Bioinformatics Advance Access originally published online on March 16, 2006
Bioinformatics 2006 22(11):1297-1301; doi:10.1093/bioinformatics/btl096
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Cyanobacterial response regulator PatA contains a conserved N-terminal domain (PATAN) with an alpha-helical insertion
1 National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health Bethesda, MD 20894, USA
2 Department of Molecular Genetics and Cell Biology, University of Chicago Chicago, IL 60637, USA
*To whom correspondence should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONRESULTSDISCUSSIONREFERENCES |
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The cyanobacterium Anabaena (Nostoc) PCC 7120 responds to starvation for nitrogen compounds by differentiating approximately every 10th cell in the filament into nitrogen-fixing cells called heterocysts. Heterocyst formation is subject to complex regulation, which involves an unusual response regulator PatA that contains a CheY-like phosphoacceptor (receiver, REC) domain at its C-terminus. PatA-like response regulators are widespread in cyanobacteria; one of them regulates phototaxis in Synechocystis PCC 6803. Sequence analysis of PatA revealed, in addition to the REC domain, a previously undetected, conserved domain, which we named PATAN (after PatA N-terminus), and a potential helix–turn–helix (HTH) domain. PATAN domains are encoded in a variety of environmental bacteria and archaea, often in several copies per genome, and are typically associated with REC, Roadblock and other signal transduction domains, or with DNA-binding HTH domains. Many PATAN domains contain insertions of a small additional domain, termed 
-clip, which is predicted to form a four-helix bundle. PATAN domains appear to participate in protein–protein interactions that regulate gliding motility and processes of cell development and differentiation in cyanobacteria and some proteobacteria, such as Myxococcus xanthus and Geobacter sulfurreducens.
Contact: galperin{at}ncbi.nlm.nih.gov
Supplementary information: http://www.ncbi.nlm.nih.gov/Complete_Genomes/SigCensus/PATAN.html
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONREFERENCES |
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The ability of certain bacteria to form multicellular aggregates or filaments is a fascinating and poorly understood phenomenon that has the potential to provide insight into eukaryotic cell development (Haselkorn, 1998; Kaplan, 2003; Søgaard-Andersen, 2004). The filamentous cyanobacterium Anabaena PCC 7120 is a convenient model organism for studies of bacterial cell differentiation (Wolk, 1996; Kaneko et al., 2001; Ehira et al., 2003; Zhang et al., 2006). In response to starvation for fixed nitrogen, certain vegetative cells of Anabaena differentiate into nitrogen-fixing cells called heterocysts. Heterocysts do not conduct oxygenic photosynthesis and are surrounded by thick glycolipid cell walls, which allow them to maintain an anaerobic environment required for the nitrogenase activity. Heterocysts are regularly spaced, comprising approximately every 10th cell in the filament (Haselkorn, 1998). Heterocyst formation is subject to a complex regulation which includes the products of more than 10 genes, including patA, patB, patN, patS, hetN, hetR, hglB (hetM) and some others (Wolk, 1996; Adams, 2000; Meeks and Elhai, 2002; Golden and Yoon, 2003).
One of the components of the heterocyst formation regulatory system is an unusual response regulator PatA (Liang et al., 1992) that contains a CheY-like phosphoacceptor (receiver, REC) domain (listed as domain PF00072 in the Pfam database, Bateman et al., 2004) at its C-terminus. PatA mutants develop heterocysts mostly at the ends of filaments and grow poorly under nitrogen-fixing conditions (Liang et al., 1992). A recent census of response regulators in sequenced prokaryotic genomes revealed multiple copies of PatA-type response regulators encoded in various cyanobacterial genomes (Galperin, 2006). In addition, sequences related to the N-terminal domain of PatA were detected in a variety of diverse bacteria. We report here a detailed sequence analysis of PatA, which revealed three novel conserved domains, and discuss their potential roles in prokaryotic signal transduction.
