Analysis of the lambdoid prophage element e14 in the E. coli K-12 genome
© Mehta et al; licensee BioMed Central Ltd. 2004
Received: 22 June 2003
Accepted: 20 January 2004
Published: 20 January 2004
Many sequenced bacterial genomes harbor phage-like elements or cryptic prophages. These elements have been implicated in pathogenesis, serotype conversion and phage immunity. The e14 element is a defective lambdoid prophage element present at 25 min in the E. coli K-12 genome. This prophage encodes important functional genes such as lit (T4 exclusion), mcrA (modified cytosine restriction activity) and pin (recombinase).
Bioinformatic analysis of the e14 prophage sequence shows the modular nature of the e14 element which shares a large part of its sequence with the Shigella flexneri phage SfV. Based on this similarity, the regulatory region including the repressor and Cro proteins and their binding sites were identified. The protein product of b1149 was found to be a fusion of a replication protein and a terminase. The genes b1143, b1151 and b1152 were identified as putative pseudogenes. A number of duplications of the stfE tail fibre gene of the e14 are seen in plasmid p15B. A protein based comparative approach using the COG database as a starting point helped detect lambdoid prophage like elements in a representative set of completely sequenced genomes.
The e14 element was characterized for the function of its encoded genes, the regulatory regions, replication origin and homology with other phage and bacterial sequences. Comparative analysis at nucleotide and protein levels suggest that a number of important phage related functions are missing in the e14 genome including parts of the early left operon, early right operon and late operon. The loss of these genes is the result of at least three major deletions that have occurred on e14 since its integration. A comparative protein level approach using the COG database can be effectively used to detect defective lambdoid prophage like elements in bacterial genomes.
Bacterial genomes harbor several types of mobile elements including transposons, insertion elements and temperate bacteriophages, both functional and defective. These elements can encode various important functions, including toxins, virulence factors, bacteriophage resistance, restriction modification systems and antibiotic resistance . Prophages, both intact and defective, have a special role in this context as they are resident elements and play a special role in the physiology of the host bacteria. They have been implicated in serotype conversion, pathogenesis and phage immunity [reviewed by [2, 3]].
The temperate lambda-like (lambdoid) phages have highly mosaic genomes with respect to each other. This forms the basis of the "modular genome hypothesis" proposed by Botstein in 1980 . According to this hypothesis phages evolve by interchanging genetic elements (modules), each of which can be considered as a functional unit [5, 6]. In spite of this diversity, E. coli and other enterobacterial genomes are recognized to contain a number of lambda-like cryptic prophages [reviewed by [7, 8]]. For example the very well characterized E. coli K-12 genome carries eight convincingly identified prophages (λ itself and seven others; all of the latter are defective and six, DLP-12, e14, Rac, QIN, CPS-53, and Eut, are thought to be lambdoid in nature [reviewed by [7, 9, 10]]). The high rate of recombination, deletions and insertions present in such cryptic phage elements makes their unambiguous detection and determination of evolutionary linkages difficult (see below).
The e14 element, the subject of this report, is one such defective prophage element that is integrated into the E. coli K-12 genome at 25 min on the chromosome within the isocitrate dehydrogenase (icd) gene [11, 12]. The sequence of the e14 element is available with the sequencing of the E. coli K-12 genome; it is 15.4 kbp long and lies between 1195432 bp and 1210646 bp on the K-12 chromosome . The element has at one end 216 bp of homology with the C-terminal end of the host icd gene, and the actual crossover for integration (the attachment site) occurs between the first 11 bp at one end of the homology in e14 and an 11 bp sequence inside the host icd gene . The integration event fused the e14 "icd replacement region" to the N-terminal portion of the host icd gene, causing only two amino acid changes in the isocitrate dehydrogenase protein . The element is capable of excision if the host SOS response is triggered. Both excision and re-integration occur in a site-specific manner [11, 15]. e14 shares its integration site with phage 21 and has a similar integration machinery to that of phage 21; both have slightly overlapping int and xis genes. These two genes are transcribed leftward and lie about 3 kb from the e14 att site [12, 14]. However, e14 and phage 21 must have different specificities of site recognition since phage 21 Int and Xis cannot cure cells of the e14 element as demonstrated by Wang et al. .
