Bacteriophage T4 Genome

Abstract

Phage T4 has provided countless contributions to the paradigms of genetics and biochemistry. Its complete genome sequence of 168,903 bp encodes about 300 gene products. T4 biology and its genomic sequence provide the best-understood model for modern functional genomics and proteomics. Variations on gene expression, including overlapping genes, internal translation initiation, spliced genes, translational bypassing, and RNA processing, alert us to the caveats of purely computational methods. The T4 transcriptional pattern reflects its dependence on the host RNA polymerase and the use of phage-encoded proteins that sequentially modify RNA polymerase; transcriptional activator proteins, a phage sigma factor, anti-sigma, and sigma decoy proteins also act to specify early, middle, and late promoter recognition. Posttranscriptional controls by T4 provide excellent systems for the study of RNA-dependent processes, particularly at the structural level. The redundancy of DNA replication and recombination systems of T4 reveals how phage and other genomes are stably replicated and repaired in different environments, providing insight into genome evolution and adaptations to new hosts and growth environments. Moreover, genomic sequence analysis has provided new insights into tail fiber variation, lysis, gene duplications, and membrane localization of proteins, while high-resolution structural determination of the "cell-puncturing device," combined with the three-dimensional image reconstruction of the baseplate, has revealed the mechanism of penetration during infection. Despite these advances, nearly 130 potential T4 genes remain uncharacterized. Current phage-sequencing initiatives are now revealing the similarities and differences among members of the T4 family, including those that infect bacteria other than Escherichia coli. T4 functional genomics will aid in the interpretation of these newly sequenced T4-related genomes and in broadening our understanding of the complex evolution and ecology of phages-the most abundant and among the most ancient biological entities on Earth.

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MICROBIOLOGY AND MOLECULAR BIOLOGY REVIEWS, Mar. 2003, p. 86–156 Vol. 67, No. 1
1092-2172/03/$08.00⫹0 DOI: 10.1128/MMBR.67.1.86–156.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.
Bacteriophage T4 Genome†
Eric S. Miller,
1
* Elizabeth Kutter,
2
Gisela Mosig,
3
‡ Fumio Arisaka,
4
Takashi Kunisawa,
5
and Wolfgang Ru¨ger
6
Department of Microbiology, North Carolina State University, Raleigh, North Carolina 27695-7615
1
; The Evergreen State College,
Olympia, Washington 98505
2
; Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee 37232
3
;
Department of Molecular and Cellular Assembly, Tokyo Institute of Technology, Yokohama 226-8501,
4
and
Department of Applied Biological Sciences, Science University of Tokyo, Noda 278-8510,
5
Japan;
and Faculty for Biology, Ruhr-University-Bochum, 44780 Bochum, Germany
6
T4 GENES TO GENOME ...........................................................................................................................................87
NUCLEOTIDE SKEW IN THE T4 GENOME.........................................................................................................88
IDENTIFYING T4 GENES..........................................................................................................................................88
Computational Strategies for Gene Assignment ..................................................................................................88
Characterized T4 Genes and the Early Genetics ...............................................................................................104
ORFs of Unknown Function and Host Lethality ...............................................................................................106
PROMOTERS AND TRANSCRIPTION FUNCTIONS ........................................................................................107
Early Transcription ................................................................................................................................................107
Middle Transcription .............................................................................................................................................109
Late Transcription..................................................................................................................................................110
Microarray Analysis of T4 Transcription............................................................................................................110
Transcription Termination and Predicted RNA Structures .............................................................................110
Intrinsic transcription terminators ..................................................................................................................110
Rho-dependent transcription terminators.......................................................................................................112
TRANSLATION AND POSTTRANSCRIPTIONAL CONTROL .........................................................................112
Ribosome-Binding Sites .........................................................................................................................................112
RNA Structure at Ribosome Binding Sites.........................................................................................................113
Internal Initiation Sites .........................................................................................................................................113
Translational Coupling ..........................................................................................................................................114
Translational Repressor Proteins.........................................................................................................................114
Codon Usage............................................................................................................................................................114
tRNAs .......................................................................................................................................................................115