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RESULTS |
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Domain organization of the PatA protein
Sequence analysis of the PatA protein from Anabaena (Nostoc) PCC 7120 (All0521, UniProt accession no. P39048 [GenBank] ) revealed a complex domain organization, in accordance with an earlier conclusion (Liang et al., 1992) that PatA consists of three distinct domains. In addition to the C-terminal REC domain of PatA, we detected an N-terminal conserved domain, hereafter called PATAN (‘pattern’, after PatA N-terminus) domain, and a disrupted helix–turn–helix (HTH) domain in the middle of the protein (see below).
PSI-BLAST (Altschul et al., 1997) searches with inclusion cut-off E-value of 0.05 started with the 190 amino acid N-terminal fragment of PatA retrieved 
120 sequences from various prokaryotes. Most of the hits were from cyanobacteria and 
-proteobacteria, but putative PATAN domains were also detected in certain representatives of Actinobacteria, Aquificae, Chloroflexi, Deinococcus/Thermus group and in several archaea (see Table 1 in the Supplementary Materials). While this domain had not been listed in public domain databases, N-terminal regions of 10 cyanobacterial PatA proteins have been included in the ProDom database (Bru et al., 2005) as family PD017487 and in Pfam_B as domain PB009947. A list of PATAN-containing proteins with several convenient query sequences and corresponding PSSMs for PSI-BLAST searches are available in the Supplementary Material.
While patA is so far the only experimentally characterized PATAN-encoding gene, two genes of this family have been identified in mutation screens. One of the six patA-like genes from Synechocystis sp. PCC 6803 (sll0038) is involved in phototaxis and has been named taxP1 gene (Yoshihara et al., 2000; Bhaya et al., 2001). In Myxococcus xanthus, a PATAN-containing protein is required for adventurous gliding motility (Youderian et al., 2003). Finally, a patA-containing contig from Fremyella diplosiphon (also called Calothrix sp. PCC 7601) showed an apparent increase in expression when illuminated with red light as compared with green light (Stowe-Evans et al., 2004).
PSI-BLAST-generated multiple sequence alignment of various PATAN domains, combined with secondary structure prediction using several different algorithms (Cuff et al., 1998; Jones, 1999; Kelley et al., 2000), produced a fairly consistent picture of four ß-strands flanked by two -helices (Fig. 1). However, the region between ß-strands 3 and 4 varied in length from 16 to 84 amino acid residues and contained from 1 to 4 predicted -helices, indicating the presence of an insertion domain (Fig. 2). Using a 65 amino acid fragment of Geobacter sulfurreducens protein GSU0213 (UniProt entry Q74GN3), roughly corresponding to this insertion (amino acid residues 55–119), as a query in a PSI-BLAST search with inclusion threshold E-value of 0.1 retrieved a large number of proteins, of which many belong to COG2804 in the COG database (Tatusov et al., 2000) and have been annotated as type II secretory pathway ATPase PulE and/or type IV pilus assembly pathway ATPase PilB. Other hits included enterobacterial bacteriophage N4 receptor protein NfrB, -proteobacterial chemotaxis histidine kinase CheA and a variety of uncharacterized multidomain proteins (see Fig. 3 in the Supplementary Materials). Some of these proteins produced two distinct hits, suggesting that this small insertion domain was tandemly duplicated. Indeed, a 30 amino acid-long overlap in these hits was detected, indicating the presence of a repeat unit of 30 amino acid residues. Furthermore, a weak (E-value 0.1–0.5) but reproducible similarity with TPR repeats was observed in many searches starting from different query sequences of this insert domain. In proteins of the PulE/PilB and NfrB families, the query sequence mapped to the region preceding the GspII_E_N domain (PF05157), previously observed in the N-terminal region of the XpsE protein (PDB: 2d27) and found to form a distinct four-helical bundle domain (Chen et al., 2005). Taken together, these observations suggested that the insertion in the PATAN domain is another distinct, small domain (hereinafter, -clip domain) that contains two repetitive units, each formed by two antiparallel -helices (in some PATAN domains, these four -helices are reduced to two or just one). Given that such helical units are mostly found in multidomain proteins that form regulatory protein complexes (Possot et al., 2000; Ulrich and Zhulin, 2005), the -clip domain is likely to have the same function as TPR repeats, namely, facilitating protein–protein interactions (Groves and Barford, 1999). Several cyanobacteria encode a family of proteins, exemplified by Thermosynechococcus elongatus protein Tlr1669, which consist entirely of -clip domains and might also participate in protein–protein interactions.
