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1To whom correspondence should be addressed (email [email protected]). a minimal set of .... responsive TrpY of Methanothermobacter thermautotrophi- cus implements ... template. In vitro transcription with Sulfolobus TFs and RNAP was performed as described previously [32]. ..... a sequence logo generator. Genome ...

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Cis-regulatory logic in archaeal transcription Eveline Peeters*1 , Nuno Peixeiro† and Guennadi Sezonov‡§ *Research group of Microbiology, Vrije Universiteit Brussel, Pleinlaan 2, B-1050 Brussels, Belgium, †Commissariat a` l’Energie Atomique et aux Energies Alternatives (CEA), iBiTec-S, Service de Biologie Integrative ´ et Gen ´ etique ´ Moleculaire, ´ F-91191 Gif-sur-Yvette Cedex, France, ‡Unite´ de Biologie Moleculaire ´ du Gene ` chez les Extremophiles, ˆ Institut Pasteur, 25–28 rue du Dr Roux, F-75724 Paris Cedex 15, France, and §Universite´ Pierre et Marie Curie, UMR 7138 ‘Systematique, ´ Adaptation, Evolution’, Paris, France

Abstract For cellular fitness and survival, gene expression levels need to be regulated in response to a wealth of cellular and environmental signals. TFs (transcription factors) execute a large part of this regulation by interacting with the basal transcription machinery at promoter regions. Archaea are characterized by a simplified eukaryote-like basal transcription machinery and bacteria-type TFs, which convert sequence information into a gene expression output according to cis-regulatory rules. In the present review, we discuss the current state of knowledge about these rules in archaeal systems, ranging from DNA-binding specificities and operator architecture to regulatory mechanisms.

Introduction Micro-organisms respond efficiently to ever-continuing changing environmental conditions by a combination of transcriptional, translational and metabolic regulation. At the level of gene transcription, the largest part of regulation is carried out during the transcription initiation phase by the action of specific TFs (transcription factors). In prokaryotes, specific TFs are mostly single-component systems, i.e. proteins that contain both the DNA-binding domain and the stimulus-response domain and convey stimuli directly into an adapted gene expression response. Stimuli range from smallmolecule ligands that interact with the TF, either metabolites or environmental compounds taken up by the cell, to signals such as light, temperature and the cellular redox state. Archaea are characterized by a eukaryote-type basal transcription machinery, in terms of both structure and organization, although being a simplified version [1–3] (Figure 1A). A basal archaeal promoter is composed of a TATA box, centred at position − 26/ − 27 with respect to the TSS (transcription start site), and a purine-rich BRE (factor B recognition element) located immediately upstream of the TATA box [4]. The unique archaeal RNAP (RNA polymerase) contains up to 13 subunits and shows large structural similarities to the eukaryotic RNAPII, exemplified by the conservation of a characteristic protruding stalk [5,6]. Whereas bacterial RNAP initiates transcription without the involvement of additional factors, archaeal RNAP requires

Key words: activation, Archaea, DNA binding, operator, repression, transcription regulation. Abbreviations used: BRE, factor B recognition element; ChIP, chromatin immunoprecipitation; ChIP-seq, ChIP followed by deep sequencing; HTH, helix–turn–helix; PIC, pre-initiation complex; RHH, ribbon–helix–helix; RNAP, RNA polymerase; SELEX, systematic evolution of ligands by exponential enrichment; TBP, TATA-box-binding protein; TF, transcription factor; TFB, transcription factor B; TSS, transcription start site. 1 To whom correspondence should be addressed (email [email protected]).

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a minimal set of two general TFs: TBP (TATA-box-binding protein) and TFB (transcription factor B). PIC (pre-initiation complex) formation consists of the following steps: first, TBP binds the promoter region at the TATA box. Subsequently, TFB binds the TBP–DNA complex and by recognizing the BRE sequence it determines the correct orientation of the PIC [7]. Finally, RNAP is recruited to the complex and positioned correctly to initiate transcription at the TSS. Several archaeal species contain multiple, divergent tfb and tbp genes and it is hypothesized that these have a regulatory role at a higher level, reminiscent of alternative σ factors in bacteria [8]. Despite having a eukaryote-like basal transcription machinery, archaeal genomic organizational properties such as coding density and operonic structure are bacterialike [9]. Furthermore, specific TFs in archaea, which are mostly single-component TFs, are homologous with bacterial TFs. Approximately 53 % of all identified TFs in archaeal genomes has at least one homologue in bacteria, as opposed to 2 % having a eukaryotic homologue [10]. By far the largest fraction of bacterial/archaeal TFs contain an HTH (helix–turn–helix) motif, followed by the RHH (ribbon– helix–helix) motif (Arc/MetJ domain) and the zinc ribbon [11,12]. Remarkably, TFs with the RHH motif are the most common regulators encoded by hyperthermophilic archaeal viruses [13]. Bacteria-like TFs in archaea and bacteria are postulated to have a common evolutionary origin: before divergence of the bacterial lineage, the last common ancestor of the prokaryotes possessed TFs with motifs similar to the contemporaneous archaeal/bacterial TFs [12]. TFs convert one or more input signals at a specific promoter into a regulatory output. Structural determinants are the TFbinding motifs encoded in the promoter DNA sequence. The present mini-review focuses on mechanisms that determine the control logic relationship between operator architecture and regulatory output in archaeal cells and their viruses. Special interest lies in the intriguing combination of a Biochem. Soc. Trans. (2013) 41, 326–331; doi:10.1042/BST20120312