Introns......................................................................................................................................................................115
mRNA and tRNA Turnover...................................................................................................................................116
Proteolysis................................................................................................................................................................116
DNA METABOLISM, REPLICATION, RECOMBINATION, AND REPAIR ...................................................117
Enzymes of Nucleotide Metabolism .....................................................................................................................117
DNA Replication Proteins .....................................................................................................................................117
Initiation of DNA Replication...............................................................................................................................118
Recombination and Recombination-Dependent DNA Replication...................................................................119
DNA Repair .............................................................................................................................................................119
MOBILE ENDONUCLEASES, GENE TRANSFER, AND GENE EXCLUSION..............................................120
T4 PARTICLE, INFECTION, AND LYSIS.............................................................................................................120
Heads........................................................................................................................................................................121
DNA Packaging .......................................................................................................................................................121
Baseplate and Tails ................................................................................................................................................122
Infection and Superinfection Exclusion...............................................................................................................124
Lysis and Lysis Inhibition .....................................................................................................................................124
RESTRICTION-MODIFICATION SYSTEMS AND PHAGE EXCLUSION .....................................................125
PREDICTED INTEGRAL MEMBRANE PROTEINS...........................................................................................125
Integral Membrane Proteins of Known Function ..............................................................................................126
Hypothetical Proteins with Predicted Cell Membrane Associations ...............................................................127
Missing Membrane-Associated Proteins .............................................................................................................127
EVOLUTIONARY PERSPECTIVES: T4 PROTEINS AND THE GENOME ....................................................128
* Corresponding author. Mailing address: Department of Microbi-
ology, North Carolina State University, Raleigh, NC 27696-7615.
Phone: (919) 515-7922. Fax: (919) 515-7867. E-mail: eric_miller@ncsu
.edu.
† Dedicated to the memory of Gisela Mosig, our friend, colleague,
and mentor.
‡ Deceased.
86

T4 Protein Structures.............................................................................................................................................128
Orthologous T4 Proteins........................................................................................................................................128
Paralogous Genes in the T4 Genome...................................................................................................................130
A Glimpse at Genome Diversity and Evolution in T4-Type Phages................................................................130
OUTLOOK ..................................................................................................................................................................131
ACKNOWLEDGMENTS ...........................................................................................................................................132
REFERENCES ............................................................................................................................................................132
T4 GENES TO GENOME
T-even phages (Fig. 1) have been major model systems in
the development of modern genetics and molecular biology
since the 1940s; many investigators have taken advantage of
their useful degree of complexity and the ability to derive
detailed genetic and physiological information with relatively
simple experiments. Bacteriophages T2 and T4 were instru-
mental in the first formulations of many fundamental biologi-
cal concepts. These include the unambiguous recognition of
nucleic acids as the genetic material; the definition of the gene
by fine-structure mutational, recombinational, and functional
analyses; the demonstration that the genetic code is triplet; the
discovery of mRNA; the importance of recombination in DNA
replication; light-dependent and light-independent DNA re-
pair mechanisms; restriction and modification of DNA; self-
splicing introns in prokaryotes; translational bypassing; and
others (506, 697). The advantages of T4 as a model system
stemmed in part from the virus’s total inhibition of host gene
expression, which allows investigators to differentiate between
host and phage macromolecular syntheses. Analysis of the
assembly of the intricate T4 capsid and of the functioning of its
nucleotide-synthesizing complex, its replisome, and its recom-
bination complexes has led to important insights into macro-
molecular interactions, substrate channeling, and cooperation
between phage and host proteins within such complexes. In-
deed, the current view of biological “molecular machines” (15,
16) has its beginnings in T4 biology; the T4 replisome, late
gene transcription complex and capsid assembly are paradigms
of molecular machines.