Experimental data on e14 is scattered in the scientific literature. The e14 element was originally identified by Greener and Hill , and mapped on the E. coli K-12 chromosome and cloned by Plasterk et al. [17, 18] and Maguin et al. . A restriction map of the element was made which largely corresponds with the now available sequence . Current E. coli genome databases attribute 20/21 ORFs to the e14 element [20–22]. Most of these are annotated as putative or hypothetical proteins and very few have a functional annotation. The element is known to encode several important functions including the lit gene involved in T4 exclusion [23, 24], the rglA (mcrA) gene involved in restriction of hydroxymethylated non-glucosylated T4 phages [25, 26], the pin gene involved in inversion of an adjacent 1794 bp segment within e14 [17, 27]. In addition to these, it is also attributed to encode a kil function and a concomitant repressor protein , and an SOS induced cell division inhibition function attributed to the sfiC gene [19, 28]. Defined regions of e14 encoding these latter functions have been implicated by mapping the kil, repressor and sfiC functions. However the actual genes corresponding to these functions have not been previously identified. Recent sequencing of numerous bacteriophage genomes now allows a much more sophisticated bioinformatic analysis of its genetic content and prediction of the function of many of the e14 genes.
E. coli is perhaps the best-understood cellular organism, and K-12 is the most highly studied E. coli strain. If this model genome is to be completely understood, and this goal now seems achievable, it is essential that we understand its prophage elements. Here, we use a sequence analysis approach to further understand the evolution, and phage- and host-related functions of the e14 element.
Results and Discussion
Overall genetic structure of e14
Annotation of genes encoded by the e14 element. The functional annotation of the e14 genes along with the BLAST and FASTA hits, the closest structural homolog if any and the cluster to which the gene belongs are listed. TM indicates the transmembrane region, SS presence of signal sequence, COG, SM, PF, IPR, PS are prefixes to COG, SMART, PFAM, INTERPRO and PROSITE ids respectively. Genes for which direct or indirect evidence for transcriptional or translational expression is available have been indicated with a (+) sign and those genes which are inducible on SOS induction are marked with a (l+) in the last column of the table
Protein length (orientation)
Domain architecture and features
Very weak match to Methyltranferase and tellurite resistance TehB (l+)
TM(22–42, 59–79, 154–174, 186–206)
PS00142 TM (61–82, 149–178)
T4 exclusion, Interacts with DNA, is a protease (l+)
phage integrase (l+)
phage excisionase (l+)
similar to Q8FET3 of E. coli O6 (l+)
similar to Zinc finger protein Q8BGS3 (l+)
cI/c2 repressor (l+)
probable homolog of cro from Shigella flexneri (+)
IPR005021, PF03354, COG4626, SM00345
Fusion of a replicase and a phage terminase
Probable pseudogene, phage portal
tail protein (baseplate?)
tail protein (baseplate?)
tail fibre assembly
tail fibre assembly
side tail fibre
PF00239, PF02796, PS00397, PS00398
DNA invertase – catalyses the inversion of 1800 bp P-region (+)
SM00507, IPR002711, IPR003615
Modified cytosine restriction endonuclease A (+)
The regulatory switch in the e14 genome
The b1145 protein is deduced to be functional, since the early left operon functions IntE and Vxis and early right operon kil function are normally off in K-12 (see below), and b1146 also seems likely to be functional by virtue of its near identity to its SfV homologue. In the well-characterized lambdoid phages the CI and Cro repressors bind to the same operators which overlap the promoters for the two divergent early operons. SfV and e14 are 95.2% identical in nucleotide sequence over a 1643 bp region that includes b1145, b1146 and the two potential operator regions. Allison et al.  predicted three inverted repeats (we note that they are all closely related to the consensus palindrome TTGTACCTNNNAGGTACAA) in SfV in the cI-cro intergenic region that might act as OR of lambda phage. These sites are maintained in the e14 sequence with two differences in the first repeat, one in the second repeat and two in the third repeat (Figure 2). Since it has been experimentally shown that LexA repression controls expression of functions in both the e14 early left and early right operons [18, 19], and transcription of the majority of genes tested in these operons have been found to increase following UV irradiation , the promoters and operators on both sides of b1145 appear to have remained intact. We note that there are also two putative operator sequences (above) between b1144 and b1145 centered on e14 bp 5976 and 5996 (and similar sequences in SfV), and that plausible, correctly oriented promoters (see below) overlap both the left and right putative early operator regions.
