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J. Biol. Chem., Vol. 279, Issue 7, 5894-5903, February 13, 2004

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Topography of the Euryarchaeal Transcription Initiation Complex^*

Michael S. Bartlett, Michael Thomm¶||, and E. Peter Geiduschek

From the Division of Biological Sciences, Center for Molecular Genetics, University of California at San Diego, La Jolla, California, 92093-0634 and the ^¶Institut für Allgemeine Mikrobiologie, Universität Kiel, Am Botanischen Garten 1-9, D-24118 Kiel, Germany

Transcription in the Archaea is carried out by RNA polymerases and transcription factors that are highly homologous to their eukaryotic counterparts, but little is known about the structural organization of the archaeal transcription complex. To address this, transcription initiation complexes have been formed with Pyrococcus furiosus transcription factors (TBP and TFB1), RNA polymerase, and a linear DNA fragment containing a strong promoter. The arrangement of proteins from base pair -35 to +20 (relative to the transcriptional start site) has been analyzed by photochemical protein-DNA cross-linking. TBP cross-links to the TATA box and TFB1 cross-links both upstream and downstream of the TATA box, as expected, but the sites of most prominent TFB1 cross-linking are located well downstream of the TATA box, reaching as far as the start site of transcription, suggesting a role for TFB1 in initiation of transcription that extends beyond polymerase recruitment. These cross-links indicate the transcription factor orientation in the initiation complex. The pattern of cross-linking of four RNA polymerase subunits (B, A', A'', and H) to the promoter suggests a path for promoter DNA relative to the RNA polymerase surface in this archaeal transcription initiation complex. In addition, an unidentified protein approximately the size of TBP cross-links to the non-transcribed DNA strand near the upstream edge of the transcription bubble. Cross-linking is specific to the polymerase-containing initiation complex and requires the gdh promoter TATA box. The location of this protein suggests that it, like TFB1, could also have a role in transcription initiation following RNA polymerase recruitment.

Received for publication, October 17, 2003 , and in revised form, November 13, 2003.

^* This work was supported by a grant from the NIGMS (at San Diego) and the Deutsche Forshungsgemeinschaft (at Kiel and Regensburg). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^|| Current address: Universität Regensburg, Lehrstuhl für Mikrobiologie, Universitätsstr. 31, D-93053 Regensburg, Germany.

A National Research Service postdoctoral fellowship from the National Institutes of Health. To whom correspondence should be addressed: Portland State University, Dept. of Biology, P. O. Box 751, Portland, OR 97207. Tel.: 503-725-3858; Fax: 503-725-3888; E-mail: micb{at}pdx.edu.

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