The redundancies of protein functions and of pathways of
DNA transactions probably allow T-even phages to exploit a
broad range of potential hosts and environments while confer-
ring substantial resistance against a wide range of antiviral
mechanisms imposed by the host (4a, 599, 599a, 601, 786). T4
also produces several enzymes with widespread commercial
applications, including its DNA and RNA ligase, polynucle-
otide kinase, and DNA polymerase. Many would argue that to
know T4 is to know the foundations of molecular biology and
the essential paradigms of genetics and gene expression.
There was a price to pay for all of the benefits provided by
this highly tractable genetic system. Early efforts to clone T4
genes were largely thwarted by the glucosylated hydroxymethyl
cytosine (HMC) DNA (which is central to the high expression
and replication of the phage genome, the concurrent total
inhibition of host transcription, and the eventual degradation
of the host DNA). Most of the available restriction endonucle-
ases failed to digest T4 DNA, delaying the gene-by-gene clon-
ing analysis that rapidly advanced in other model organisms.
Eventually, multiply mutant T4 strains defective in the nucle-
ases that cleave unmodified DNA, in the enzymes leading to
the synthesis of HMC-DNA, and in the protein blocking tran-
scription of cytosine-containing DNA were constructed (1020).
These T4dC (or T4C) strains permitted the construction of
detailed restriction maps of T4 (137a, 139, 600, 814, 833a,
1214) and rapidly accelerated cloning and sequence analysis of
T4 gene clusters. By the early 1990s, much of the genome had
been sequenced, but extensive regions remained intractable.
The uncloned DNA appeared to largely encode proteins in-
volved in the transition from host to phage metabolism, nucle-
ases, and other proteins toxic to the Escherichia coli cloning
host. These regions were sequenced by different members of
the T4 community, who closed the gaps by using PCR to carry
out direct sequencing without cloning. Regions that have not
otherwise been published include the nrdC-tk region (labora-
tory of E. Kutter), the e-tRNA region (laboratories of V. Me-
syanzhinov and E. Kutter), the 34–35 region (laboratory of E.
Goldberg), the t-asiA.5 region (laboratory of J. Drake) and the
ndd-rIIB region (laboratories of K. Kreuzer and M. Uzan). The
complete 168,903-bp sequence of the T4 genome is available as
GenBank accession no. AF158101 and as entry NC_000866 at
the NCBI Entrez Genome site (http://www.ncbi.nlm.nih.gov/
Entrez). Among sequenced viruses in the database, only
Pseudomonas phage ␾KZ (727), the African swine fever virus,
herpesviruses, chlorella virus, and vaccinia virus have larger
genomes.
The T4 genome is a rich arena for evaluating complete
genomes in the context of a well-characterized biological sys-
tem. Here, we demonstrate the use of some of the computa-
tional tools currently available for complete genome sequence
FIG. 1. Electron micrographs of bacteriophage T4. The well-rec-
ognized T4 morphology was nature’s prototype of the NASA lunar
excursion module. (A) Extended tail fibers recognize the bacterial
envelope, and its prolate icosahedral head contains the 168,903-bp
dsDNA genome. Reprinted with permission of M. Wurtz, Biozentrum,
Basel, Switzerland. (B) The DNA genome is delivered into the host
through the internal tail tube, which is visible protruding from the end
of the contracted tail sheath. Courtesy of W. Ru¨ger.
VOL. 67, 2003 BACTERIOPHAGE T4 GENOME 87

analysis and discuss the new insights gained from this analysis
of the T4 genome and its nearly 300 genes.
NUCLEOTIDE SKEW IN THE T4 GENOME
T4 DNA has only 34.5% G⫹C, while its E. coli host has
about 50% G⫹C. If T4 were assembled from “modules” of
other genomes, as has been suggested for many phages (dis-
cussed below), different regions might be expected to have
quite different G⫹C contents, particularly if they were recently
acquired. However, only 18 of the known or predicted genes
have less than 60% A⫹T and only 4 have less than 58%.
