1887

Abstract

Efflux pumps export a wide variety of proteinaceous and non-proteinaceous substrates across the Gram-negative cell wall. For the filamentous cyanobacterium sp. strain PCC 7120, the ATP-driven glycolipid efflux pump DevBCA–TolC has been shown to be crucial for the differentiation of N-fixing heterocysts from photosynthetically active vegetative cells. In this study, a homologous system was described. All0809/8/7–TolC form a typical ATP-driven efflux pump as shown by surface plasmon resonance. This putative exporter is also involved in diazotrophic growth of sp. PCC 7120. A mutant in encoding the periplasmic membrane fusion protein of the pump was not able to grow without combined nitrogen. Although heterocysts of this mutant were not distinguishable from those of the wild-type in light and electron micrographs, they were impaired in providing the microoxic environment necessary for N fixation. RT-PCR of transcripts and localization studies on All0807–GFP revealed that All0809/8/7 was initially downregulated during heterocyst maturation and upregulated at later stages of heterocyst formation in all cells of the filament. A substrate of the efflux pump could not be identified in ATP hydrolysis assays. We discuss a role for All0809/8/7–TolC in maintaining the continuous periplasm and how this would be of special importance for heterocyst differentiation.

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2012-10-01
2024-10-04
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References

  1. Black T. A., Cai Y., Wolk C. P. ( 1993). Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena . Mol Microbiol 9:77–84 [View Article][PubMed]
    [Google Scholar]
  2. Black K., Buikema W. J., Haselkorn R. ( 1995). The hglK gene is required for localization of heterocyst-specific glycolipids in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 177:6440–6448 [View Article][PubMed]
    [Google Scholar]
  3. Blight M. A., Holland I. B. ( 1990). Structure and function of haemolysin B, P-glycoprotein and other members of a novel family of membrane translocators. Mol Microbiol 4:873–880 [View Article][PubMed]
    [Google Scholar]
  4. Cai Y. P., Wolk C. P. ( 1990). Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences. J Bacteriol 172:3138–3145[PubMed]
    [Google Scholar]
  5. Davidson R. C., Blankenship J. R., Kraus P. R., de Jesus Berrios M., Hull C. M., D’Souza C., Wang P., Heitman J. ( 2002). A PCR-based strategy to generate integrative targeting alleles with large regions of homology. Microbiology 148:2607–2615[PubMed]
    [Google Scholar]
  6. Elhai J., Wolk C. P. ( 1988a). Conjugal transfer of DNA to cyanobacteria. Methods Enzymol 167:747–754[PubMed]
    [Google Scholar]
  7. Elhai J., Wolk C. P. ( 1988b). A versatile class of positive-selection vectors based on the nonviability of palindrome-containing plasmids that allows cloning into long polylinkers. Gene 68:119–138 [View Article][PubMed]
    [Google Scholar]
  8. Fan Q., Huang G., Lechno-Yossef S., Wolk C. P., Kaneko T., Tabata S. ( 2005). Clustered genes required for synthesis and deposition of envelope glycolipids in Anabaena sp. strain PCC 7120. Mol Microbiol 58:227–243 [View Article][PubMed]
    [Google Scholar]
  9. Fay P., Kulasooriya S. A. ( 1972). Tetrazolium reduction and nitrogenase activity in heterocystous blue-green algae. Arch Mikrobiol 87:341–352 [View Article][PubMed]
    [Google Scholar]
  10. Fiedler G., Arnold M., Hannus S., Maldener I. ( 1998). The DevBCA exporter is essential for envelope formation in heterocysts of the cyanobacterium Anabaena sp. strain PCC 7120. Mol Microbiol 27:1193–1202 [View Article][PubMed]
    [Google Scholar]
  11. Fiedler G., Muro-Pastor A. M., Flores E., Maldener I. ( 2001). NtcA-dependent expression of the devBCA operon, encoding a heterocyst-specific ATP-binding cassette transporter in Anabaena spp. J Bacteriol 183:3795–3799 [View Article][PubMed]
    [Google Scholar]
