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Journal of Bacteriology, June 2005, p. 4149-4162, Vol. 187, No. 12
0021-9193/05/$08.00+0     doi:10.1128/JB.187.12.4149-4162.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Identification of the {Omega}4406 Regulatory Region, a Developmental Promoter of Myxococcus xanthus, and a DNA Segment Responsible for Chromosomal Position-Dependent Inhibition of Gene Expression

Jennifer Loconto ,{dagger},{ddagger} Poorna Viswanathan,{dagger} Scott J. Nowak,§ Monica Gloudemans, and Lee Kroos*

Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824

Received 14 December 2004/ Accepted 4 March 2005

When starved, Myxococcus xanthus cells send signals to each other that coordinate their movements, gene expression, and differentiation. C-signaling requires cell-cell contact, and increasing contact brought about by cell alignment in aggregates is thought to increase C-signaling, which induces expression of many genes, causing rod-shaped cells to differentiate into spherical spores. C-signaling involves the product of the csgA gene. A csgA mutant fails to express many genes that are normally induced after about 6 h into the developmental process. One such gene was identified by insertion of Tn5 lac at site {Omega}4406 in the M. xanthus chromosome. Tn5 lac fused transcription of lacZ to the upstream {Omega}4406 promoter. In this study, the {Omega}4406 promoter region was identified by analyzing mRNA and by testing different upstream DNA segments for the ability to drive developmental lacZ expression in M. xanthus. The 5' end of {Omega}4406 mRNA mapped to approximately 1.3 kb upstream of the Tn5 lac insertion. A 1.0-kb DNA segment from 0.8 to 1.8 kb upstream of the Tn5 lac insertion, when fused to lacZ and integrated at a phage attachment site in the M. xanthus chromosome, showed a similar pattern of developmental expression as Tn5 lac {Omega}4406. The DNA sequence upstream of the putative transcriptional start site was strikingly similar to promoter regions of other C-signal-dependent genes. Developmental lacZ expression from the 1.0-kb segment was abolished in a csgA mutant but was restored upon codevelopment of the csgA mutant with wild-type cells, which supply C-signal, demonstrating that the {Omega}4406 promoter responds to extracellular C-signaling. Interestingly, the 0.8-kb DNA segment immediately upstream of Tn5 lac {Omega}4406 inhibited expression of a downstream lacZ reporter in transcriptional fusions integrated at a phage attachment site in the chromosome but not at the normal {Omega}4406 location. To our knowledge, this is the first example in M. xanthus of a chromosomal position-dependent effect on gene expression attributable to a DNA segment outside the promoter region.

* Corresponding author. Mailing address: Department of Biochemistry, Michigan State University, East Lansing, MI 48824. Phone: (517) 355-9726. Fax: (517) 353-9334. E-mail: kroos{at}pilot.msu.edu.

{dagger} J.L. and P.V. contributed equally to the work presented.

{ddagger} Present address: The Anthony Nolan Research Institute, The Royal Free and University College Medical School, London, United Kingdom.

§ Present address: Skirball Institute of Biomolecular Medicine, 540 First Avenue, New York, NY 10016.

Journal of Bacteriology, June 2005, p. 4149-4162, Vol. 187, No. 12
0021-9193/05/$08.00+0     doi:10.1128/JB.187.12.4149-4162.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • 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]  
  • Viswanathan, P., Murphy, K., Julien, B., Garza, A. G., Kroos, L. (2007). Regulation of dev, an Operon That Includes Genes Essential for Myxococcus xanthus Development and CRISPR-Associated Genes and Repeats. J. Bacteriol. 189: 3738-3750 [Abstract] [Full Text]  
  • Gronewold, T. M. A., Kaiser, D. (2007). Mutations of the Act Promoter in Myxococcus xanthus. J. Bacteriol. 189: 1836-1844 [Abstract] [Full Text]  
  • Viswanathan, K., Viswanathan, P., Kroos, L. (2006). Mutational Analysis of the Myxococcus xanthus {Omega}4406 Promoter Region Reveals an Upstream Negative Regulatory Element That Mediates C-Signal Dependence. J. Bacteriol. 188: 515-524 [Abstract] [Full Text]  


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