Therefore, while some genes may have been more recently
acquired, most of the T4 genome appears to have a lengthy,
common history. Interestingly, it is the capsid proteins that
have the lowest A⫹T contents, and these are the most widely
conserved in the T4-related phages (701, 748, 919, 1069) and
presumably among the earliest to have arisen. Gene 23, en-
coding the major head protein, is the lowest, at 55% A⫹T. It
also uses the highest proportion of codons that are translation-
ally optimal for the host (65%), in keeping with its very high
level of expression; about 1,000 copies of the protein are
needed per phage particle synthesized.
A substantial skew toward G and against C in the coding
strand is observed in translated regions. Only four genes have
more than 20% C in the coding strand, while about 130 have
more than 20% G and 37 have more than 22% G. A and T are
more equitably divided between the strands. However, the AT
bias is strong in the third position of codons, as expected with
high-A⫹T genomes, and reflection points in the bias (Fig. 2)
do correlate with changes in the direction of T4 transcription
(499). Whether these biases are coupled to effects of transcrip-
tion or replication on directional mutation pressure, as sug-
gested previously (499), remains to be demonstrated. Variably
used multiple origins of T4 DNA replication (see below) pre-
sumably preclude the use of nucleotide skew analysis to iden-
tify the origin of replication, as it is often used for microbial
chromosomes (352). Overall, AT skew is a strong predictor of
T4 coding regions and the transcribed strand, although in a few
regions both strands are transcribed and, in at least one region,
both are translated.
A genome of AT compositional bias presents issues of DNA
structure that are worthy of brief consideration. Starting with a
balanced 50% A⫹T genome, each GC replaced by an AT base
pair eliminates one Watson-Crick hydrogen bond. This sug-
gests that the evolution of HMC and glucosylation conferred a
secondary selective advantage: it not only protects the DNA
against degrading endonucleases but also improves double-
strand stability. The OH and H side groups of the added
glucose are able to form hydrogen bonds when in proximity
with neighboring bases (456, 457). With only one hydrogen
bond formed per glucose residue, the approximately 16% glu-
cosylated HMC in T4 DNA could compensate for the 14%
A⫹T bias above average in the genome.
The AT-rich T4 genome may also present features advanta-
geous for a virus: a DNA structure different from the B-DNA
of its host (809). On a local scale, the structure would approach
D-form DNA: a polymer consisting of poly(dA-dT) double
strands, overwound with only 8 bp per turn, a wider and shal-
lower major groove, and a deeper and narrower minor groove
(126, 127, 636). Close contacts of the glucosyl residues with
side groups of neighboring bases could alter the preferred
values of roll, slide, and twist angles of base pairs (258). Such
forces and structural features can influence the outward ap-
pearance of the DNA in a way that may be recognized by
proteins. Enzymes that melt DNA as part of their action (such
as RNA polymerase and DNA polymerase) might transcribe
and replicate AT-rich DNA faster than they would transcribe
and replicate DNA with a balanced GC and AT content or
might attract RNA polymerase and other host proteins in a
competitive manner.
IDENTIFYING T4 GENES
On the basis of all available criteria, we conclude that T4 has
about 300 probable genes packed into its 168,903-bp genome.
The nucleotide positions of all probable genes, promoters,
terminators, and the best characterized origins of replication
are given in Table 1, along with several calculated properties
for the genes and their encoded proteins. T4 has a total of 289
probable protein-encoding genes, 8 tRNA genes, and at least 2
other genes that encode small, stable RNAs of unknown func-
tion. Table 2 summarizes and references the functions and
properties of the approximately 156 genes that have been char-
acterized by mutation and/or by the properties of cloned gene
products. Imprecision in the number of “genes” reflects ambi-
guities of genetic nomenclature, when some genes contain
multiple coding regions (for instance, genes 16, 17, and 49
encode more than one protein).
Computational Strategies for Gene Assignment
The probability that an open reading frame (ORF) encodes
a protein can be estimated by various computational methods
that depend on observed patterns in the distribution of bases in
known genes, along with such criteria as the presence of ap-
parent translation initiation regions and the relationship to
promoters and other genes. In the assembly and annotation of
the T4 genome, the main tools used were the correlation co-
efficient, which compares the fractional use of each base at
each of the three codon positions to those of a set of known T4
genes (971; T. Stidham, S. Peterson, and E. Kutler, Abstr.
