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Compilation and analysis of [sigma]54-dependent promoter sequences
Nucleic Acids Research Pages 4305-4313

Compilation and analysis of [sigma]54-dependent promoter sequences
Introduction
The -24/-12 Promoter
Contacts Between [sigma]54 And
Transcriptional Start Sites In -24/-12 Promoters
Spacing Between The -24 And -12
Summary And Conclusions
Acknowledgements
References

Compilation and analysis of [sigma]54-dependent promoter sequences

Humberto Barrios, Brenda Valderrama, Enrique Morett*

Departamento de Reconocimiento Molecular y Bioestructura, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos 62271, México

Received June 1, 1999; Revised and Accepted September 28, 1999

ABSTRACT

Promoters recognized by the RNA-polymerase with the alternative sigma factor [sigma]54 (E[sigma]54) are unique in having conserved positions around -24 and -12 nucleotides upstream from the transcriptional start site, instead of the typical -35 and -10 boxes. Here we compile 186 -24/-12 promoter sequences reported in the literature and generate an updated and extended consensus sequence. The use of the extended consensus increases the probability of identifying genuine -24/-12 promoters. The effect of several reported mutations at the -24/-12 elements on RNA-polymerase binding and promoter strength is discussed in the light of the updated consensus.

INTRODUCTION

The upstream regulatory region of all bacterial genes or operons contains the promoter, that is the DNA sequence which determines specific recognition by the RNA polymerase to initiate transcription. The eubacterial RNA polymerase is a heterotetrameric enzyme constituted by one [beta], one [beta][prime] and two [alpha] subunits (1). This `core' enzyme interacts with the initiation factor [sigma] to form the transcriptionally active holoenzyme (E[sigma]). The addition of the [sigma] factor confers upon the core the specificity for the recognition of promoter sequences.

All known [sigma] factors belong to two different families: those evolutionarily related to the Escherichia coli housekeeping factor [sigma]70, and those related to the alternative factor [sigma]54 (2). Each family of [sigma] factors has different promoter sequence recognition, isomerization and regulation properties. E[sigma]70 does not form stable closed-promoter complexes, therefore transcription can be initiated spontaneously in the absence of activator proteins (3). In contrast, E[sigma]54 forms physically detectable closed-promoter complexes but it is unable to initiate transcription spontaneously. This polymerase is absolutely dependent on additional transcriptional factors, denominated enhancer binding proteins (EBPs), to initiate RNA synthesis (4). E[sigma]54 controls several ancillary processes including the degradation of xylene and toluene, transport of dicarboxylic acids, pilin synthesis, nitrogen fixation, hydrogen uptake (reviewed in 5,13), flagellar assembly (6), arginine catabolism (7), alginate production (8), rhamnolipid production (9), acetoin catabolism (10), mannose uptake (11) and proline iminopeptidase activity (12).

The basic promoters recognized by the E[sigma]70 family, although diverse in sequence, are normally configured around two hexamers centered between -10 and -35 nucleotides upstream from the transcriptional start site (14). In contrast, E[sigma]54 recognizes promoter sequences with conserved GG and GC elements located -24 and -12 nucleotides upstream from the transcriptional start site +1, that is one DNA helical turn closer than the recognition elements in -35/-10 promoters (15). The aim of the present work was the compilation and analysis of -24/-12 promoter sequences reported in the literature, either based on experimental analysis or identified by sequence similarity, and the discussion of possible regulatory implications. With the information obtained we refined the consensus sequence of [sigma]54-dependent promoters and carried out a comparative analysis of the effect of reported mutations affecting some of these promoters.

THE -24/-12 PROMOTER CONSENSUS SEQUENCE

We used three criteria to identify putative -24/-12 promoters: (i) mapped transcriptional start site with or without additional genetic evidence for the promoter; (ii) genetic evidence (mutation or heterologous gene expression); and (iii) putative promoters reported in the literature on the basis of sequence similarity to the -24/-12 elements. A collection of 186 sequences satisfying any of the three selection criteria is shown in Table 1. The nucleotide sequences were obtained from GenBank through the National Institute of Health server (http://www3.ncbi.nlm.nih.gov/entrez/ ). The sequence of each promoter including 10 nucleotides upstream and 10 nucleotides downstream from the highly conserved -24/-12 elements is shown in Table 1. For 85 of these promoters their transcriptional start site has been experimentally determined. A list of identified EBPs activating each promoter or the presence of putative EBP binding sites is included in Table 2 for the cases reported. The relative nucleotide frequency at each position and the consensus sequence for each subgroup and for the whole collection is shown in Figure 1.


