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Volume 152, Issue 10

Different subcellular locations of secretome components of Gram-positive bacteria Free

Abstract

Gram-positive bacteria contain different types of secretion systems for the transport of proteins into or across the cytoplasmic membrane. Recent studies on subcellular localization of specific components of these secretion systems and their substrates have shown that they can be present at various locations in the cell. The translocons of the general Sec secretion system in the rod-shaped bacterium have been shown to localize in spirals along the cytoplasmic membrane, whereas the translocons in the coccoid are located in a microdomain near the septum. In both bacteria the Sec translocons appear to be located near the sites of cell wall synthesis. The Tat secretion system, which is used for the transport of folded proteins, probably localizes in the cytoplasmic membrane and at the cell poles of . In the ABC transporter dedicated to the transport of a small antimicrobial peptide is distributed throughout the membrane. Possible mechanisms for maintaining the localization of these secretion machineries involve their interaction with proteins of the cytoskeleton or components of the cell wall synthesis machinery, or the presence of lipid subdomains surrounding the transport systems.

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2006-10-01
2024-04-19
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References

  1. Berthelmann F, Brüser T. 2004; Localization of the Tat translocon components in Escherichia coli . FEBS Lett 569:82–88 [CrossRef]
     [Google Scholar]
  2. Binenbaum Z, Parola A. H, Zaritsky A, Fishov I. 1999; Transcription- and translation-dependent changes in membrane dynamics in bacteria: testing the transertion model for domain formation. Mol Microbiol 32:1173–1182 [CrossRef]
     [Google Scholar]
  3. Blaylock B, Jiang X, Rubio A, Pogliano K, Moran C. P. Jr 2004; Zipper-like interaction between proteins in adjacent daughter cells mediates protein localization. Genes Dev 18:2916–2928 [CrossRef]
     [Google Scholar]
  4. Buist G, Kok J, Leenhouts K. J, Dabrowska M, Venema G, Haandrikman A. J. 1995; Molecular cloning and nucleotide sequence of the gene encoding the major peptidoglycan hydrolase of Lactococcus lactis , a muramidase needed for cell separation. J Bacteriol 177:1554–1563
     [Google Scholar]
  5. Calamita H. G, Doyle R. J. 2002; Regulation of autolysins in teichuronic acid-containing Bacillus subtilis cells. Mol Microbiol 44:601–606 [CrossRef]
     [Google Scholar]
  6. Campo N, Tjalsma H, Buist G. 7 other authors 2004; Subcellular sites for bacterial protein export. Mol Microbiol 53:1583–1599 [CrossRef]
     [Google Scholar]
  7. Cole R. M, Hahn J. J. 1962; Cell wall replication in Streptococcus pyogenes . Science 135:722–724 [CrossRef]
     [Google Scholar]
  8. Comfort D, Clubb R. T. 2004; A comparative genome analysis identifies distinct sorting pathways in gram-positive bacteria. Infect Immun 72:2710–2722 [CrossRef]
     [Google Scholar]
  9. Daniel R. A, Errington J. 2003; Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113:767–776 [CrossRef]
     [Google Scholar]
  10. Demchick P, Koch A. L. 1996; The permeability of the wall fabric of Escherichia coli and Bacillus subtilis . J Bacteriol 178:768–773
     [Google Scholar]
  11. Fishov I, Woldringh C. L. 1999; Visualization of membrane domains in Escherichia coli . Mol Microbiol 32:1166–1172 [CrossRef]
     [Google Scholar]
  12. Gajic O, Buist G, Kojic M, Topisirovic L, Kuipers O. P, Kok J. 2003; Novel mechanism of bacteriocin secretion and immunity carried out by lactococcal multidrug resistance proteins. J Biol Chem 278:34291–34298 [CrossRef]
     [Google Scholar]
  13. Giepmans B. N, Adams S. R, Ellisman M. H, Tsien R. Y. 2006; The fluorescent toolbox for assessing protein location and function. Science 312:217–224 [CrossRef]
     [Google Scholar]
  14. Hyyrylainen H. L, Vitikainen M, Thwaite J, Wu H, Sarvas M, Harwood C. R, Kontinen V. P, Stephenson K. 2000; d-Alanine substitution of teichoic acids as a modulator of protein folding and stability at the cytoplasmic membrane/cell wall interface of Bacillus subtilis . J Biol Chem 275:26696–26703
     [Google Scholar]