Evergreen Int. Phage Biol. Meet. p. 51, 1993), and the linguis-
tics-based analysis, GenMark (99, 671). These methods were
supplemented by identification of likely Shine-Dalgarno (SD)
sequences for ribosome binding. As discussed below, such
analyses indicate that virtually all the uncharacterized ORFs of
T4 probably do encode proteins. Most known T4 genes have
correlation coefficients above 0.85, as do most of the unas-
signed ORFs (Table 1). However, there appear to be con-
straints on the composition of some specific proteins that result
in far lower values. This is seen for a few of the well-charac-
terized but very small T4 genes, such as stp (⫺0.14), and for
those that are predicted to encode integral membrane pro-
teins, such as imm (0.31) and ac (0.51). Negative values are
generally seen where a short but definitely expressed reading
frame is superimposed on a different reading frame of another
gene, such as 30.3⬘, or in the complementary strand, as in
repEA and repEB. Therefore, while a high correlation coeffi-
cient makes it very likely that an ORF does indeed encode a
88 MILLER ET AL. MICROBIOL.MOL.BIOL.REV.

protein product, a low correlation coefficient cannot be used to
exclude that possibility.
Work with T4 makes it clear that precisely identifying pro-
tein-coding regions can be complex, even in prokaryotes. (i)
Five known T4 genes and several other ORFs have functional
internal starts, with good experimental evidence for genes 17
and 49 that the shorter proteins have distinct functional roles
(39, 286, 784, 788). In these two cases, separate but related
gene names have been assigned (e.g., 17, 17⬘, and 17⬙)to
indicate this complex relationship. We expect that other exam-
ples of internal translational start sites will be identified.
(ii) Five other genes and ORFs have two closely spaced start
codons with similarly strong values for the sequence informa-
tion content (defined below) at their translation initiation sites
FIG. 2. Intrastrand biases (nucleotide skew) in the T4 genome. (A) Cumulative values of the number of T’s minus the number of A’sina
contiguous strand of the T4 genome for the first (F), second (䊐), and third (E) codon positions and for the intergenic regions (⫹), plotted against
the genome position. The plus strand was used (5⬘ to 3⬘), from position 0 clockwise through the genome map, for the calculation. (B) Cumulative
values of C’s minus G’s plotted as described for panel A. (C) Vertical lines show the distribution of genes in each strand, where “Direct” is the