  12. Flores E., Herrero A. ( 2010). Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat Rev Microbiol 8:39–50 [View Article][PubMed]
    [Google Scholar]
  13. Flores E., Herrero A., Wolk C. P., Maldener I. ( 2006). Is the periplasm continuous in filamentous multicellular cyanobacteria?. Trends Microbiol 14:439–443 [View Article][PubMed]
    [Google Scholar]
  14. Fokina O., Chellamuthu V. R., Zeth K., Forchhammer K. ( 2010). A novel signal transduction protein P(II) variant from Synechococcus elongatus PCC 7942 indicates a two-step process for NAGK–P(II) complex formation. J Mol Biol 399:410–421 [View Article][PubMed]
    [Google Scholar]
  15. Kim H. M., Xu Y., Lee M., Piao S., Sim S. H., Ha N. C., Lee K. ( 2010). Functional relationships between the AcrA hairpin tip region and the TolC aperture tip region for the formation of the bacterial tripartite efflux pump AcrAB-TolC. J Bacteriol 192:4498–4503 [View Article][PubMed]
    [Google Scholar]
  16. Kobayashi N., Nishino K., Yamaguchi A. ( 2001). Novel macrolide-specific ABC-type efflux transporter in Escherichia coli . J Bacteriol 183:5639–5644 [View Article][PubMed]
    [Google Scholar]
  17. Kumar K., Mella-Herrera R. A., Golden J. W. ( 2010). Cyanobacterial heterocysts. Cold Spring Harb Perspect Biol 2:a000315 [View Article][PubMed]
    [Google Scholar]
  18. Lau S. Y., Zgurskaya H. I. ( 2005). Cell division defects in Escherichia coli deficient in the multidrug efflux transporter AcrEF-TolC. J Bacteriol 187:7815–7825 [View Article][PubMed]
    [Google Scholar]
  19. Lázaro S., Fernández-Piñas F., Fernández-Valiente E., Blanco-Rivero A., Leganés F. ( 2001). pbpB, a gene coding for a putative penicillin-binding protein, is required for aerobic nitrogen fixation in the cyanobacterium Anabaena sp. strain PCC7120. J Bacteriol 183:628–636 [View Article][PubMed]
    [Google Scholar]
  20. Lehner J., Zhang Y., Berendt S., Rasse T. M., Forchhammer K., Maldener I. ( 2011). The morphogene AmiC2 is pivotal for multicellular development in the cyanobacterium Nostoc punctiforme . Mol Microbiol 79:1655–1669 [View Article][PubMed]
    [Google Scholar]
  21. Maldener I., Fiedler G., Ernst A., Fernández-Piñas F., Wolk C. P. ( 1994). Characterization of devA, a gene required for the maturation of proheterocysts in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 176:7543–7549[PubMed]
    [Google Scholar]
  22. Maldener I., Hannus S., Kammerer M. ( 2003). Description of five mutants of the cyanobacterium Anabaena sp strain PCC 7120 affected in heterocyst differentiation and identification of the transposon-tagged genes. FEMS Microbiol Lett 224:205–213 [View Article][PubMed]
    [Google Scholar]
  23. Mariscal V., Flores E. ( 2010). Multicellularity in a heterocyst-forming cyanobacterium: pathways for intercellular communication. Adv Exp Med Biol 675:123–135 [View Article][PubMed]
    [Google Scholar]
  24. Merino-Puerto V., Mariscal V., Schwarz H., Maldener I., Mullineaux C. W., Herrero A., Flores E. ( 2011). FraH is required for reorganization of intracellular membranes during heterocyst differentiation in Anabaena sp. strain PCC 7120. J Bacteriol 193:6815–6823 [View Article][PubMed]
    [Google Scholar]
  25. Mitschke J., Vioque A., Haas F., Hess W. R., Muro-Pastor A. M. ( 2011). Dynamics of transcriptional start site selection during nitrogen stress-induced cell differentiation in Anabaena sp. PCC7120. Proc Natl Acad Sci U S A 108:20130–20135 [View Article][PubMed]
    [Google Scholar]
  26. Moslavac S., Nicolaisen K., Mirus O., Al Dehni F., Pernil R., Flores E., Maldener I., Schleiff E. ( 2007a). A TolC-like protein is required for heterocyst development in Anabaena sp. strain PCC 7120. J Bacteriol 189:7887–7895 [View Article][PubMed]
    [Google Scholar]
  27. Moslavac S., Reisinger V., Berg M., Mirus O., Vosyka O., Plöscher M., Flores E., Eichacker L. A., Schleiff E. ( 2007b). The proteome of the heterocyst cell wall in Anabaena sp. PCC 7120. Biol Chem 388:823–829 [View Article][PubMed]