  15. Johnson A. S, Lewis P. J, van Horck S. 2004; Dynamic localization of membrane proteins in Bacillus subtilis . Microbiology 150:2815–2824 [CrossRef]
     [Google Scholar]
  16. Jones L. J, Carballido-Lopez R, Errington J. 2001; Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis . Cell 104:913–922 [CrossRef]
     [Google Scholar]
  17. Kawai F, Shoda M, Harashima R, Sadaie Y, Hara H, Matsumoto K. 2004; Cardiolipin domains in Bacillus subtilis Marburg membranes. J Bacteriol 186:1475–1483 [CrossRef]
     [Google Scholar]
  18. Kirby J. R, Niewold T. B, Maloy S, Ordal G. W. 2000; CheB is required for behavioural responses to negative stimuli during chemotaxis in Bacillus subtilis . Mol Microbiol 35:44–57 [CrossRef]
     [Google Scholar]
  19. Lamanna A. C, Ordal G. W, Kiessling L. L. 2005; Large increases in attractant concentration disrupt the polar localization of bacterial chemoreceptors. Mol Microbiol 57:774–7785 [CrossRef]
     [Google Scholar]
  20. Leenhouts K, Buist G, Kok J. 1999; Anchoring of proteins to lactic acid bacteria. Antonie Van Leeuwenhoek 76:367–376 [CrossRef]
     [Google Scholar]
  21. Lorenz H, Hailey D. W, Lippincott-Schwartz J. 2006; Fluorescence protease protection of GFP chimeras to reveal protein topology and subcellular localization. Nat Methods 3:205–210 [CrossRef]
     [Google Scholar]
  22. Matias V. R, Beveridge T. J. 2005; Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol Microbiol 56:240–251 [CrossRef]
     [Google Scholar]
  23. Meile J. C, Wu L. J, Ehrlich S. D, Errington J, Noirot P. 2006; Systematic localisation of proteins fused to the green fluorescent protein in Bacillus subtilis : identification of new proteins at the DNA replication factory. Proteomics 6:2135–2146 [CrossRef]
     [Google Scholar]
  24. Merchante R, Pooley H. M, Karamata D. 1995; A periplasm in Bacillus subtilis . J Bacteriol 177:6176–6183
     [Google Scholar]
  25. Murakami T, Haga K, Takeuchi M, Sato T. 2002; Analysis of the Bacillus subtilis spoIIIJ gene and its paralogue gene, yqjG . J Bacteriol 184:1998–2004 [CrossRef]
     [Google Scholar]
  26. Narita J, Okano K, Kitao T, Ishida S, Sewaki T, Sung M. H, Fukuda H, Kondo A. 2006; Display of α -amylase on the surface of Lactobacillus casei cells by use of the PgsA anchor protein, and production of lactic acid from starch. Appl Environ Microbiol 72:269–275 [CrossRef]
     [Google Scholar]
  27. Navarre W. W, Schneewind O. 1999; Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63:174–229
     [Google Scholar]
  28. Nguyen H. D, Schumann W. 2005; Establishment of an experimental system allowing immobilization of proteins on the surface of Bacillus subtilis cells. J Biotechnol 122:473–482
     [Google Scholar]
  29. Nishibori A, Kusaka J, Hara H, Umeda M, Matsumoto K. 2005; Phosphatidylethanolamine domains and localization of phospholipid synthases in Bacillus subtilis membranes. J Bacteriol 187:2163–2174 [CrossRef]
     [Google Scholar]
  30. Nouaille S, Commissaire J, Gratadoux J. J, Ravn P, Bolotin A, Gruss A, Le Loir Y, Langella P. 2004; Influence of lipoteichoic acid d-alanylation on protein secretion in Lactococcus lactis as revealed by random mutagenesis. Appl Environ Microbiol 70:1600–1607 [CrossRef]
     [Google Scholar]
  31. Pallen M. J. 2002; The ESAT-6/WXG100 superfamily – and a new Gram-positive secretion system?. Trends Microbiol 10:209–212 [CrossRef]
     [Google Scholar]
  32. Pinho M. G, Errington J. 2003; Dispersed mode of Staphylococcus aureus cell wall synthesis in the absence of the division machinery. Mol Microbiol 50:871–881 [CrossRef]
     [Google Scholar]
  33. Pop O. I, Westermann M, Volkmer-Engert R, Schulz D, Lemke C, Schreiber S, Gerlach R, Wetzker R, Muller J. P. 2003; Sequence-specific binding of prePhoD to soluble TatA[sub]d[/sub] indicates protein-mediated targeting of the Tat export in Bacillus subtilis . J Biol Chem 278:38428–38436 [CrossRef]
     [Google Scholar]
  34. Rafelski S. M, Theriot J. A. 2006; Mechanism of polarization of Listeria monocytogenes surface protein ActA. Mol Microbiol 59:1262–1279 [CrossRef]
     [Google Scholar]
  35. Rao C. V, Kirby J. R, Arkin A. P. 2005; Phosphatase localization in bacterial chemotaxis: divergent mechanisms, convergent principles. Phys Biol 2:148–158 [CrossRef]
     [Google Scholar]
  36. Ray N, Nenninger A, Mullineaux C. W, Robinson C. 2005; Location and mobility of twin arginine translocase subunits in the Escherichia coli plasma membrane. J Biol Chem 280:17961–17968 [CrossRef]