plus strand for which the analysis was performed and “Complementary” is the minus strand. Reprinted from reference 499, with permission from
the publisher.
VOL. 67, 2003 BACTERIOPHAGE T4 GENOME 89

TABLE 1. Feature coordinates of the T4 genome
Gene
a
Strand
b
Start
c
Stop
c
Length (bp)
d
Length (aa)
d
Correlation
e
coefficient
pI
f
M
r
f
Start 1
Pm ⫺ 123
Pm ⫺ 377
rIIA ⫺ 2189 12 2,178 725 0.99 6.131 82,903
Pm ⫺ 2263
rIIA.1 ⫺ 2403 2200 204 67 0.89 7.156 8,129
Pe (1.4–3.9) ⫺ 2422
60⫹⫺2802 2458 345 160 0.93 8.738 18,600
60⫹⫺2990 2853 138
60.1 ⫺ 3351 2971 381 126 0.96 9.364 14,651
mobA ⫺ 3767 3654 114 37 0.78 9.54 4,192
Pe (3.6) ⫺ 3847
39 ⫺ 5328 3778 1,551 516 0.96 7.103 57,978
Pm ⫺ 5349
Term ⫺ 5384
39.1 ⫺ 5595 5398 198 65 0.79 7.997 7,156
39.2 ⫺ 5839 5702 138 45 0.86 8.497 5,107
goF ⫽ comCa ⫺ 6267 5842 426 141 0.91 4.462 16,682
cef ⫽ mb ⫺ 6482 6267 216 71 0.95 5.203 8,464
motB ⫺ 7141 6653 489 162 0.98 9.205 18,219
Pe (5.9–7.3) ⫺ 7179
motB.1 ⫺ 7650 7291 360 119 0.84 4.993 13,804
motB.2 ⫺ 8161 7661 501 166 0.93 6.45 19,736
Pe (8.1) ⫺ 8182
dexA ⫺ 8908 8225 684 227 0.98 4.763 25,966
dexA.1 ⫺ 9150 8908 243 80 0.90 5.31 9,392
dexA.2 ⫺ 9388 9143 246 81 0.93 4.184 9,518
dda ⫺ 10729 9410 1,320 439 0.99 7.982 49,903
dda.1 ⫺ 11037 10726 312 103 0.84 9.776 12,104
srd ⫺ 11785 11039 747 248 0.89 9.999 29,044
Pe (11.5) ⫺ 11815
modA ⫺ 12510 11908 603 200 0.94 6.035 23,350
modB ⫺ 13130 12507 624 207 0.91 5.306 24,244
Pe (12.8) ⫺ 13150
modA.2 ⫺ 13380 13198 183 60 0.83 4.11 7,024
modA.3 ⫺ 13859 13389 471 156 0.94 6.628 18,333
modA.4 ⫺ 14016 13852 165 54 0.91 5.852 6,162
srh ⫺ 14216 14013 204 67 0.66 6.7 8,104
mrh ⫺ 14676 14191 486 161 0.92 4.33 18,494
mrh.1 ⫺ 15026 14685 342 113 0.77 3.649 12,621
mrh.2 ⫺ 15232 15026 207 68 0.82 5.687 8,257
Pe (15.0) ⫺ 15252
Term ⫺ 15305
soc ⫺ 15573 15331 243 80 0.95 6.361 9,117
Pl ⫺ 15597
Pl ⫺ 16162
segF ⫽ 69 ⫺ 16280 15606 675 224 0.78 10.148 26,218
Pl ⫺ 16359
56 ⫺ 16785 16270 516 171 0.78 4.734 20,425
oriA ⫺ 16763
Pm ⫺ 16813
dam ⫺ 17625 16846 780 259 0.93 8.846 30,420
61 ⫽ 58 ⫺ 18963 17935 1,029 342 0.96 9.174 39,782
Pm ⫺ 19122
61.1 ⫺ 19130 18966 165 54 0.92 5.333 5,896
61.2 ⫺ 19758 19132 627 208 0.91 6.323 24,334
sp ⫽ rV ⫺ 20051 19758 294 97 0.93 4.769 10,994
Pe (19.8) ⫺ 20073
61.4 ⫺ 20369 20112 258 85 0.75 9.828 10,187
dmd ⫽ 61.5 ⫺ 20553 20371 183 60 0.75 5.138 7,027
Pe (20.3) ⫺ 20576
41 ⫺ 22039 20612 1,428 475 0.98 5.439 53,602
Term ⫺ 22347
40 ⫺ 22393 22049 345 114 0.91 4.793 13,291
uvsX ⫺ 23561 22386 1,176 391 0.98 5.310 43,999
Pm ⫺ 23752
segA ⫺ 24235 23570 666 221 0.92 9.933 25,342
Continued on following page
90 MILLER ET AL. M
ICROBIOL.MOL.BIOL.REV.

