1887

Abstract

Gas vesicle formation in haloarchaea involves 14 gas vesicle protein () genes. The strong promoter drives the expression of , which encodes the major gas vesicle structural proteins GvpA and GvpC, whereas the oppositely oriented promoter initiates the synthesis of the two regulator proteins, GvpD and GvpE. GvpE activates and , and requires a 20 nt upstream activator sequence (UAS). UAS and UAS partially overlap in the centre of the 35 bp intergenic region. The basal and GvpE-induced activities of and were investigated in transformants. Each UAS consists of two 8 nt portions (, 1A+2A; , 1D+2D), and mutations in the overlapping 1A and 1D portions affected the GvpE induction of both promoters. Substitution of one of the UAS portions by a nonsense sequence showed that a complete UAS is required for activation. The activation of was more efficient compared with . Promoter with UAS in configuration 1A+1A was still activated by GvpE, but was not inducible with UAS in configuration 1D+1D. The TATA box and/or transcription factor B recognition element (BRE) were exchanged between and All elements of functioned well in the environment of ‘’ and transferred the stronger activity to ‘’. In contrast, the respective ‘’ chimeras were less active, and BRE was not functional in the environment of ‘. The relative strengths of the two promoters were substantially determined by the BRE. A 4 nt scanning mutagenesis uncovered an additional regulatory element in the region between TATA and the transcriptional start site of .

Funding
This study was supported by the:
  • German Research Foundation DFG (Award Pf 165/10-1)
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.060178-0
2012-11-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/11/2815.html?itemId=/content/journal/micro/10.1099/mic.0.060178-0&mimeType=html&fmt=ahah