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Figure 1 Main features of archaeal TF binding and mechanisms of regulation (A) Overview of molecular mechanisms of archaeal transcription regulation and binding locations for which the corresponding mechanism has been observed, ranging from far upstream of promoter (A), close upstream of promoter (B), overlapping core promoter (C), downstream of promoter (D) to downstream of TSS (E). The symbol + indicates that the mechanism has been demonstrated, the symbol ( + ) indicates that the mechanism has been postulated without conclusive proof. (B) Selected examples of DNA-binding specificities of archaeal TFs: Phr of P. furiosus [22], Ss-LrpB of S. solfataricus [20,35] and the as yet unidentified TF regulating arabinose metabolic and transport genes in Sulfolobus sp. [31]. Specificities are based on identified binding sites, and represented as sequence logos, which are ordered stacks of letters in which each letter’s height indicates the information content at a particular position of the binding motif. Sequence logos have been constructed with WebLogo [50] (http://www.weblogo.berkeley.edu).

eukaryote-type basal transcription machinery and bacterialike TFs.

Architecture of archaeal operators The molecular basis of the functioning of a TF is founded in its sequence-specific interaction with the DNA. Detailed studies of the DNA-binding sequence specificity (determined by the relative binding affinities to all possible binding sites) of archaeal TFs are relatively scarce. Often, only a limited number of binding sites is known on the basis of experimental or in silico (e.g. phylogenetic footprinting) approaches. Mutational analysis of binding sites, combined with in vitro DNA-binding assays [14–24], in vitro transcription assays [25] or in vivo reporter gene assays [21,26,27], have provided deeper insights into the DNA-binding energy landscape and corresponding regulatory outputs for a variety of archaeal TFs. For some of these proteins, a higher-resolution DNAbinding profile has been obtained by applying the method of SELEX (systematic evolution of ligands by exponential enrichment) [24,28,29]. ChIP-on-chip [ChIP (chromatin immunoprecipitation) using microarrays] or ChIP-seq (ChIP followed by deep sequencing), which are among the most powerful techniques to map DNA-binding sites of a TF genome-wide in an in vivo context, has been rarely applied in archaea [30], despite its proven success in bacterial and eukaryotic systems.

Given the bacterial nature of DNA-binding motifs, it is evident that archaeal TFs recognize specific DNA sequences in a similar fashion as their bacterial counterparts. DNA sequence motifs have almost invariably a semi-palindromic nature, which reflects the two-fold symmetry of the binding proteins caused by homodimerization. Examples of DNAbinding sequence specificities for a selection of archaeal TFs are shown in Figure 1(B). Sizes of binding motifs can range from a minimal 8 bp, exemplified by the ARA box motif in Sulfolobus [27,31] to 24 bp, as is the case for the heat-shock regulator Phr in Pyrococcus furiosus [22]. Typical binding motifs usually have a size between 11 and 17 bp with a number of less- or non-informative base pairs in the centre. Each dyad symmetry-determining half-site allows base-specific interactions in the major groove of the DNA, either with the recognition α-helix of an HTH motif [12] or with the β-sheet face of a RHH motif [32]. The alignment of two half-sites in a binding site is highly constrained, as demonstrated for SsLrpB from Sulfolobus solfataricus: whereas an insertion of 1 or 2 bp in the centre of the binding site is still tolerated, albeit resulting in a much lower binding affinity, a 1 bp deletion completely abolishes DNA binding, pointing to a limited conformational flexibility of the TF protein [17]. Binding to a single site is exceptional; most TFs recognize an array of binding sites, resulting in homoco-operative binding, which enhances the global binding affinity, but also leads to a higher sensitivity and a non-linear regulatory response. Frequently, there is one primary site that exerts  C The

