Chapter 26Transcription and Translation

Bhattacharyya S, Go MF, Dunn BE, et al.

Publication Details

Regulation of the transcription and translation mechanisms of Helicobacter pylori is presumed to be similar to those of the well-studied Escherichia coli, because both are gram-negative bacteria. Complete DNA sequencing of the genomes of two different strains of H. pylori has allowed the application of powerful sequence homology searches to assign putative functions to various open reading frames (ORFs), leading to hypotheses regarding transcriptional and translational processes in H. pylori genomes (3, 47). In the short time since both genomes were sequenced, a large number of experimental investigations based on sequence analyses have contributed significantly to our understanding of these basic biochemical mechanisms in H. pylori.

Several excellent reviews have summarized information obtained from examination of the published genome sequences of H. pylori (2, 14, 28, 29). This chapter focuses on experimental results dealing with transcription and translation obtained in the past few years.


RNA Polymerase

DNA-dependent RNA polymerase mediates synthesis of RNA from a DNA template. Bacterial RNA polymerases usually consist of four polypeptides: an α subunit dimer (encoded by rpoA gene), a β subunit (rpoB gene), a β′ subunit (rpoC gene), and a σ factor that is responsible for the promoter-specific initiation of transcription (8, 9). The α subunit of RNA polymerase (rpoA gene) is likely encoded by ORF HP1213 (35). Tomb et al. detected an unexpected fusion of rpoB and rpoC genes encoded by ORF HP1198 (47) when they analyzed the H. pylori genome sequence. This unusual fusion of the rpoBC gene was subsequently confirmed in other H. pylori strains and in Helicobacter felis (54). The fused rpoB-rpoC gene encodes a 300-kDa protein that would be a component of the complete RNA polymerase, but assays of the enzymatic activity of the polymerase comprising this fused polypeptide have not been performed (54). Since the genes encoding the β and the β′ subunits are separate in all other bacteria except in gastric Helicobacter sp., it was suggested that the unusual arrangement of these genes might contribute to pathogenesis (54). A genetically constructed fusion of the rpoB-rpoC genes in E. coli increased the efficiency of RNA polymerase assembly in vitro (55). On the other hand, studies with H. pylori containing artificially separated genes encoding β and β′ subunits showed that the bacteria are viable, do not display growth abnormalities, and are able to colonize mice (55). Thus, although H. pylori may derive some advantage from this unique structure, the fusion of rpoB-rpoC genes appears to be an evolutionary accident.

Sigma Factors

On the basis of sequence similarity searches, the H. pylori genome encodes three sigma factors: σ70 factor encoded by the gene HP0088 (rpoD), σ28 encoded by the gene HP1032 (fliA), and σ54 encoded by the gene HP0714 (rpoN) (47). Homologs of the stationary-phase specific sigma factor RpoS, the heat shock protein-specific sigma factor RpoH, or σ32 have not been identified in the two reported genome sequences (3, 47). In E. coli and Salmonella enterica serovar Typhimurium, the onset of stationary phase induces expression of many virulence-specific genes, which require the RpoS sigma factor (4, 12, 13, 49). The absence of an ortholog of rpoS suggests that H. pylori either does not reach or sustains stationary-phase conditions. Alternatively, H. pylori may have RpoS-independent mechanism(s) to regulate gene expression during stationary phase (46). The discovery that H. pylori undergoes spontaneous autolysis toward the end of log-phase growth and the conversion of bacteria into coccoid forms is consistent with these explanations (33). The lack of an identifiable ortholog of rpoH has been interpreted as suggesting that H. pylori may respond to stress differently than other bacteria (5).

The predominant sigma factor in H. pylori is σ70, sometimes referred to as σ80 owing to its larger size (78 kDa) (5). Beier et al. cloned the H. pylori rpoD gene in E. coli and demonstrated that recombinant H. pylori σ70 produced in E. coli is functional and can be incorporated into the E. coli RNA polymerase holoenzyme, but is not interchangeable with E. coli σ70 (5, 52). E. coli RNA polymerases were prepared containing either the E. coli or the H. pylori σ70. The in vitro transcription profile of these polymerases from the H. pylori cagA promoter showed that polymerase containing H. pylori σ70 recognized the cagA promoter more efficiently than those containing the E. coli sigma factor (43). In contrast, polymerase containing H. pylori σ70 recognized the tac promoter (a hybrid of E. coli lactose and tryptophan promoters) poorly compared with polymerase containing the E. coli sigma factor (5). Even more dramatic results were obtained when the tac promoter construct was tested in vivo in H. pylori, which indicated that the tac promoter was not recognized above background level.