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Threading the predicted structure of the PATAN domain against a library of known structural folds using GenThreader and 3D-PSSM (Jones, 1999; Kelley et al., 2000) returned no reliable hits, suggesting that PATAN might have a novel structure. However, the predicted organization of the PATAN domain with its four-strand antiparallel ß-sheet and two flanking
-helices is suggestive of the profilin fold, which is found in a variety of ligand-binding signaling domains, including PAS, GAF and Roadblock/LC7 (Taylor and Zhulin, 1999; Ho et al., 2000; Lunin et al., 2004). Sequence analysis of the 60 amino acid middle region of the PatA family proteins from cyanobacteria revealed a conserved HTH motif similar to the ones in the transcriptional regulators of the ArsR family (see Fig. 4 in the Supplementary Materials). Thus, cyanobacterial PatA family proteins can be predicted to bind DNA and regulate transcription. However, in the original PatA protein from Anabaena PCC 7120, the HTH domain appears to be disrupted, suggesting that this protein has lost DNA-binding properties.
Domain architectures of PATAN-containing proteins
In cyanobacteria, PATAN domains are almost invariably found in association with HTH and REC domains, which conforms to the canonical domain architecture of response regulators of PatA type (Fig. 2). The number of patA paralogs per genome generally correlates with the genome size but not with the ability of cyanobacteria to form heterocysts (Table 1). Indeed, genomes of non-heterocystous cyanobacteria Crocosphaera watsonii and Synechocystis sp. PCC 6803 encode more PatA-like proteins than heterocystous Anabaena PCC 7120 and Anabaena variabilis. However, the relatively large genome of the early-branching cyanobacterium Gloeobacter violaceus encodes only a single PatA-type regulator with a truncated PATAN domain, which might be related to the fact that G.violaceus does not form thylakoids. The notion that the functions of PatA-type response regulators go beyond regulation of heterocyst formation is also supported by experimental data on their involvement in phototaxis and response to low temperature in Synechocystis sp. PCC 6803 (Suzuki et al., 2000; Yoshihara et al., 2000; Bhaya et al., 2001).
While the presence of PatA-type response regulators appears to be a specifically cyanobacterial trait, other bacteria and archaea encode combinations of the PATAN domains with predicted HTH domains that are likely to function as transcriptional regulators. There are also PATAN-containing response regulators that have the characteristic domain organization with the REC domain at their N-termini (Fig. 2). In addition, the PATAN domain is often found in combination with other signaling domains, such as Roadblock/LC7, TPR, cNMP-binding domain and the recently described HD-superfamily response output domain, HDOD (PF08668; Galperin, 2004, 2006). In several -proteobacteria, the PATAN domain is fused to FRGAF (FrgA-GAF, see Fig. 5 in the Supplementary Materials), a distinct variant of the GAF domain (Aravind and Ponting, 1997) that is found in the M.xanthus protein FrgA (UniProt entry Q9RF11), which is involved in the regulation of M.xanthus fruiting body formation (Cho et al., 2000). Domain architectures of PATAN-containing proteins support the hypothesis that the PATAN domain is a signaling domain that participates in prokaryotic cell development and differentiation. After the REC and HTH domains, the third domain most commonly associated with PATAN is the Roadblock/LC7 (PF03259) domain (Bowman et al., 1999; Koonin and Aravind, 2000). This association could already be seen in the original description of the prokaryotic Roadblock/LC7 (MglB-family) domain, which showed the genomic context of the Roadblock/LC7 in Aquifex aeolicus: the PATAN-HTH-encoding aq_1845 gene, sandwiched between mglB-like aq_1847 and the mglA-like aq_1844 gene, has been marked as an uncharacterized gene (Koonin and Aravind, 2000). Adjacent genes encoding PATAN and Roadblock/LC7 domains are also found in many other genomes, including bacteria Deinococcus radiodurans, Chloroflexus aurantiacus, each of the three PATAN-encoding actinobacterial genomes (Nocardia farcinica, Streptomyces avermitilis, Streptomyces coelicolor), as well as in archaea Archaeoglobus fulgidus and Methanothermobacter thermautotrophicus. Most -proteobacteria encode at least one fusion protein that combines PATAN and Roadblock/LC7 domains.