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regulation, whereas the other sites are auxiliary operators merely assisting in the occupation of the primary site and contributing to repression or activation only to a minor extent. For example, besides the ARA box located close to the araS promoter in Sulfolobus, a distal upstream ARA box was identified that can be deleted without affecting activation [27]. For Ptr2 from Methanocaldococcus jannaschii, an auxiliary site was identified inside the ORF (open reading frame) that is bound but does not contribute to activation [25]. There are spatial constraints on the placement of multiple binding sites and these are usually governed by the DNA helical structure in such a way that it allows binding of different TF molecules to the same face of the helix. Centre-to-centre distances corresponding to two or three full helical turns between juxtaposed binding sites are most common [20,21,25,33–36]. Decreasing or increasing this spacing with a half-helical turn (5–6 bp) affects DNA-binding co-operativity, affinity and the resulting regulatory effect ([25,36] and E. Peeters and D. Charlier, unpublished work). Binding sites are not always as well delineated as in the above examples: in some cases, initial binding to a core binding site causes extensive co-operative binding extending in one direction from the nucleation site [18,20,24]. In this additionally bound region, only highly degenerated binding motifs can be recognized.

Molecular mechanisms of transcription regulation The relative positions of TF-binding sites with respect to the promoter and TSS are also constrained. Whether a TF acts as an activator or as a repressor does not depend on a specific DNA-binding mechanism or protein domain, but is usually determined by the binding site location with respect to the promoter (Figure 1A). Although it is difficult to unambiguously predict regulatory effects based merely on these locations, it is clear that activators have a tendency to bind upstream of the promoter and repressors overlapping with or downstream of the promoter.

Repressors Two major repression mechanisms have been described in archaea and archaeoviruses. A first mechanism entails the binding of the TF at a site overlapping the BRE and TATA box promoter elements thereby impairing promoter access for TBP and TFB through steric hindrance [16,19,22,23,37,38]. In a second mechanism, the TF binds to a site downstream of the TATA box. In this case, the binding of TBP and TFB is not prevented, but instead the recruitment of RNAP is inhibited [21,23,33,38–41]. Such a mechanism is employed by the hetero-oligomeric NrpRI–NrpRII repressor complex ¨ and it has in the methanogen Methanosarcina mazei Go1, been demonstrated that this repressor complex establishes protein–protein interactions with TBP and TFB thereby sequestering the basal TFs at the promoter [41]. It is speculated that both repression mechanisms invoke a different responsiveness upon derepression: whereas in the case of TBP/TFB inhibition, the entire PIC needs to  C The

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be formed before transcription can be initiated, the second mechanism allows the pre-bound TBP and TFB to rapidly recruit RNAP after derepression leading to a shorter response time [37]. Depending on the biological function of the target gene(s) and associated input signals, this responsiveness could be crucial for cellular fitness. Curiously, the tryptophanresponsive TrpY of Methanothermobacter thermautotrophicus implements both mechanisms simultaneously by binding the intergenic region of a divergent operon and regulating one arm (trpY-autoregulation) by blocking RNAP recruitment and the other arm (trpEGCFBAD) by inhibiting TBP binding [18]. Not all repression mechanisms observed in archaeal systems can be classified under these two major repression mechanisms: occurrences have been reported of repressors that initially bind only upstream of the core promoter, but displace TBP and TFB by extending this binding further downstream, as has been shown for the RHH-containing AvtR from an archaeal lipothrixvirus [24] and for TrpY [18]. In the latter case, the protein constrains negative supercoils into the DNA.

Activators Characterized transcriptional activators usually bind at a single or primary operator site located immediately upstream or partially overlapping BRE [20,25–27,34,42], which is also called the upstream activating sequence. For traditional 15– 17 bp sites, this binding location positions the TF at the same helical face as the basal TFs (centre-to-centre distance of approximately two helical turns between TF-binding site and TATA box). In the case of Ptr2, it has been demonstrated that this spacing is critical for activation [25]. Auxiliary operator sites are located upstream of the primary site, downstream of the TATA box (as shown for Sta1 [43]), or downstream of the TSS [25]. Exceptions have been described in which TFs activate a promoter from a nucleation site located further upstream with binding progressing towards the promoter at higher concentrations [20,24]. For those activators for which the mechanistic details have been unravelled, it is clear that activation occurs at one of the initial steps of PIC assembly, namely binding of TBP or TFB by means of stimulating protein–protein interactions. In contrast with repressors, which can function in combination with any promoter strength, activators are generally associated with promoters having large deviations from the consensus BRE and/or TATA box sequences [34,42,44]. Furthermore, the activation effect can only be observed in vitro in the presence of minimal concentrations of the basal TFs. Whereas for some activators, specific interactions with either TBP [34] or TFB [42,44] have been demonstrated, other activators such as the gas vesicle regulator GvpE are able to interact with both [45,46]. Moreover, GvpE interacts with five different TBPs of Halobacterium salinarum [45].