These observations indicate that H. pylori σ70 allows the RNA polymerase to recognize specifically H. pylori promoters, although some of its promoters are also recognized in E. coli. The specificity of H. pylori σ70 has been traced to the spacer region between domain 1 and 2 of the H. pylori RpoD protein (5). Shirai et al. reported that hybrids of H. pylori and E. coli RpoD protein have unexpected properties on the basis of their ability to activate promoters in E. coli (40). A mutation in H. pylori rpoD gene could not be isolated, suggesting an absolute requirement of σ70 for the viability of bacteria (5).

H. pylori σ28 and σ54 allow RNA polymerase to recognize genes involved in flagellar biosynthesis (24). In a search for accessory genes regulating σ54-dependent promoters, Spohn and Scarlato selected ORF HP0703, encoding FlgR, as a possible candidate owing to its high homology with the nitrogen regulatory NtrC gene family (42). Studies using E. coli and other bacteria showed that transcription based on σ54-dependent promoters requires a regulatory protein of the NtrC family that binds upstream (>100 bp) from the transcription initiation site (42).

Most genes involved in flagellar biosynthesis require σ54 factor for transcription, and Spohn and Scarlato identified σ54-recognized promoters that regulate transcription of flagellar basal-body and hook genes, as well as enhancer-binding protein FlgR (flagellum regulator protein), a trans-activating protein of the NtrC family (42). These authors constructed an isogenic mutant of ORF HP0703, which was deficient in the transcription of σ54-dependent promoters. This ORF has high sequence similarities with the proteins involved in the regulation of flagellar biosynthesis (42). In bacterial motility assays the mutant shows a loss of motility functions (45). The transcription of σ70-dependent promoters (cagA and ureAB) is unaltered in this mutant, suggesting a specific defect in expression of σ54-dependent promoters (23). In vitro biochemical studies should clarify if ORF HP0703 acts in an analogous manner to the NtrC protein of E. coli (42).

Transcription Termination

In E. coli and other bacteria the precise termination of the RNA transcript requires the presence of termination factors. In E. coli transcriptional termination requires factor Rho (11, 38, 51) or the presence of a stem and loop structure in the RNA (Rho-independent termination) (25, 31, 48). Very few RNA stem and loop structures have been identified in the H. pylori genome, suggesting that accurate termination of transcripts is Rho-dependent (47, 50). Further supporting evidence comes from the finding of termination factor orthologs rho, nusA, nusB, and nusG, which participate in accurate transcription termination in E. coli (37). The roles of the proteins expressed by these genes have not been defined in H. pylori but are presumed to be similar to those of their E. coli homologs.

Establishing and characterizing a random mutagenesis technique for H. pylori, Bijlsma et al. illustrated the importance of experimental studies to complement sequence similarity-based predictions (6). They isolated a urease-deficient mutation owing to an insertion in ORF HP0247, which is annotated as an ATP-dependent RNA helicase (deaD gene) (6). Downstream from ORF HP0247 are ORFs HP0248 and HP0249 of unassigned functions (47). On the basis of sequence similarity searches alone, there was no reason to suspect a specific defect in urease activity owing to loss of function of ORF HP0247, HP0248, or HP0249 (6). The gene(s) responsible for the loss of urease activity and the mechanism remain unknown, but specific interaction of putative deaD with ureAB mRNA is an interesting possibility. Manos et al. also attributed a defect in spontaneous catalase-negative H. pylori mutants to the lack of transcription of the katA gene (27). Although the gene responsible for this defect has not been identified, the inability to detect katA transcript in catalase-negative mutants and the lack of mutations in the promoter or in the katA ORF suggest a transcription-specific defect (27, 30).


H. pylori promoters are classified by the sigma factors involved (or presumed to be involved) to direct their transcription, i.e., the σ70-dependent, σ54-dependent, and σ28-dependent promoters. Table 1 summarizes known properties of various H. pylori promoters.