DNA replication functions
Modular genome organization
The presently annotated e14 genome contains 20/21 predictable ORFs, which are available from the public databases including the Ecogene database , Genobase  and the Swissprot database . Most of these encode putative proteins with no current functional annotation. Based on available data, sequence similarity, domain and motif searches an attempt was made to provide functional annotation for all the ORFs (Table 1). In the following paragraphs we will comment on the e14 genes from left to right across the element.
Most lambdoid bacteriophages do not have any complete genes between the att site and the int gene. However, e14 genes b1137, b1138 and lit lie between the att site and integrase gene. This has resulted in speculations regarding the origin of these genes. The three genes also show a significantly lower G+C content (Table 1) than the remainder of e14. All the three genes show LexA-dependent transcriptional induction on UV irradiation , but this could be an indirect result of e14 induction. Interestingly, the intergenic region between b1138 and lit harbors a region with eight bp multiple exact repeats which are highly AT rich. b1137 was previously annotated as a putative methyltransferase and involved in tellurite resistance, but these matches are very weak; it also shows four possible transmembrane segments and low similarity to certain eukaryotic proteins. The next ORF encodes the lit function. Expression of this protein inhibits protein expression late in phage T4 development. The protein interacts with a short sequence, the gol region within gene 23 that is the major head protein gene of phage T4 . Lit is a protease known to cleave EF-Tu resulting in global inhibition of translation and death of E. coli cells infected with T4 phage . These three e14 genes are unique in that none have convincing homologs in the current database that are phage bacteria encoded. Therefore the origins of this region are difficult to establish. It could have been picked up "recently" by the original functional phage ancestor of e14 through a specialized transduction (imprecise excision) mechanism before its integration here, or it could have been inserted here by some other process after e14's integration; its location next to att makes the former path more attractive.
By sequence homology with phage 21 and other phages, the integrase and excisionase function are encoded by intE and vxis, respectively, which form overlapping ORFs that are almost certainly functional as e14 is capable of SOS induced excision from the chromosome. Both IntE (b1140) and Vxis (b1141) show LexA-dependent transcriptional induction on UV-irradiation .
The small hypothetical b1142 protein is about 11 kDa in size and is similar to the N-terminal region of gene c3200 of E. coli O6:H1 CFT073 (87 % identity over 54 residues) . The latter protein is much larger than its e14 homolog, and is encoded in a similar position in a lambdoid prophage in that genome. The C-terminal region of this CFT073 protein shows close sequence similarity to hypothetical proteins in SfV, ST64B, CPS-53, and Xylella fastidiosa prophage XfP4 , and each of these homologs lies in the early left operon in these lambdoid elements. It is possible that b1142 is a remnant of a larger gene and the deletion event that truncated it could be the left major e14 deletion in Figure 1. Gene b1143 encodes a protein with weak similarity to the putative protein encoded by gene STY2069 of Salmonella enterica CT18  which lies in the early left operon of a prophage there. b1144 encodes a 94 amino acid protein which matches prophage-encoded hypothetical proteins early left operon from S. flexneri and S. enterica. b1144 also shows high transcriptional induction upon UV-irradiation .
The next two ORFs, b1145 and b1146, correspond to the CI repressor and Cro proteins as discussed in the previous section.
The b1147 and b1148 genes have no known function, but both show convincing similarity to hypothetical proteins of lambdoid phage origin. For example, phages SfV and ST64B carry homologs of b1147 and b1148 in similar locations as in e14. The roles of these homologs have not been studied, however a lethal (kil) function that kills the host bacterium was mapped by Plasterk and van de Putte  to what we now can deduce is the b1146–b1149 interval. Since b1146 and b1149 are homologs of non-lethal genes, it seems most likely that b1147 and/or b1148 encode this lethal function. We also note that a lethal sfiC function was mapped to the e14 element by Maguin et al. . Their data are consistent with sfiC being a CI repressor-controlled gene, but its location was not accurately mapped. It is not known whether kil and sfiC are the same or different functions. Experimental evidence suggests that the sfiC gene product interacts with the FtsZ cell division protein and is responsible for an irreversible blockage of cell division , unlike the reversible inhibition brought about by SulA . The protein product is highly stable even in lon+ strains and does not show significant similarity to any non-phage protein. It is interesting that other lambdoid phages are known to encode FtsZ inhibitors in their early left operons [43–47].