Figure 1. Relative frequency of each nucleotide per position and consensus sequences of the -24/-12 promoters. (A) Entire collection of the 186 -24/-12 promoters and putative promoters; (B) the 85 promoters with mapped transcriptional start sites; (C) the 101 putative promoters without mapped transcriptional start sites; (D) dinucleotide frequency composition of the 85 promoters with mapped transcriptional start sites. R, purines; Y, pyrimidines; W is A or T. Poisson statistics were used to express the standard deviation for each nucleotide (53).


Table 1. Nucleotide sequence of the 186 -24/-12 promoters used in this study
The first column is the gene name and the second column the organism name abbreviated as follows: Al.den, Alcaligenes denitrificans; Al.eut, Alcaligenes eutrophus; A.fae, Alcaligenes faecalis; Az.bra, Azospirillum brasilense; Az.cau, Azorhizobium caulinodans; Az.vin, Azotobacter vinelandii; Az.chr, Azotobacter chroococcum; Bc.sub, Bacillus subtilis; Br.jap, Bradyrhizobium japonicum; Cw.rhi, Cowpea Rhizobium; Cm.col, Campylobacter coli; Cl.cre, Caulobacter crescentus; En.agg, Enterobacter agglomerans; En.clo, Enterobacter cloacae; Er.chr, Erwinia chysanthemi; Es.col, Escherichia coli; Hr.ser, Herbaspirillum seropedicae; Kl.aer, Klebsiella aerogenes; Kl.oxy, Klebsiella oxytoca; Kl.pne, Klebsiella pneumoniae; Mb.the, Methanobacterium thermoautotrophicum; Mc.cap, Methylococcus capsulatus; Mx.xan, Myxococcus xanthus; Ns.gon, Neisseria gonorrhoeae; Pr.rhi, Parasponia Rhizobium; Pt.vul, Proteus vulgaris; Ps.aer, Pseudomonas aeruginosa, Ps.put, Pseudomonas putida, Ps.syr, Pseudomonas syringae; Rh.leg, Rhizobium leguminosarum; b.pha, Rhizobium leguminosarum biovar phaseoli; b.tri, Rhizobium leguminosarum biovar trifolii; b.vic, Rhizobium leguminosarum biovar viciae; Rh.mel, Sinorhizobium meliloti; Rh.pha, Rhizobium phaseoli; Rh.sp, Rhizobium sp.; Rh.BT, Rhizobium BTAi1; Rh.tri, Rhizobium trifolii; Rh.pNG, Rhizobium plasmid NGR2; Rb.cap, Rhodobacter capsulatus; Rs.rub, Rhodospirillum rubrum; Rs.cen, Rhodospirillum centenum; Th.fer, Thiobacillus ferrooxidans; Sl.typ, Salmonella typhimurium; Vb.alg, Vibrio alginolyticus; Vb.cho, Vibrio cholera. TSS, transcriptional start site. Promoter sequences from 47 organisms are represented in our study. However, for only 33 of them has the rpoN gene been identified and sequenced.

Table 2. Regulatory features derived from the analysis of the 186 -24/-12 promoters used in this study
Organism names are as in Table 1. TSSD, distance from the transcriptional start site to the C of the conserved -12 element; EBP, experimentally identified activator of the EBP family; Bin.site, possible EBP binding site identified by sequence similarity; Distance, the distance from the second G of the -24 element to the EBP binding site.

The consensus sequences shown in Figure 1 are depicted following a previously reported definition (14), where any nucleotide occurring with a frequency of more than six standard deviations from the expected random occurrence of each nucleotide (0.25) is denoted highly conserved (upper case), between three and six standard deviations is denoted weakly conserved (lower case), and below three standard deviations is not significant (N). As previously reported, the highest conservation was found around the -24 and the -12 elements (15). Around the -24 element, from position -31 to -20, there are eight highly conserved and three weakly conserved nucleotides with the sequence mrNrYTGGCACG (Fig. 1). Around the -12 element (positions -15 to -8), there are five highly conserved and one weakly conserved nucleotides with the sequence TTGCWNNw. Thus, the mrNrYTGGCACG-N4-TTGCWNNw sequence is the updated consensus for the -24/-12 promoters.