References

  1. Baliga N. S., Goo Y. A., Ng W. V., Hood L., Daniels C. J., DasSarma S. ( 2000). Is gene expression in Halobacterium NRC-1 regulated by multiple TBP and TFB transcription factors?. Mol Microbiol 36:1184–1185 [View Article] [PubMed]
    [Google Scholar]
  2. Bauer M., Marschaus L., Reuff M., Besche V., Sartorius-Neef S., Pfeifer F. ( 2008). Overlapping activator sequences determined for two oppositely oriented promoters in halophilic Archaea. Nucleic Acids Res 36:598–606 [View Article] [PubMed]
    [Google Scholar]
  3. Bell S. D., Cairns S. S., Robson R. L., Jackson S. P. ( 1999a). Transcriptional regulation of an archaeal operon in vivo and in vitro . Mol Cell 4:971–982 [View Article] [PubMed]
    [Google Scholar]
  4. Bell S. D., Kosa P. L., Sigler P. B., Jackson S. P. ( 1999b). Orientation of the transcription preinitiation complex in archaea. Proc Natl Acad Sci U S A 96:13662–13667 [View Article] [PubMed]
    [Google Scholar]
  5. Bleiholder A., Frommherz R., Teufel K., Pfeifer F. ( 2012). Expression of multiple tfb genes in different Halobacterium salinarum strains and interaction of TFB with transcriptional activator GvpE. Arch Microbiol 194:269–279 [View Article] [PubMed]
    [Google Scholar]
  6. Brenneis M., Hering O., Lange C., Soppa J. ( 2007). Experimental characterization of cis-acting elements important for translation and transcription in halophilic archaea. PLoS Genet 3:e229 [View Article] [PubMed]
    [Google Scholar]
  7. Chomczynski P., Sacchi N. ( 1987). Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Anal Biochem 162:156–159 [View Article] [PubMed]
    [Google Scholar]
  8. Coker J. A., DasSarma P., Kumar J., Müller J. A., DasSarma S. ( 2007). Transcriptional profiling of the model Archaeon Halobacterium sp. NRC-1: responses to changes in salinity and temperature. Saline Syst 3:6 [View Article] [PubMed]
    [Google Scholar]
  9. Englert C., Krüger K., Offner S., Pfeifer F. ( 1992). Three different but related gene clusters encoding gas vesicles in halophilic archaea. J Mol Biol 227:586–592 [View Article] [PubMed]
    [Google Scholar]
  10. Facciotti M. T., Reiss D. J., Pan M., Kaur A., Vuthoori M., Bonneau R., Shannon P., Srivastava A., Donohoe S. M. & other authors ( 2007). General transcription factor specified global gene regulation in archaea. Proc Natl Acad Sci U S A 104:4630–4635 [View Article] [PubMed]
    [Google Scholar]
  11. Geiduschek E. P., Ouhammouch M. ( 2005). Archaeal transcription and its regulators. Mol Microbiol 56:1397–1407 [View Article] [PubMed]
    [Google Scholar]
  12. Gregor D., Pfeifer F. ( 2001). Use of a halobacterial bgaH reporter gene to analyse the regulation of gene expression in halophilic archaea. Microbiology 147:1745–1754 [PubMed]
    [Google Scholar]
  13. Gregor D., Pfeifer F. ( 2005). In vivo analyses of constitutive and regulated promoters in halophilic archaea. Microbiology 151:25–33 [View Article] [PubMed]
    [Google Scholar]
  14. Hofacker A., Schmitz K. M., Cichonczyk A., Sartorius-Neef S., Pfeifer F. ( 2004). GvpE- and GvpD-mediated transcription regulation of the p-gvp genes encoding gas vesicles in Halobacterium salinarum . Microbiology 150:1829–1838 [View Article] [PubMed]
    [Google Scholar]
  15. Holmes M. L., Dyall-Smith M. L. ( 2000). Sequence and expression of a halobacterial β-galactosidase gene. Mol Microbiol 36:114–122 [View Article] [PubMed]
    [Google Scholar]
  16. Kosa P. F., Ghosh G., DeDecker B. S., Sigler P. B. ( 1997). The 2.1-Å crystal structure of an archaeal preinitiation complex: TATA-box-binding protein/transcription factor (II)B core/TATA-box. Proc Natl Acad Sci U S A 94:6042–6047 [View Article] [PubMed]
    [Google Scholar]
  17. Krüger K., Hermann T., Armbruster V., Pfeifer F. ( 1998). The transcriptional activator GvpE for the halobacterial gas vesicle genes resembles a basic region leucine-zipper regulatory protein. J Mol Biol 279:761–771 [View Article] [PubMed]
    [Google Scholar]
  18. Lam W. L., Doolittle W. F. ( 1989). Shuttle vectors for the archaebacterium Halobacterium volcanii . Proc Natl Acad Sci U S A 86:5478–5482 [View Article] [PubMed]
    [Google Scholar]
  19. Lie T. J., Hendrickson E. L., Niess U. M., Moore B. C., Haydock A. K., Leigh J. A. ( 2010). Overlapping repressor binding sites regulate expression of the Methanococcus maripaludis glnK 1 operon. Mol Microbiol 75:755–762 [View Article] [PubMed]