The b1149 protein appears to be a unique fusion between a replication protein and phage terminase. While the first 78 residues are quite similar to the N-termini of putative replication proteins from E. coli O157:H7 prophage CP-933P  (sprot id: Q8XAD8) and phages ΦP27 , ST64T  and SfV. The rest of the b1149 protein is extremely similar to the C-termini of terminase proteins of ST64B (98% identical) and SfV (96%) and other phages. The deletion that caused this gene fusion is the middle major e14 deletion in Figure 1, and it seems unlikely that the b1149 protein product is now functional. b1150 is a very small protein that is highly similar to proteins encoded by genes in the same location by phages ST64B, SfV and ΦP27. b1151 closely resembles portal proteins involved in head assembly from phages ST64B and ΦP27 over the N-terminal 135 amino acid residues. In bacteriophage ST64B the portal protein is 414 residues and ΦP27 protein is 413 residues. b1151 is almost certainly a C-terminally truncated pseudogene derived from a homolog of these larger proteins. This truncation and the N-terminal truncation relative to its homologs of the next gene, b1152, represent the boundaries of the right major e14 deletion in Figure 1. b1152 and b1153 are tail protein homologs of gene 47 and 48 proteins of phage Mu, which has a contractile tail. SfV phage tail proteins are their closest homologs and occur in similar relative positions. The N-terminal 106 residues of b1154 are similar to a 22 kDa protein from SfV (85% identity over 100 residues) and show similarity to side tail fiber proteins in other phages. The remaining C-terminal 103 residues are weakly related to the predicted protein of gene plu2959 of Photorhabdus luminescens TT01 , which lies in the tail region of a prophage in that genome. The left boundary of the Pin-invertible element which starts 11582 bp from the left attachment site of e14, lies within b1154, 96 codons from the 5'-terminus. b1155 shows close resemblance in its C-terminal region to genes in prophages CPS-53 of E. coli K-12, CP933H of E. coli EDL933, and Sti8 of S. enterica CT18. TfaE (b1156) shows 90% identity to the tail fibre assembly protein of bacteriophage HK97. b1154 and b1155 proteins are members of the large tail fibre assembly (Tfa) protein family that includes phage T4 gene 38 and Mu gene 50 proteins.
The pin (b1158) protein is a site-specific DNA invertase like the Min invertase of p15B, Gin of phage Mu, Hin of S. enterica, and Cin of phages P1 and P7, as well as putative invertases on a number of prophages in the sequenced bacterial genomes such as Sp1 of E. coli Sakai , Sti3 and Sti7 of S. enterica CT18, and Fels-2 of S. enterica LT2 . These invertases in turn belong to a larger family of site-specific resolvase and recombinase proteins. The Pin protein catalyses the inversion of a 1794 bp long fragment referred to as the P-element . This invertible element lies between 11582–13405 bases from the left att site and encompasses the four ORFs b1154, b1155, b1156 and stfE (b1157). When the early right/late operon fusion, in which these genes lie, is transcribed, genes b1155 and b1156 are not expected to be expressed in the shown (Figure 1) orientation of the P-element (and b1157 is not expected to have any bone fide translation start), but after inversion, the b1157 open reading frame would be fused to the N-terminal 96 codons of b1154 and b1156 would be placed in the correct orientation for expression. StfE (b1157) and b1154 appear to encode the C-termini of alternate side tail fibre proteins, and b1155 and b1156 appear to encode alternate as tail fibre assembly proteins.
The last gene of the e14 element, mcrA, encodes a methylation-dependent restriction endonuclease belonging to the HNH family of proteins found in several bacterial and bacteriophage systems [25, 53]. In vivo studies on McrA suggest that it restricts T-even phage DNA that is hydroxymethylated and non-glucosylated (RglA activity) and also cleaves Hpa II and Sss I methylated DNA . No close homologs of mcrA are known on other phage or prophage genomes, but many temperate phages carry genes that protect the host bacterium from attack by other phages.
Predicted promoters for the e14 element. Putative promoters predicted using BPROM available at the website http://www.softberry.com. Scores are as given by BPROM. Promoters with a score above 3 were considered for the study. Only those promoters which could be associated with some gene are listed. Promoter for the shorter ORF of b1146 was predicted based on Allison et al.  and GeneMark program and hence is omitted from the table.
Predicted terminators for the e14 element. 'rho' independent terminators in the e14 genome as predicted by the GCG terminator program. Only terminators, which could be associated with genes are listed here.