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DISCUSSION |
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Despite the abundance of PATAN-encoding genes in bacterial genomes, only three of them have known mutant phenotypes. These include the Anabaena patA gene that is required for heterocyst formation (Liang et al., 1992), the taxP1 gene (sll0038) in Synechocystis sp., involved in phototaxis (Yoshihara et al., 2000; Bhaya et al., 2001) and response to low temperature (Suzuki et al., 2000) and a gene that is required for adventurous gliding motility in M.xanthus (Youderian et al., 2003). Microarray experiments identified two patA-like genes as the ones induced by red light (Stowe-Evans et al., 2004) and by low temperature (Ehira et al., 2005). These phenotypes, as well as domain combinations formed by PATAN (Fig. 2), indicate that the PATAN domain is a novel component of prokaryotic signal transduction machinery. In cyanobacteria and
-proteobacteria, PATAN-containing proteins are involved in chemotaxis and in regulation of complex developmental processes, such as formation of heterocysts (Anabaena) or pili and fruiting bodies (M.xanthus). The exact function of the PATAN domain remains unclear; the absence of universally conserved amino acid residues (Fig. 1) makes it unlikely that this domain has an enzymatic activity. However, the predicted structural similarity with PAS and GAF domains suggests that, like these domains, PATAN binds specific ligands. Ligand-binding by the PATAN domain might modulate DNA-binding by the HTH domains of predicted transcriptional regulators with PATAN–HTH domain architecture (Fig. 2). In cyanobacterial PatA-type response regulators, which additionally contain the -clip (Fig. 3 in Supplementary Material) and REC domains, DNA-binding by the predicted HTH domain (Fig. 4 in Supplementary Material) could be additionally modulated by phosphorylation of the REC domain by a two-component sensor kinase and/or protein–protein interactions mediated by the -clip domain.
Cyanobacterial patA genes are mostly found in chemotaxis operons (Bhaya et al., 2001), suggesting that their role involves transduction of environmental signals sensed by the chemotactic machinery. An additional function of the PatA protein in Anabaena is implied by the observation that sonicated filaments, so shortened that the terminal heterocysts make up >10% of the cells, nevertheless grow very slowly on N2 as nitrogen source (Liang et al., 1992). This observation was interpreted to mean that PatA functions in N2 reduction or in the transport of fixed nitrogen to neighboring vegetative cells. A phylogenetic tree of cyanobacterial PATAN domains (see Fig. 6 in the Supplementary Materials) shows four clear branches, which indicates that these groups have diverged early in cyanobacterial evolution and might reflect their functional divergence. It must be noted that PATAN domains are absent in marine picocyanobacteria with their relatively small genome sizes (Table 1). They are also missing in such -proteobacteria as Desulfovibrio vulgaris, which otherwise has a fairly sophisticated signal transduction system (Galperin, 2005). In contrast, some other -proteobacteria encode multiple PATAN-containing proteins (Table 1). The reasons for such a phyletic distribution remain unknown and might reflect still poorly understood peculiarities of signal transduction in these bacteria.
In other organisms, frequent association of the PATAN domain with the Roadblock/LC7 domain and occasional association with the GSPII_E_N domain suggest that PATAN participates in multiprotein signaling complexes that could also include MglA-like GTPases, MasK-like Ser/Thr protein kinases (Thomasson et al., 2002) and a variety of other proteins. The identification of the PATAN domain should help in the identification of additional components of this complex signal transduction machinery and in understanding its role(s) in the regulation of prokaryotic cell motility, development, and differentiation.
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Acknowledgments |
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The authors thank Patricia Hartzell for helpful discussion. This work was supported by the Intramural Research Program of the National Library of Medicine at the US National Institutes of Health. Funding to pay the Open Access publication charges was provided by the Intramural Research Program of the NIH, National Library of Medicine.
Conflict of Interest: none declared.
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FOOTNOTES |
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Associate Editor: Alex Bateman
Received on February 18, 2006; revised on March 9, 2006; accepted on March 10, 2006
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