    [Google Scholar]
  20. Littlefield O., Korkhin Y., Sigler P. B. ( 1999). The structural basis for the oriented assembly of a TBP/TFB/promoter complex. Proc Natl Acad Sci U S A 96:13668–13673 [View Article] [PubMed]
    [Google Scholar]
  21. Müller S., Klein A. ( 2001). Coordinate positive regulation of genes encoding [NiFe] hydrogenases in Methanococcus voltae . Mol Genet Genomics 265:1069–1075 [View Article] [PubMed]
    [Google Scholar]
  22. Noll I., Müller S., Klein A. ( 1999). Transcriptional regulation of genes encoding the selenium-free [NiFe]-hydrogenases in the archaeon Methanococcus voltae involves positive and negative control elements. Genetics 152:1335–1341 [PubMed]
    [Google Scholar]
  23. Offner S., Pfeifer F. ( 1995). Complementation studies with the gas vesicle-encoding p-vac region of Halobacterium salinarium PHH1 reveal a regulatory role for the p-gvpDE genes. Mol Microbiol 16:9–19 [View Article] [PubMed]
    [Google Scholar]
  24. Palmer B. R., Marinus M. G. ( 1994). The dam and dcm strains of Escherichia coli – a review. Gene 143:1–12 [View Article] [PubMed]
    [Google Scholar]
  25. Pfeifer F., Ghahraman P. ( 1993). Plasmid pHH1 of Halobacterium salinarium: characterization of the replicon region, the gas vesicle gene cluster and insertion elements. Mol Gen Genet 238:193–200 [PubMed]
    [Google Scholar]
  26. Pfeifer F., Offner S., Krüger K., Ghahraman P., Englert C. ( 1993). Transformation of halophilic archaea and investigation of gas vesicle synthesis. Syst Appl Microbiol 16:569–577 [View Article]
    [Google Scholar]
  27. Pfeifer F., Zotzel J., Kurenbach B., Röder R., Zimmermann P. ( 2001). A p-loop motif and two basic regions in the regulatory protein GvpD are important for the repression of gas vesicle formation in the archaeon Haloferax mediterranei . Microbiology 147:63–73 [PubMed]
    [Google Scholar]
  28. Plößer P., Pfeifer F. ( 2002). A bZIP protein from halophilic archaea: structural features and dimer formation of cGvpE from Halobacterium salinarum . Mol Microbiol 45:511–520 [View Article] [PubMed]
    [Google Scholar]
  29. Renfrow M. B., Naryshkin N., Lewis L. M., Chen H. T., Ebright R. H., Scott R. A. ( 2004). Transcription factor B contacts promoter DNA near the transcription start site of the archaeal transcription initiation complex. J Biol Chem 279:2825–2831 [View Article] [PubMed]
    [Google Scholar]
  30. Scheuch S., Pfeifer F. ( 2007). GvpD-induced breakdown of the transcriptional activator GvpE of halophilic archaea requires a functional p-loop and an arginine-rich region of GvpD. Microbiology 153:947–958 [View Article] [PubMed]
    [Google Scholar]
  31. Scheuch S., Marschaus L., Sartorius-Neef S., Pfeifer F. ( 2008). Regulation of gvp genes encoding gas vesicle proteins in halophilic Archaea. Arch Microbiol 190:333–339 [View Article] [PubMed]
    [Google Scholar]
  32. Sun J., Klein A. ( 2004). A LysR-type regulator is involved in the negative regulation of genes encoding selenium-free hydrogenases in the archaeon Methanococcus voltae . Mol Microbiol 52:563–571 [View Article] [PubMed]
    [Google Scholar]
  33. Teufel K., Pfeifer F. ( 2010). Interaction of transcription activator GvpE with TATA-box-binding proteins of Halobacterium salinarum . Arch Microbiol 192:143–149 [View Article] [PubMed]
    [Google Scholar]
  34. Teufel K., Bleiholder A., Griesbach T., Pfeifer F. ( 2008). Variations in the multiple tbp genes in different Halobacterium salinarum strains and their expression during growth. Arch Microbiol 190:309–318 [View Article] [PubMed]
    [Google Scholar]
  35. Turkarslan S., Reiss D. J., Gibbins G., Su W. L., Pan M., Bare J. C., Plaisier C. L., Baliga N. S. ( 2011). Niche adaptation by expansion and reprogramming of general transcription factors. Mol Syst Biol 7:554 [View Article] [PubMed]
    [Google Scholar]
  36. Zimmermann P., Pfeifer F. ( 2003). Regulation of the expression of gas vesicle genes in Haloferax mediterranei: interaction of the two regulatory proteins GvpD and GvpE. Mol Microbiol 49:783–794 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.060178-0
Loading
/content/journal/micro/10.1099/mic.0.060178-0
Loading

Data & Media loading...

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