Modulation of PrfA activity in Listeria monocytogenes upon growth in different culture media. Microbiology 154:3856–3876PubMedCrossRefGoogle Scholar
  19. 19.
    Todhanakasem T, Young G (2008) Loss of flagellar-based motility by Listeria monocytogenes results in the formation of hyperbiofilms. J Bacteriol 190:6030–6034PubMedCrossRefGoogle Scholar
  20. 20.
    Tsai H, Hodgson D (2003) Development of a synthetic minimal medium for Listeria monocytogenes. Appl Environ Microbiol 69:6943–6945PubMedCrossRefGoogle Scholar
  21. 21.
    Ueda A, Attila C, Whiteley M, Wood T (2009) Uracil influences quorum sensing and biofilm formation in Pseudomonas aeruginosa and fluorouracil is an antagonist. Microb Biotechnol 2:62–74PubMedCrossRefGoogle Scholar
  22. 22.
    Yamazaki Y, Danelishvili L, Wu M, Macnab M, Bermudez L (2006) Mycobacterium avium genes associated with the ability to form a biofilm. Appl Environ Microbiol 72:819–825PubMedCrossRefGoogle Scholar
  23. 23.
    Zhou Q, Feng F, Wang L, Feng X, Yin X, Luo Q (2011) Virulence regulator PrfA is essential for biofilm formation in Listeria monocytogenes but not in Listeria innocua. Curr Microbiol 63:186–192PubMedCrossRefGoogle Scholar
  24. 24.
    Zhu Y, Xiong Y, Sadykov M, Fey P, Lei M, Lee C, Bayer A, Somerville G (2009) Tricarboxylic acid cycle-dependent attenuation of Staphylococcus aureus in vivo virulence by selective inhibition of amino acid transport. Infect Immun 77:4256–4264PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Qingchun Zhou
    • 1
  • Xiaoqin Feng
    • 1
  • Qiang Zhang
    • 1
  • Feifei Feng
    • 1
  • Xiaojiao Yin
    • 1
  • Junli Shang
    • 1
  • Huiping Qu
    • 1
  • Qin Luo
    • 1
    Email author
  1. 1.Hubei Key Laboratory of Genetic Regulation and Integrative Biology, College of Life ScienceCentral China Normal UniversityWuhanPeople’s Republic of China

Personalised recommendations