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Journal of Bacteriology, July 2008, p. 4416-4426, Vol. 190, No. 13
0021-9193/08/$08.00+0     doi:10.1128/JB.00265-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

EspA, an Orphan Hybrid Histidine Protein Kinase, Regulates the Timing of Expression of Key Developmental Proteins of Myxococcus xanthus{triangledown}

Penelope I. Higgs,1* Sakthimala Jagadeesan,1 Petra Mann,1 and David R. Zusman2

Department of Ecophysiology, Max Planck Institute for Terrestrial Microbiology, Marburg D35043, Germany,1 Department of Molecular and Cell Biology, University of California, Berkeley, California 94720-32042

Received 21 February 2008/ Accepted 26 March 2008

Myxococcus xanthus undergoes a complex starvation-induced developmental program that results in cells forming multicellular fruiting bodies by aggregating into mounds and then differentiating into spores. This developmental program requires at least 72 h and is mediated by a temporal cascade of gene regulators in response to intra- and extracellular signals. espA mutants, encoding an orphan hybrid histidine kinase, alter the timing of this developmental program, greatly accelerating developmental progression. Here, we characterized EspA and demonstrated that it autophosphorylates in vitro on the conserved histidine residue and then transfers the phosphoryl group to the conserved aspartate residue in the associated receiver domain. The conserved histidine and aspartate residues were both required for EspA function in vivo. Analysis of developmental gene expression and protein accumulation in espA mutants indicated that the expression of the A-signal-dependent spi gene was not affected but that the MrpC transcriptional regulator accumulated earlier, resulting in earlier expression of its target, the FruA transcriptional regulator. Early expression of FruA correlated with acceleration of both the aggregation and sporulation branches of the developmental program, as monitored by early methylation of the FrzCD chemosensory receptor and early expression of the sporulation-specific dev and Mxan_3227 ({Omega}7536) genes. These results show that EspA plays a key role in the timing of expression of genes necessary for progression of cells through the developmental program.

* Corresponding author. Mailing address: Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch Strasse 1, 35043 Marburg, Germany. Phone: (49) 6421 178301. Fax: (49) 6421 178309. E-mail: higgs{at}mpi-marburg.mpg.de

{triangledown} Published ahead of print on 4 April 2008.

Journal of Bacteriology, July 2008, p. 4416-4426, Vol. 190, No. 13
0021-9193/08/$08.00+0     doi:10.1128/JB.00265-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Jagadeesan, S., Mann, P., Schink, C. W., Higgs, P. I. (2009). A Novel "Four-component" Two-component Signal Transduction Mechanism Regulates Developmental Progression in Myxococcus xanthus. J. Biol. Chem. 284: 21435-21445 [Abstract] [Full Text]  
  • Mittal, S., Kroos, L. (2009). Combinatorial Regulation by a Novel Arrangement of FruA and MrpC2 Transcription Factors during Myxococcus xanthus Development. J. Bacteriol. 191: 2753-2763 [Abstract] [Full Text]  
  • Mittal, S., Kroos, L. (2009). A combination of unusual transcription factors binds cooperatively to control Myxococcus xanthus developmental gene expression. Proc. Natl. Acad. Sci. USA 106: 1965-1970 [Abstract] [Full Text]  
  • Kroos, L. (2008). Bacterial Development in the Fast Lane. J. Bacteriol. 190: 4373-4376 [Full Text]  


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