1887

Abstract

Many bacteria use the chaperone–usher (CU) secretion pathway to assemble on their surfaces typical or atypical fimbrial organelles. Four consecutive genes of DK1622, MXAN3885–3882, were predicted to constitute an operon encoding a CU-like system involved in the assembly of the spore coat; however, experimental evidence supporting this hypothesis was lacking. In this study, co-transcription of MXAN3885–3883 was verified, and we found that this operon was expressed 12–15 h after initiation of development under conditions of stringent starvation. The MXAN3885 protein, which is highly homologous to, but expressed earlier than, the spore coat protein U of another strain, DZF1, was present mainly on the outer surface of myxospores. Inactivation of MXAN3883, encoding a putative outer membrane usher, inhibited assembly of MXAN3885 protein on spore surfaces and caused certain morphological alterations in the spore coat. Hence, the CU-like pathway in indeed functions in spore coat biogenesis. Based on chaperone amino acid sequence comparisons, our analysis suggests that the structural basis of the CU-like pathway for spore coat assembly may be different from that of most surface structures assembled by classical CU systems.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.047134-0
2011-07-01
2020-07-03
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/7/1886.html?itemId=/content/journal/micro/10.1099/mic.0.047134-0&mimeType=html&fmt=ahah

References

  1. Dahl J. L., Tengra F. K., Dutton D., Yan J., Andacht T. M., Coyne L., Windell V., Garza A. G..( 2007;). Identification of major sporulation proteins of Myxococcus xanthus using a proteomic approach. J Bacteriol189:3187–3197 [CrossRef][PubMed]
    [Google Scholar]
  2. Downard J. S., Zusman D. R..( 1985;). Differential expression of protein S genes during Myxococcus xanthus development. J Bacteriol161:1146–1155[PubMed]
    [Google Scholar]
  3. Dworkin M..( 1996;). Recent advances in the social and developmental biology of the myxobacteria. Microbiol Rev60:70–102[PubMed]
    [Google Scholar]
  4. Emanuelsson O., Brunak S., von Heijne G., Nielsen H..( 2007;). Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc2:953–971 [CrossRef][PubMed]
    [Google Scholar]
  5. Furuichi T., Komano T., Inouye M., Inouye S..( 1985;). Functional complementation between the two homologous genes, ops and tps, during differentiation of Myxococcus xanthus. Mol Gen Genet199:434–439 [CrossRef][PubMed]
    [Google Scholar]
  6. Gollop R., Inouye M., Inouye S..( 1991;). Protein U, a late-developmental spore coat protein of Myxococcus xanthus, is a secretory protein. J Bacteriol173:3597–3600[PubMed]
    [Google Scholar]
  7. Gorski L., Kaiser D..( 1998;). Targeted mutagenesis of sigma54 activator proteins in Myxococcus xanthus. J Bacteriol180:5896–5905[PubMed]
    [Google Scholar]
  8. Hodgkin J., Kaiser D..( 1979;). Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): two gene systems control movement. Mol Gen Genet171:177–191 [CrossRef]
    [Google Scholar]
  9. Hung D. L., Knight S. D., Woods R. M., Pinkner J. S., Hultgren S. J..( 1996;). Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J15:3792–3805[PubMed]
    [Google Scholar]
  10. Inouye M., Inouye S., Zusman D. R..( 1979;a). Gene expression during development of Myxococcus xanthus: pattern of protein synthesis. Dev Biol68:579–591 [CrossRef][PubMed]
    [Google Scholar]
  11. Inouye M., Inouye S., Zusman D. R..( 1979;b). Biosynthesis and self-assembly of protein S, a development-specific protein of Myxococcus xanthus. Proc Natl Acad Sci U S A76:209–213 [CrossRef][PubMed]
    [Google Scholar]
  12. Kashefi K., Hartzell P. L..( 1995;). Genetic suppression and phenotypic masking of a Myxococcus xanthus frzF defect. Mol Microbiol15:483–494 [CrossRef][PubMed]
    [Google Scholar]
  13. Klemm P., Christiansen G..( 1990;). The fimD gene required for cell surface localization of Escherichia coli type 1 fimbriae. Mol Gen Genet220:334–338 [CrossRef][PubMed]
    [Google Scholar]
