Nucleic Acids Research Advance Access originally published online on January 18, 2008
Nucleic Acids Research 2008 36(5):1429-1442; doi:10.1093/nar/gkm1116
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Nucleic Acids Research, 2008, Vol. 36, No. 5 1429-1442
© 2008 The Author(s)
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Molecular Biology |
Transcription regulation of the type II restriction-modification system AhdI
1Waksman Institute, Piscataway, NJ 08854, USA, 2Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Pushchino, 142292 Russia, 3Mathematical Biosciences Institute, The Ohio State University, Columbus, OH 43210, USA, 4Biophysics Laboratories, Institute of Biomedical and Biomolecular Sciences, University of Portsmouth, UK, 5E. A. Doisy Department of Biochemistry and Molecular Biology, St. Louis University Medical School, St. Louis, MO 63104, USA, 6Institute of Gene Biology, Russian Academy of Sciences, Moscow 117312 and 7Institute of Molecular Genetics, Moscow 123182, Russia
*To whom correspondence should be addressed. Tel: +1 732 445 6095; Fax: +1 732 445 5735; Email: severik{at}waksman.rutgers.edu
Received September 20, 2007. Revised November 28, 2007. Accepted November 28, 2007.
The Restriction-modification system AhdI contains two convergent transcription units, one with genes encoding methyltransferase subunits M and S and another with genes encoding the controller (C) protein and the restriction endonuclease (R). We show that AhdI transcription is controlled by two independent regulatory loops that are well-optimized to ensure successful establishment in a naïve bacterial host. Transcription from the strong MS promoter is attenuated by methylation of an AhdI site overlapping the -10 element of the promoter. Transcription from the weak CR promoter is regulated by the C protein interaction with two DNA-binding sites. The interaction with the promoter-distal high-affinity site activates transcription, while interaction with the weaker promoter-proximal site represses it. Because of high levels of cooperativity, both C protein-binding sites are always occupied in the absence of RNA polymerase, raising a question how activated transcription is achieved. We develop a mathematical model that is in quantitative agreement with the experiment and indicates that RNA polymerase outcompetes C protein from the promoter-proximal-binding site. Such an unusual mechanism leads to a very inefficient activation of the R gene transcription, which presumably helps control the level of the endonuclease in the cell.
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