Abstract
Transcriptional regulation in the archaea involves a mosaic of DNA-binding proteins frequently (although not exclusively) of bacterial type, modulating a eukaryal-type core transcription apparatus. Methanocaldococcus jannaschii (Mja) Ptr2, a homologue of the Lrp/AsnC family of bacterial transcription regulators that are among the most widely disseminated archaeal DNA-binding proteins, has been shown to activate transcription by its conjugate hyperthermophilic RNA polymerase. Here, two in vitro systems have been exploited to show that Ptr2 and a Lrp homologue from the thermophile Methanothermococcus thermolithotrophicus (Mth) activate transcription over a approximately 40 degrees C range, in conjunction with their cognate TATA-binding proteins (TBPs) and with heterologous TBPs. A closely related homologue from the mesophile Methanococcus maripaludis (Mma) is nearly inert as a transcriptional activator, but a cluster of mutations that converts a surface patch of Mma Lrp to identity with Ptr2 confers transcriptional activity. Mja, Mth, and Mma TBPs are interchangeable for basal transcription, but their ability to support Lrp-mediated transcriptional activation varies widely, with Mja TBP the most active and Mth TBP the least active partner. The implications of this finding for understanding the roles of TBP paralogues in supporting the gene-regulatory repertoires of archaeal genomes are briefly noted.
MeSH Terms
Amino Acid Sequence
Archaeal Proteins/physiology
DNA/metabolism
DNA-Binding Proteins/physiology
Methanococcus/genetics
Molecular Sequence Data
TATA-Box Binding Protein/physiology
Transcriptional Activation
Chemicals
Archaeal Proteins
DNA-Binding Proteins
Ptr2 protein, Methanococcus jannaschii
TATA-Box Binding Protein
DNA
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Ouhammouch Mohamed
Center for Molecular Genetics and Division of Biological Sciences, University of California-San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0634, USA. mouham@biomail.ucsd.edu
Geiduschek E Peter
References (29)
29 references, click to expand
-
The Sulfolobus solfataricus Lrp-like protein LysM regulates lysine biosynthesis in response to lysine availability.
J Biol Chem. 2002 Aug 16;277(33):29537-49
PMID: 12042311
-
The genome of M. acetivorans reveals extensive metabolic and physiological diversity.
Genome Res. 2002 Apr;12(4):532-42
PMID: 11932238
-
ilvIH operon expression in Escherichia coli requires Lrp binding to two distinct regions of DNA.
J Bacteriol. 2002 Oct;184(19):5293-300
PMID: 12218014
-
The Lrp family of transcriptional regulators.
Mol Microbiol. 2003 Apr;48(2):287-94
PMID: 12675791
-
Archaeal chromatin and transcription.
Mol Microbiol. 2003 May;48(3):587-98
PMID: 12694606
-
Activation of archaeal transcription by recruitment of the TATA-binding protein.
Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5097-102
PMID: 12692306
-
Structure of a ternary transcription activation complex.
Mol Cell. 2004 Jan 16;13(1):45-53
PMID: 14731393
-
The archaeal feast/famine regulatory protein: potential roles of its assembly forms for regulating transcription.
Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):2840-5
PMID: 14976242
-
Efficient site-directed in vitro mutagenesis using phagemid vectors.
Biotechniques. 1989 Mar;7(3):282-9
PMID: 2698649
-
An archaebacterial cell-free transcription system. The expression of tRNA genes from Methanococcus vannielii is mediated by a transcription factor.
Nucleic Acids Res. 1990 Mar 25;18(6):1361-7
PMID: 2326183
-
Efficient site-directed mutagenesis using uracil-containing DNA.
Methods Enzymol. 1991;204:125-39
PMID: 1943776
-
Purification and characterization of a general transcription factor, aTFB, from the archaeon Methanococcus thermolithotrophicus.
J Biol Chem. 1993 Nov 15;268(32):24047-52
PMID: 8226949
-
Functional interaction of yeast and human TATA-binding proteins with an archaeal RNA polymerase and promoter.
Proc Natl Acad Sci U S A. 1995 Jan 17;92(2):472-6
PMID: 7831313
-
The 2.1-A 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. 1997 Jun 10;94(12):6042-7
PMID: 9177165
-
Development of genetic approaches for the methane-producing archaebacterium Methanococcus maripaludis.
Biofactors. 1997;6(1):37-46
PMID: 9233538
-
Crystal structure of ATF-2/c-Jun and IRF-3 bound to the interferon-beta enhancer.
EMBO J. 2004 Nov 10;23(22):4384-93
PMID: 15510218
-
A fully recombinant system for activator-dependent archaeal transcription.
J Biol Chem. 2004 Dec 10;279(50):51719-21
PMID: 15485836
-
Archaeal genetics - the third way.
Nat Rev Genet. 2005 Jan;6(1):58-73
PMID: 15630422
-
Promoter architecture and response to a positive regulator of archaeal transcription.
Mol Microbiol. 2005 May;56(3):625-37
PMID: 15819620
-
Archaeal transcription and its regulators.
Mol Microbiol. 2005 Jun;56(6):1397-407
PMID: 15916593
-
DNA-binding proteins and evolution of transcription regulation in the archaea.
Nucleic Acids Res. 1999 Dec 1;27(23):4658-70
PMID: 10556324
-
The structural basis for the oriented assembly of a TBP/TFB/promoter complex.
Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13668-73
PMID: 10570130
-
Is gene expression in Halobacterium NRC-1 regulated by multiple TBP and TFB transcription factors?
Mol Microbiol. 2000 Jun;36(5):1184-5
PMID: 10844702
-
Mechanism of autoregulation by an archaeal transcriptional repressor.
J Biol Chem. 2000 Oct 13;275(41):31624-9
PMID: 10900210
-
An Lrp-like transcriptional regulator from the archaeon Pyrococcus furiosus is negatively autoregulated.
J Biol Chem. 2000 Dec 8;275(49):38160-9
PMID: 10973967
-
A thermostable platform for transcriptional regulation: the DNA-binding properties of two Lrp homologs from the hyperthermophilic archaeon Methanococcus jannaschii.
EMBO J. 2001 Jan 15;20(1-2):146-56
PMID: 11226165
-
Crystal structure of the Lrp-like transcriptional regulator from the archaeon Pyrococcus furiosus.
EMBO J. 2001 Mar 1;20(5):990-7
PMID: 11230123
-
A Pyrococcus homolog of the leucine-responsive regulatory protein, LrpA, inhibits transcription by abrogating RNA polymerase recruitment.
Nucleic Acids Res. 2002 Feb 1;30(3):701-10
PMID: 11809882
-
Structural basis of transcription activation: the CAP-alpha CTD-DNA complex.
Science. 2002 Aug 30;297(5586):1562-6
PMID: 12202833