  14. Knight S. D..( 2007;). Structure and assembly of Yersinia pestis F1 antigen. The Genus Yersinia: from Genomics to Function74–87 Perry R. D., Fetherston J. D.. New York: Springer; [CrossRef]
    [Google Scholar]
  15. Kroos L., Kuspa A., Kaiser D. A..( 1986;). A global analysis of developmentally regulated genes in Myxococcus xanthus. Dev Biol117:252–266 [CrossRef][PubMed]
    [Google Scholar]
  16. Kuehn M. J., Ogg D. J., Kihlberg J., Slonim L. N., Flemmer K., Bergfors T., Hultgren S. J..( 1993;). Structural basis of pilus subunit recognition by the PapD chaperone. Science262:1234–1241 [CrossRef][PubMed]
    [Google Scholar]
  17. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A. et al.( 2007;). clustal w and clustal_x version 2. Bioinformatics23:2947–2948 [CrossRef][PubMed]
    [Google Scholar]
  18. McCleary W. R., Esmon B., Zusman D. R..( 1991;). Myxococcus xanthus protein C is a major spore surface protein. J Bacteriol173:2141–2145[PubMed]
    [Google Scholar]
  19. Norgren M., Båga M., Tennent J. M., Normark S..( 1987;). Nucleotide sequence, regulation and functional analysis of the papC gene required for cell surface localization of Pap pili of uropathogenic Escherichia coli. Mol Microbiol1:169–178 [CrossRef][PubMed]
    [Google Scholar]
  20. Nuccio S. P., Bäumler A. J..( 2007;). Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev71:551–575 [CrossRef][PubMed]
    [Google Scholar]
  21. Poole S. T., McVeigh A. L., Anantha R. P., Lee L. H., Akay Y. M., Pontzer E. A., Scott D. A., Bullitt E., Savarino S. J..( 2007;). Donor strand complementation governs intersubunit interaction of fimbriae of the alternate chaperone pathway. Mol Microbiol63:1372–1384 [CrossRef][PubMed]
    [Google Scholar]
  22. Saier M. H. Jr.( 2006;). Protein secretion and membrane insertion systems in Gram-negative bacteria. J Membr Biol214:75–90 [CrossRef][PubMed]
    [Google Scholar]
  23. Sauer F. G., Remaut H., Hultgren S. J., Waksman G..( 2004;). Fiber assembly by the chaperone–usher pathway. Biochim Biophys Acta1694:259–267 [CrossRef][PubMed]
    [Google Scholar]
  24. Shi W., Sun H..( 2002;). Type IV pilus-dependent motility and its possible role in bacterial pathogenesis. Infect Immun70:1–4 [CrossRef][PubMed]
    [Google Scholar]
  25. Søgaard-Andersen L., Overgaard M., Lobedanz S., Ellehauge E., Jelsbak L., Rasmussen A. A..( 2003;). Coupling gene expression and multicellular morphogenesis during fruiting body formation in Myxococcus xanthus. Mol Microbiol48:1–8 [CrossRef][PubMed]
    [Google Scholar]
  26. Spaink H. P., Okker R. J. H., Wijffelman C. A., Pees E., Lugtenberg B. J. J..( 1987;). Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Plant Mol Biol9:27–39 [CrossRef]
    [Google Scholar]
  27. Teintze M., Thomas R., Furuichi T., Inouye M., Inouye S..( 1985;). Two homologous genes coding for spore-specific proteins are expressed at different times during development of Myxococcus xanthus. J Bacteriol163:121–125[PubMed]
    [Google Scholar]
  28. Waksman G., Hultgren S. J..( 2009;). Structural biology of the chaperone–usher pathway of pilus biogenesis. Nat Rev Microbiol7:765–774 [CrossRef][PubMed]
    [Google Scholar]
  29. Wall D., Kolenbrander P. E., Kaiser D..( 1999;). The Myxococcus xanthus pilQ (sglA) gene encodes a secretin homolog required for type IV pilus biogenesis, social motility, and development. J Bacteriol181:24–33[PubMed]
    [Google Scholar]
  30. Zavialov A. V., Kersley J., Korpela T., Zav'yalov V. P., MacIntyre S., Knight S. D..( 2002;). Donor strand complementation mechanism in the biogenesis of non-pilus systems. Mol Microbiol45:983–995 [CrossRef][PubMed]
    [Google Scholar]
  31. Zavialov A. V., Berglund J., Pudney A. F., Fooks L. J., Ibrahim T. M., MacIntyre S., Knight S. D..( 2003;). Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell113:587–596 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.047134-0
Loading
/content/journal/micro/10.1099/mic.0.047134-0
Loading

Data & Media loading...

Most cited this month 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