     [Google Scholar]
  37. Rosch J, Caparon M. 2004; A microdomain for protein secretion in Gram-positive bacteria. Science 304:1513–1515 [CrossRef]
     [Google Scholar]
  38. Rosch J. W, Caparon M. G. 2005; The ExPortal: an organelle dedicated to the biogenesis of secreted proteins in Streptococcus pyogenes . Mol Microbiol 58:959–968 [CrossRef]
     [Google Scholar]
  39. Rubio A, Jiang X, Pogliano K. 2005; Localization of translocation complex components in Bacillus subtilis : enrichment of the signal recognition particle receptor at early sporulation septa. J Bacteriol 187:5000–5002 [CrossRef]
     [Google Scholar]
  40. Rudner D. Z, Pan Q, Losick R. M. 2002; Evidence that subcellular localization of a bacterial membrane protein is achieved by diffusion and capture. Proc Natl Acad Sci U S A 99:8701–8706 [CrossRef]
     [Google Scholar]
  41. Sakata N, Terakubo S, Mukai T. 2005; Subcellular location of the soluble lytic transglycosylase homologue in Staphylococcus aureus . Curr Microbiol 50:47–51 [CrossRef]
     [Google Scholar]
  42. Schaffer C, Messner P. 2005; The structure of secondary cell wall polymers: how Gram-positive bacteria stick their cell walls together. Microbiology 151:643–651 [CrossRef]
     [Google Scholar]
  43. Scheffers D. J, Pinho M. G. 2005; Bacterial cell wall synthesis: new insights from localization studies. Microbiol Mol Biol Rev 69:585–607 [CrossRef]
     [Google Scholar]
  44. Scheffers D. J, Jones L. J, Errington J. 2004; Several distinct localization patterns for penicillin-binding proteins in Bacillus subtilis . Mol Microbiol 51:749–764
     [Google Scholar]
  45. Shiomi D, Yoshimoto M, Homma M, Kawagishi I. 2006; Helical distribution of the bacterial chemoreceptor via colocalization with the Sec protein translocation machinery. Mol Microbiol 60:894–906 [CrossRef]
     [Google Scholar]
  46. Steen A, Buist G, Leenhouts K. J, El Khattabi M, Grijpstra F, Zomer A. L, Venema G, Kuipers O. P, Kok J. 2003; Cell wall attachment of a widely distributed peptidoglycan binding domain is hindered by cell wall constituents. J Biol Chem 278:23874–23881 [CrossRef]
     [Google Scholar]
  47. Tiyanon K, Doan T, Lazarus M. B, Fang X, Rudner D. Z, Walker S. 2006; Imaging peptidoglycan biosynthesis in Bacillus subtilis with fluorescent antibiotics. Proc Natl Acad Sci U S A 103:11033–11038 [CrossRef]
     [Google Scholar]
  48. Tjalsma H, Bolhuis A, Jongbloed J. D, Bron S, van Dijl J. M. 2000; Signal peptide-dependent protein transport in Bacillus subtilis : a genome-based survey of the secretome. Microbiol Mol Biol Rev 64:515–547 [CrossRef]
     [Google Scholar]
  49. Tjalsma H, Bron S, van Dijl J. M. 2003; Complementary impact of paralogous Oxa1-like proteins of Bacillus subtilis on post-translocational stages in protein secretion. J Biol Chem 278:15622–15632 [CrossRef]
     [Google Scholar]
  50. Ton-That H, Marraffini L. A, Schneewind O. 2004; Protein sorting to the cell wall envelope of Gram-positive bacteria. Biochim Biophys Acta 1694269–278 [CrossRef]
     [Google Scholar]
  51. Vanounou S, Parola A. H, Fishov I. 2003; Phosphatidylethanolamine and phosphatidylglycerol are segregated into different domains in bacterial membrane. A study with pyrene-labelled phospholipids. Mol Microbiol 49:1067–1079 [CrossRef]
     [Google Scholar]
  52. Wandersman C. 1998; Protein and peptide secretion by ABC exporters. Res Microbiol 149:163–170 [CrossRef]
     [Google Scholar]
  53. Yamada S, Sugai M, Komatsuzawa H, Nakashima S, Oshida T, Matsumoto A, Suginaka H. 1996; An autolysin ring associated with cell separation of Staphylococcus aureus . J Bacteriol 178:1565–1571
     [Google Scholar]
  54. Yamamoto H, Kurosawa S, Sekiguchi J. 2003; Localization of the vegetative cell wall hydrolases LytC, LytE, and LytF on the Bacillus subtilis cell surface and stability of these enzymes to cell wall-bound or extracellular proteases. J Bacteriol 185:6666–6677 [CrossRef]
     [Google Scholar]
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Different subcellular locations of secretome components of Gram-positive bacteria
Microbiology 152, 2867 (2006); https://doi.org/10.1099/mic.0.29113-0
/content/journal/micro/10.1099/mic.0.29113-0
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