    [Google Scholar]
  28. Muro-Pastor A. M., Olmedo-Verd E., Flores E. ( 2006). All4312, an NtcA-regulated two-component response regulator in Anabaena sp. strain PCC 7120. FEMS Microbiol Lett 256:171–177 [View Article][PubMed]
    [Google Scholar]
  29. Nicolaisen K., Hahn A., Schleiff E. ( 2009a). The cell wall in heterocyst formation by Anabaena sp. PCC 7120. J Basic Microbiol 49:5–24 [View Article][PubMed]
    [Google Scholar]
  30. Nicolaisen K., Mariscal V., Bredemeier R., Pernil R., Moslavac S., López-Igual R., Maldener I., Herrero A., Schleiff E., Flores E. ( 2009b). The outer membrane of a heterocyst-forming cyanobacterium is a permeability barrier for uptake of metabolites that are exchanged between cells. Mol Microbiol 74:58–70 [View Article][PubMed]
    [Google Scholar]
  31. Rippka R., Deruelles J., Waterbury J. B., Herdman M., Stanier R. Y. ( 1979). Generic assignments, strain stories and properties of pure cultures of cyanobacteria. J Gen Appl Microbiol 111:1–61 [View Article]
    [Google Scholar]
  32. Staron P., Forchhammer K., Maldener I. ( 2011). Novel ATP-driven pathway of glycolipid export involving TolC protein. J Biol Chem 286:38202–38210 [View Article][PubMed]
    [Google Scholar]
  33. Tikhonova E. B., Dastidar V., Rybenkov V. V., Zgurskaya H. I. ( 2009). Kinetic control of TolC recruitment by multidrug efflux complexes. Proc Natl Acad Sci U S A 106:16416–16421 [View Article][PubMed]
    [Google Scholar]
  34. Winkenbach F., Wolk C. P., Jost M. ( 1972). Lipids of membranes and of the cell envelope in heterocysts of a blue-green alga. Planta 107:69–80 [View Article]
    [Google Scholar]
  35. Wolk C. P., Vonshak A., Kehoe P., Elhai J. ( 1984). Construction of shuttle vectors capable of conjugative transfer from Escherichia coli to nitrogen-fixing filamentous cyanobacteria. Proc Natl Acad Sci U S A 81:1561–1565 [View Article][PubMed]
    [Google Scholar]
  36. Xu Y., Sim S. H., Song S., Piao S., Kim H. M., Jin X. L., Lee K., Ha N. C. ( 2010). The tip region of the MacA α-hairpin is important for the binding to TolC to the Escherichia coli MacAB–TolC pump. Biochem Biophys Res Commun 394:962–965 [View Article][PubMed]
    [Google Scholar]
  37. Xu Y., Song S., Moeller A., Kim N., Piao S., Sim S. H., Kang M., Yu W., Cho H. S. & other authors ( 2011). Functional implications of an intermeshing cogwheel-like interaction between TolC and MacA in the action of macrolide-specific efflux pump MacAB-TolC. J Biol Chem 286:13541–13549 [View Article][PubMed]
    [Google Scholar]
  38. Yuan Y. R., Blecker S., Martsinkevich O., Millen L., Thomas P. J., Hunt J. F. ( 2001). The crystal structure of the MJ0796 ATP-binding cassette. Implications for the structural consequences of ATP hydrolysis in the active site of an ABC transporter. J Biol Chem 276:32313–32321 [View Article][PubMed]
    [Google Scholar]
  39. Yum S., Xu Y., Piao S., Sim S. H., Kim H. M., Jo W. S., Kim K. J., Kweon H. S., Jeong M. H. & other authors ( 2009). Crystal structure of the periplasmic component of a tripartite macrolide-specific efflux pump. J Mol Biol 387:1286–1297 [View Article][PubMed]
    [Google Scholar]
  40. Zgurskaya H. I., Krishnamoorthy G., Ntreh A., Lu S. ( 2011). Mechanism and function of the outer membrane channel TolC in multidrug resistance and physiology of enterobacteria. Front Microbiol 2:189[PubMed] [CrossRef]
    [Google Scholar]
  41. Zhao J., Wolk C. P. ( 2008). Developmental biology of heterocysts, 2006. Myxobacteria: Multicellularity and Differentiation397–418 Whitworth D. E. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  42. Zhu J., Jäger K., Black T., Zarka K., Koksharova O., Wolk C. P. ( 2001). HcwA, an autolysin, is required for heterocyst maturation in Anabaena sp. strain PCC 7120. J Bacteriol 183:6841–6851 [View Article][PubMed]
    [Google Scholar]
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