The subgroup with mapped transcriptional start site presented the extended consensus sequence but not the subgroup without mapped transcriptional start site (compare Fig. 1B and C). This discrepancy probably reflects the inclusion of incorrectly assigned -24/-12 promoter sequences in the compilation of the latter group. When the consensus sequence is displayed as the most frequent dinucleotide (Fig. 1D), it becomes apparent that at some positions one type of dinucleotide is strongly favored. For example, at position -14 T is by far the most abundant nucleotide (85%) but the presence of a pyrimidine is almost 100% conserved. Similarly, at positions -20 and -21 R and Y are >90% conserved.

A comparison of the consensus sequence derived by group and the relative occurrence of the most common nucleotide at each position is shown in Table 3. In the subgroup with mapped transcriptional start site, the G at the -24 position is 100% conserved; the G at the -25 position is 99% conserved, with the exception of the Myxococcus xanthus gene 4521 promoter (16,17); the G at the -13 position is 96% conserved with the exception of the Pseudomonas aeruginosa oprE (18), the E.coli glnH and the Neisseria gonorrhoeae pip (12,19) promoters; whereas the C at the -12 position is 96% conserved with the exceptions of the Alcaligenes eutrophus hoxK (20), the E.coli pspA (21), the Rhizobium leguminosarum biovar viciae nifH (22) and the Rhodospirillum rubrum glnB (23) promoters.


Table 3. Comparison of -24/-12 promoter consensus sequences
Numbers under the sequences represent the relative occurrence of the nucleotide at that position (percent).
A, consensus sequence from the 186 compiled promoters.
B, consensus sequence from 85 promoters with mapped transcriptional start site.
C, consensus sequence from 101 putative promoters without mapped transcriptional start site.
D, consensus sequence obtained from the comparison of groups A, B and C.

CONTACTS BETWEEN [SIGMA]54 AND THE PROMOTER IN CLOSED COMPLEXES AND RELEVANCE OF EACH POSITION

Comparison of the deduced protein sequences of the [sigma]54 factors showed that they are highly conserved (24): two well characterized motifs, a helix-turn-helix and a highly conserved sequence of 10 amino acids known as RpoN-box, are involved in the recognition of the -24 and -12 promoter elements, respectively (25-27). The promoter residues contacted by E54[sigma] have been extensively described (28-31): [sigma]54 contacts actually extend from positions -31 to -5, although only for the GG and GC dinucleotides at positions -24 and -12 have specific protein-DNA interactions been detected (30). Further addition of the core polymerase induces a distortion downstream from the -12 element but the reactivity towards methylating reagents did not change, indicating that the core subunits do not contact the promoter directly but through [sigma]54 (29,30,32). It has been proposed that the -24 element functions as an attachment determinant for E[sigma]54 whereas the -12 element is involved in the fine modulation of an already established closed-complex towards its isomerization (33).

Mutations reported elsewhere helped to identify positions critical for the promoter function (16,27,34-38). Table 4 shows several reported mutations in -24/-12 promoters and a quantitative analysis of their effect. All the changes in the highly conserved positions -25/-24 and -13/-12 are down-mutations, reducing drastically the binding of E[sigma]54 (31,33) and the expression, except for the M.xanthus 4521 gene promoter which has an A at -25 (Table 4, lane E) (39). Qualitatively, similar changes reported in the Azorhizobium caulinodans nifA (40), the Caulobacter crescentus flbG and flaN (41-43) and the Klebsiella pneumoniae nifH (44) promoters, also presented a down-phenotype. Mutations in the K.pneumoniae nifH promoter at the -26 and -16 positions decreased the expression by 25% and at the -15 position by 75% (35,37), whereas simultaneous mutations at the -17, -16 and -15 positions decreased the expression by 55% (Table 4, lane C) (35). The substitution of the latter residues for three Ts enhanced the [sigma]54 and E[sigma]54 binding affinities both in vivo and in vitro (31,40,45). Mutations around the -24 region that increased the similarity to the consensus; for example, a change of G for A at the -22 position in the K.pneumoniae nifL promoter, enhanced the expression level more than 2-fold (34).