Table 1. Known properties of various H. pylori promoters.

Table 1

Known properties of various H. pylori promoters.

Role of −10 and −35 Hexamers in Transcription

Forsyth et al. studied the H. pylori vacA promoter using mutational analysis (15). Alignment of the vacA −10 regions of 12 different H. pylori strains revealed a TAAAAA consensus sequence, which matches the consensus E. coli −10 hexamer (TAtaaT) at four of the six positions. The absence of consensus H. pylori −35 sequence suggests that there may be structural differences between H. pylori RpoD and homologous proteins of other bacteria (41). The alignment of vacA −35 regions of H. pylori 26695 with the corresponding domains of other bacterial species reveals a consensus sequence (TTTATG) that matches the consensus E. coli −35 hexamer (TTGACA) at three of the six positions (47) (Table 1). To study the role of the putative vacA −10 hexamer in transcription, the sequence AGATCT was substituted for the native −10 vacA sequence (TAAAAG) of H. pylori 60190. Introduction of this mutation into the chromosome of H. pylori vacA reporter strain 60190 VX-1 resulted in a mutant with 15-fold less D-xylose import (XylE) activity than the control strain, indicating the importance of the −10 sequence in vacA transcription. Of the point mutations in the TGN motifs located at positions −15 to −13, a twofold reduction in vacA transcriptional activity was seen with the mutation at the −14 position (G to T). This suggests that this position, which is located outside the −10 hexamer, may participate in H. pylori RNA polymerase binding (15). Similarly, deletion of six nucleotides (TTTATG) in the −35 region (−37 to −32) results in significant decrease in XylE activity, indicating the involvement of the −35 region in RNA polymerase binding and transcription in H. pylori.


The translational apparatus is required for expression of the genetic information encoded in cells. Components include ribosomes, tRNA, mRNA, numerous ligands, ions, nucleotides, and several proteins, including tRNA-modifying enzymes, aminoacyl-tRNA synthetases, and the proteins transiently associated with ribosomes.

Translational Machinery

Analysis of the H. pylori genome sequence showed the presence of two separate sets of 23S-5S-16S rRNA genes and one 5S rRNA gene (47), which are the major molecular components needed for translation. A total of 36 tRNA genes were found in H. pylori, which are organized in seven clusters and 12 single genes. Orthologs of the genes encoding nine tRNA-modifying enzymes have been found (Table 2), but no ORFs similar to tRNA maturation genes (e.g., rnd, rph, or rnpB) have been identified (28).

Table 2. Putative tRNA-modifying enzymes, related genes, and ORFs.

Table 2

Putative tRNA-modifying enzymes, related genes, and ORFs.

In bacteria the mature 70S ribosomal particle can be dissociated into two subunits, a small 30S and a large 50S subunit (7). A total of 21 ribosomal proteins (S1 to S21) constituting the 30S subunit are encoded by H. pylori. Thirty-one orthologs of the ribosomal proteins encoding the 50S subunit have also been detected (L1 to L7, L9 to L11, L13 to L24, L27 to L29, and L31 to L36). The H. pylori ORFs HP1298, HP1048, and HP0124, homologous to the genes infA, infB, and infC, respectively, in Bacillus spp., participate in the maturation of the initial complex of 70S ribosome with initiation factor fMet-tRNAfMet, mRNA, and GTP. H. pylori encodes four peptide chain elongation factors. These are EF-G (HP1995, fusA), EF-P (HP0177, efp), EF-Ts (HP0177, tsf), and EF-Tu (HP1205, tufB). The ORFs HP0077, HP0171, and HP1256 are orthologs of the genes coding for the three peptide release factors RF-1, Rf-2, and RRF, respectively (47).