Homologous regions of e14 with other phage and bacterial genomes. Regions of similarity of e14 with other genomes. All the regions indicated show greater than 85% identity in the region of the match. The matching regions in e14 are ordered based on position in the e14 genome. Figure 1 provides a schematic representation of this table.
Correspond e14 protein
S. flexneri phage V
ymfK, ymfL, ymfM
S. typhimurium phage ST64B
E. coli CFT073
E. coli O157:H7
S. flexneri 2a str. 301
Plasmid p15B (X62121)
tfaA, stfE (-)
S. enterica serovar Typhi Ty2
Search for prophage elements other genomes
Predicted phage like elements using a comparative protein based approach. Phage elements detected in other genomes using orthology to e14 proteins as a criterion. Clustering of orthologous proteins (COG hits) for the e14 proteins in different organisms was examined. Only those organisms with two or more COG hits in the e14 element are listed. Estimates of the boundaries of the phage element are provided. 26 phage related regions could be identified by this analysis out of which 23 are already known phage areas in the bacterial genomes. Two (labeled P2 and P3) of the remaining three regions are probably non-phage areas. *The regions which have not been previously identified as prophage element have been marked as P1, P2 and P3. $Denotes approximate boundaries.
Proteins in e14
Related COG member
E. coli O157:H7 EDL933
b1149, b1151, b1159
z1359, z1362, z1356
b1149, b1151, b1158, b1159
z1803, z1806, z1817, z1800
b1149, b1149, b1151, b1159
z6045, z6070, z6042, z6047
b1145, b1154, b1155, b1157, b1158
z0309, z0314, z0315, z0317, zpinH
b1140, b1141, b1145, b1155, b1157
z1866, z1867, zumuD, z1920, z1918
b1140, b1143, b1155
zintT, z2978, z2983
b1145, b1149, b1151
z3358, z3332, z3328
E. coli K-12
b1156, b1157, b1158
ynac, stfr, pinr
b1156, b1157, b1158
ydfm, ydfn, pinq
B. subtilis 168
M. loti MAFF303099
b1150, b1154, b1157
CC1890, CC1902, CC1904
X. fastidiosa 9a5c
N. meningitidis Z2491 (serogroup A)
b1152, b1153, b1157
NMA1323, NMA1324, NMA1325
1768530 to 1807766
S. pyogenens SF370 (serotype M1)
spy0671, spy0655, spy1468
Further, this region is also identified as a possible phage element "5" and shows compositional variation compared to the rest of the Bacillus subtilis genome . We could thus identify several lambdoid prophage elements in a representative set of bacterial genomes using such a protein level approach. This approach takes into consideration the modular nature of phage genomes and looks for orthologs of the genes of the defective prophage e14 that exist in proximity of each other. We hasten to mention that a number of putative prophages were not found by this analysis. But this exercise was knowingly severely limited by only taking orthologs of e14 genes into consideration, and a similar approach using the entire pool of known lambdoid phage (or even all temperate phage) genes should make a much more sensitive and robust technique for detecting phage elements, and, importantly, it can be automated.
Sequence manipulation and analysis was done using the EMBOSS  and GCG  suite of sequence analysis tools. Perl scripts were used for calculating cumulative GC plots and facilitating other searches. The cumulative GC was calculated as ∑(G-C)/(G+C) using a window size of 500. Domain searches were done using the NCBI CDD server , Interpro , PFAM  and SMART  databases were used where ever necessary. Promoter sequences in the e14 genome were detected using the BPROM  utility. The predicted promoters were then analyzed for the presence of ORFs in close vicinity. The promoters for which an ORF could not be assigned are not listed in this work. Rho-independent terminators were detected using the terminator program available with the GCG package. The program is an adaptation of the terminator program by Brendel and Trifonov 1984 . Promoters and terminators that could not be explained functionally were ignored though the prediction servers identified several with high scores. Information on operons within the e14 genome was obtained with TIGROperons . The COG database  was used to find orthologs of proteins encoded by the e14 element. For the proteins, which are not known to belong to any of the COGs listed, the COGNITOR application was used to identify orthologs.
PM was responsible for data collection and analysis. SK conceived of the study, and participated in its design and analysis. SC helped to bring this information into the biological context of past and current prophage research.
PM and SK thank Sri Vidhya for help during manuscript preparation. We acknowledge the use of the Bioinformatics Centre facility funded by DBT, Govt of India, and CSIR for fellowship to PM, DBT Indo-Israel project to SK, and NIH grant AI49003 to SC.
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