Table 4. Effect of some mutations in -24/-12 promoters
Relative values (%) are shown in parentheses.
A, consensus sequence from the -24/-12 promoters with mapped transcriptional start sites derived from this analysis.
B, mutant forms of the K.pneumoniae nifL promoter (34,37).
C, mutant forms of the K.pneumoniae nifH promoter (35-37).
D, mutant forms of the B.subtilis levD promoter (38).
E, mutant forms of the M.xanthus 4521 gene promoter (16).
F, mutant forms of the K.pneumoniae glnA promoter (27).

TRANSCRIPTIONAL START SITES IN -24/-12 PROMOTERS

[sigma]70-Dependent promoters generally initiate transcription at a purine, adenine being more frequently utilized than guanine (14). The selection of this nucleotide is influenced by the sequence around -35 and by the composition of the -2 to -5 positions (46,47). In our collection of 85 [sigma]54-dependent promoters with a mapped transcriptional start site a significant proportion of them (64%) also initiate transcription at a purine (Fig. 2). In [sigma]70-dependent promoters the spacing between the first nucleotide of the -10 element and the transcriptional start site is usually 6 or 7 nt, although functional examples between 4 and 10 nt have been reported (14).


Figure 2. Distribution of transcriptional start sites for the 85 -24/-12 promoters. The reference position is the conserved C of the -12 element.

The first group of -24/-12 promoters being characterized initiate transcription precisely 12 nt downstream from the conserved GC element; this coincidence led to the operational designation of these promoters as -24/-12 (15). Our updated compilation of 85 promoters with mapped transcriptional start sites from 28 different species provides evidence that the initial nucleotide selection is more flexible than initially considered. In Figure 2 we present these data as a Gaussian distribution similar to that obtained from the analysis of [sigma]70-dependent promoters from Bacillus subtilis and E.coli (48,49), with the significant difference that instead of the preferential use of a single position, the use of nucleotides 11, 12 and 13 downstream from the GC for initiation of transcription is roughly equally frequent (24, 20 and 27% respectively).

A few examples of transcripts starting 3 nt before and after positions 11-13 have been also described and were included in the analysis. The shortest distance reported is 8 nt for the Parasponia rhizobium nifH (50), the Rhodospirillum centenum cheAY (51) and the R.rubrum nifJ (52) promoters. At present, there are no reported examples of transcriptional starts between 17 and 20 nt. The longest distance reported is 21 nt for the P.aeruginosa algD promoter (53,54). Based on these results it is not possible to predict accurately a transcriptional start site for -24/-12 promoters based solely on the promoter sequence.

SPACING BETWEEN THE -24 AND -12 CONSERVED ELEMENTS

The optimal spacing between the -35 and -10 elements in [sigma]70-dependent promoters is 17 +/- 1 nt, but functional promoters with spacing between 15 and 20 non-conserved nucleotides have been reported (14,55). In contrast, deletions of one or more nucleotides in the stretch between the -24/-12 elements abolished promoter function (16,36,41-43). Thus, a stringent requirement for these motifs to be positioned on the same face of the DNA helix seems to be a necessary condition for the binding of E[sigma]54. Although there are no published examples of nucleotide insertions between the -24/-12 elements, it is reasonable to predict that any insertion might severely disrupt promoter function.

SUMMARY AND CONCLUSIONS

Here we present an updated compilation of [sigma]54-dependent promoters and the derivation of an extended consensus sequence. The new consensus extends from positions -8 to -31 relative to the transcriptional start site (Fig. 1 and Table 3). Interestingly, the observed contacts of [sigma]54 with the promoter DNA span exactly this length (30). Although the informational content of the extended consensus sequence is still low to accurately predict -24/-12 promoters, profile searches using this sequence increased 4-fold the probability of identifying bona fide promoters in the bacterial subgroup of the EMBL/GenBank database, compared to the previous consensus (data not shown).

The consensus sequence derived from our collection of 186 -24/-12 promoter elements and putative promoter elements from 47 different bacterial species shows a remarkable conservation both in sequence and in structure in contrast to the flexible consensus derived from [sigma]70-dependent promoters. This conservation symbolizes the strict requirements for promoter recognition and function required for a highly controlled regulation.

ACKNOWLEDGEMENTS

We wish to thank Ricardo Grande and Mariana Peimbert for their comments on the manuscript. This work was supported in part by a grant from Consejo Nacional de Ciencia y Tecnología (Conacyt). H.B. was recipient of a Conacyt scholarship.

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