Dual regulators Not all TFs in archaea have a dedicated function as either activator or repressor. For example, TrmBL1, Tgr, SurR and

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Figure 2 Autoregulation by the S. solfataricus TF Ss-LrpB (A) Autoradiograph of an in vitro transcription assay with a negatively supercoiled plasmid containing the Ss-lrpB promoter as template. In vitro transcription with Sulfolobus TFs and RNAP was performed as described previously [32]. Each transcription reaction was performed with 100 ng of plasmid DNA, 200 ng of TBP, 200 ng of TFB and 500 ng of RNAP. Synthesized RNA was detected by means of primer extension with a sequence-specific gel-purified 32 P-labelled primer. The RM (recovery marker) is a labelled fragment that was added to the transcription reaction mixtures before extraction and precipitation. Ss-LrpB concentrations are indicated on top of the lanes in nM. The ‘switch’ between activation and repression has been observed repeatedly, with the level of activation being dependent on the transcription conditions (concentrations of active TBP, TFB, RNAP and Ss-LrpB). Below the autoradiograph, a quantification plot is shown. The relative amount of transcripts, normalized against the RM signal and against the transcription level in the reaction without Ss-LrpB (= 1.0), is given as a function of the Ss-LrpB concentration. (B) A hypothetical model of the autoregulatory process of Ss-LrpB. Binding sites of Ss-LrpB (Box1, Box2 and Box3) and the main promoter elements BRE, TATA box and initiator (Inr), containing the first transcribed nucleotide, are indicated (HA, high affinity; LA, low affinity). The scheme displays the major Ss-LrpB-DNA-binding states that exist in a dynamic equilibrium, and the assumed regulatory output (activation or repression) for each of these binding states.

AvtR can perform either function at different promoters depending on the position of the binding site [19,38,40]. We have gathered proof that the HTH-containing TF Ss-LrpB from S. solfataricus can bring on opposite regulatory effects at the same promoter, namely the promoter of its own gene, in a concentration-dependent manner (Figure 2). Ss-LrpB binds three distinct regularly spaced binding sites, coined Box1, Box2 and Box3, immediately upstream of the promoter [35]. The two outer boxes, Box1 and Box3, are high-affinity boxes, whereas the middle box, Box2, exhibits very low binding affinity. Box2 is only stably contacted when both outer boxes are already occupied [35]. Imaging by AFM (atomic force microscopy) showed the formation of a highly dense complexed region in which the DNA appears to be wrapped [47]. The assembly of the Ss-LrpB–operator autoregulatory complex is a complicated process involving the formation of several different binding states and significant conformational changes in the DNA. However, the nature of the resulting

regulatory effects (autorepression and/or autoactivation) is so far unknown. To analyse the effect of Ss-LrpB on gene expression, we conducted an in vitro transcription assay with a reconstituted Sulfolobus transcription system (Figure 2A). Using a supercoiled DNA template containing the Ss-lrpB operator region, we observed a dual regulatory effect of SsLrpB as a function of the protein concentration. At 13 nM Ss-LrpB, the level of transcription increased significantly with respect to the basal level. At a concentration only 4.5-fold higher, Ss-LrpB affected transcription clearly in a negative instead of positive manner. Thus Ss-LrpB autoregulation appears to be a highly sensitive concentration-dependent switch between autoactivation and autorepression. Further experimental work is required to reveal the underlying mechanisms of this complex regulatory response, but it can be envisaged that different binding states exhibit different regulatory outcomes and that Ss-LrpB-induced changes  C The

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in the local DNA topology, caused by the wrapping, in the saturated complex might contribute to the observed repression (Figure 2B).

Concluding remarks Archaeal TFs interact with DNA in a bacteria-like mode, in terms of both binding motif sequences and relative locations with respect to the promoter (i.e. close to or overlapping with the core promoter). However, the mechanisms of the modulation of transcription initiation efficiency are fundamentally different from bacterial TFs given the different nature of the basal transcription machinery. Whereas repressors can inhibit the binding of any of the elements of the PIC, activators interact with TBP and/or TFB. Main tendencies emerge, but despite significant efforts to understand cis-regulatory logic of archaeal TFs, only a minor subset of all existing archaeal TFs have been characterized so far. Therefore it will not be surprising if future investigations unravel a wider variation of regulatory strategies and mechanisms, which might be more complicated than initially thought (as exemplified by Ss-LrpB autoregulation). Furthermore, as in bacterial and eukaryotic organisms, it is anticipated that transcription regulatory networks exist in archaea, which are not yet well understood. In the future, state-of-the-art high-throughput techniques, such as ChIP-seq, SELEX-seq, protein-binding microarrays, microfluidics measurements of protein–DNA interactions and high-throughput gene reporter measurements [48,49], could assist in accelerating the gain in knowledge of DNAbinding specificities of archaeal TFs and the associated cisregulatory rules that determine gene expression output.

Acknowledgements We thank Daniel Charlier for a critical reading of the paper. E.P. is a postdoctoral fellow of the Research Foundation Flanders (Fonds voor Wetenschappelijk Onderzoek – Vlaanderen).

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