Posttranslational Modifications

All the aminoacyl-tRNA synthetases are present in H. pylori except glutaminyl-tRNA synthetase (glnS) and asparaginyl-tRNA synthetase (ansS). Both tRNAGlu and tRNAGln are aminoacylated to glutamate by a single glutamyl-tRNA synthetase in bacterial species. The formation of glutaminyl-tRNA may be accomplished by amidation of glutamate to glutamine in a reaction that is functionally analogous to the glutamine synthetase reaction (44). This transamidation may also occur in H. pylori. However, in H. pylori the product of the second glutamyl-tRNA synthetase encoded by the genes HP0643 and HP0476 (gltX) may perform the function of glutaminyl-tRNA synthetase (47). The H. pylori genome is unique in the absence of an asparaginyl-tRNA synthetase gene. The transamidation process from Asp-tRNAAsn to Asn-tRNAAsn may operate in H. pylori (47) in a manner similar to the archeon Haloferax volcanni (21), which also lacks the asparaginyl-tRNA synthetase gene. Alternatively, this process may be similar to the homologs of the gatABC genes of Bacillus subtilis in which the products of ORFs HP0830, HP0658, and HP0975 can amidate glutamate-charged tRNAs to make glutamine-charged tRNAs. The products of these H. pylori genes may also be responsible for the amidation of the aspartate-charged tRNAs.

In E. coli, proteins PII (GlnB), uridylyltransferase/uridyl-removing enzyme (GlnD), and adenylyl-transferase (GlnE) are required for the posttranslational modification of the glutamine synthetase GlnA (36). E. coli GlnA has 47% homology with H. pylori GlnA, but no E. coli GlnB, GlnD, and GlnE homologs were identified (16) in the H. pylori genome sequences (3, 47). Recent experimental evidence suggests that H. pylori glutamine synthetase (glnA) is not modulated by adenylation (16). The conventional adenylation site has the consensus sequence NLYDLP, which is replaced in H. pylori by NLFKLT (residues 405 to 410) (16, 39). Since Tyr407 residue is the well-conserved target for adenylation, and H. pylori glutamate synthetase lacks that residue, it was concluded that no adenylation occurs for this enzyme within this motif (16, 39). Further analysis of glnA suggests that the activity of H. pylori glutamine synthetase is not modulated by adenylation and therefore not regulated by posttranslational modification (16).

Additional Functions

The antibacterial activity of the cecropin-like amino-terminal polypeptide was reported from the ribosomal protein RpL1 of H. pylori (34). Cecropins are antibacterial polypeptides, composed of two amphipathic α-helices joined by a hinge (20). Unlike several RpL1 proteins from other bacteria, the RpL1 N terminus of H. pylori has the ability to form a perfect amphipathic helix. These antibacterial polypeptides are active against gram-negative E. coli strain D21 and gram-positive Bacillus megaterium strain Bm11, but not against the H. pylori strains tested (34). These peptides may be released in the stomach during bacterial autolysis (33) and act against faster-growing microorganisms.

Regulation of Gene Expression

In E. coli, ppGpp, guanosine-3′-5′-bis(diphosphate), and its analog pppGpp are mediators of the stringent response that coordinates a variety of cellular activities in response to the change in nutritional status. The major trigger for this response is a decrease in the intracellular concentration of aminoacyl-tRNA (10). The gene products involved in this process are ppGpp synthetase I (relA), ppGpp3′-pyrophospho-hydrolase/ppGpp synthetase II (spoT), and ppGpp γ-pyrophosphatase (gpp) (18, 53). No genes related to relA have been identified in either of the published H. pylori genomes, but HP0775 and HP0278 are orthologs of spoT and gppA genes, respectively (47). Therefore, they may be the key elements of the stringent response in H. pylori.

Akada et al. reported the control of the urease operon of H. pylori by mRNA decay in response to environmental pH (1). They concluded that the urease gene cluster of H. pylori consists of two operons, ureAB and ureIEFGH. The latter operon is regulated posttranscriptionally by mRNA decay in response to environmental pH. The ureE″ transcript may contribute to production of the active product for nickel incorporation into the active site during the final step of urease biosynthesis.


Complete DNA sequencing of the H. pylori genome has allowed sequence-similarity comparisons with other gram-negative bacteria. Investigations are in progress to confirm the function of homologous molecules in transcriptional and translational processes. These studies demonstrate the universality of many aspects of structure and function in the gram-negative bacterial species. However, it is clear that H. pylori transcription and translation processes may have important differences from those of E. coli. The significance of these differences, the relationship(s) to bacterial physiology, and the contributions to the pathogenesis of disease processes are under active investigation.


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