TABLE 1—Continued
Gene
a
Strand
b
Start
c
Stop
c
Length (bp)
d
Length (aa)
d
Correlation
e
coefficient
pI
f
M
r
f
Pm ⫺ 24460
␤-gt ⫺ 25455 24400 1,056 351 0.97 9.079 40,670
42 ⫺ 26219 25479 741 246 0.98 5.933 28,492
Pm ⫺ 26317
imm ⫺ 26624 26373 252 83 0.31 9.436 9,343
imm.1 ⫺ 27013 26636 378 125 0.96 6.486 14,074
Pe (26.4) ⫺ 27044
Term ⫺ 27183
43 ⫺ 29893 27197 2,697 898 0.97 6.087 103,622
Pm ⫺ 29931
Term ⫺ 29967
regA ⫺ 30340 29972 369 122 0.77 8.939 14,620
62 ⫺ 30905 30342 564 187 0.93 8.592 21,364
44 ⫺ 31866 30907 960 319 0.98 7.016 35,790
Term ⫺ 31912
45 ⫺ 32603 31917 687 228 0.98 4.759 24,861
Pm ⫺ 32626
rpbA ⫺ 33048 32659 390 129 0.98 7.283 14,712
45.2 ⫺ 33246 33058 189 62 0.85 5.671 7,477
Pm ⫺ 33257
46 ⫺ 34984 33302 1,683 560 0.98 8.263 63,588
Pm ⫺ 35014
46.1 ⫺ 35187 34981 207 68 0.73 4.068 8,153
46.2 ⫺ 35431 35168 264 87 0.85 4.288 10,268
Pe (35.3) ⫺ 35662
47 ⫺ 36447 35428 1,020 339 0.98 4.981 39,170
Pm ⫺ 36576
47.1 ⫺ 36584 36444 141 46 0.25 4.210 5,321
Term ⫺ 36622
␣-gt ⫺ 37826 36624 1,203 400 0.94 6.358 46,709
mobB ⫺ 38679 37885 795 264 0.78 9.737 30,367
Pm ⫺ 38681
Term ⫺ 38731
␣-gt.2 ⫺ 38922 38731 192 63 0.91 9.135 7,322
␣-gt.3 ⫺ 39110 38907 204 67 0.91 9.609 7,931
␣-gt.4 ⫺ 39396 39079 318 105 0.87 8.849 12,445
␣-gt.5 ⫺ 39616 39398 217 72 0.95 4.22 8,548
55 ⫺ 40157 39600 558 185 0.94 5.45 21,537
Pm ⫺ 40180
55.1 ⫺ 40456 40193 264 87 0.79 4.114 9,846
55.2 ⫺ 40785 40459 327 108 0.88 9.717 12,727
Term ⫺ 40836
55.3 ⫺ 41038 40799 240 79 0.52 8.751 9,153
55.4 ⫺ 41170 41039 132 43 0.52 8.575 5,145
Pe (40.4) ⫺ 41225
55.5 ⫺ 41471 41178 294 97 0.75 9.821 11,809
55.6 ⫺ 41646 41464 183 60 0.71 9.581 6,962
Pe (41.0) ⫺ 41670
Term ⫺ 41800
nrdH ⫺ 42113 41805 309 102 0.93 9.075 11,720
55.8 ⫺ 42328 42116 213 70 0.80 9.26 7,913
Pm ⫺ 42805
nrdG ⫺ 42916 42446 471 156 0.78 8.312 18,248
Pm ⫺ 43023
mobC ⫺ 43538 42906 633 210 0.88 9.852 23,978
nrdD⫹⫺44814 43535 1,280 605 0.99 6.889 67,964
I-TevII ⫺ 45612 44836 777 258 0.98 9.808 30,371
Pl ⫺ 45625
nrdD⫹⫺46385 45848 538
Pm ⫺ 46441
49⬘⫺46699 46382 318 105 11,888
49 ⫺ 46855 46382 474 157 0.79 8.618 18,145
Pl ⫺ 46879
Term ⫺ 46884
pin ⫺ 47382 46897 486 161 0.98 4.369 18,817
Pe (46.7) ⫺ 47416
49.1 ⫺ 47521 47366 156 51 0.80 3.780 6,163
Continued on following page
V
OL. 67, 2003 BACTERIOPHAGE T4 GENOME 91

TABLE 1—Continued
Gene
a
Strand
b
Start
c
Stop
c
Length (bp)
d
Length (aa)
d
Correlation
e
coefficient
pI
f
M
r
f
49.2 ⫺ 47826 47506 321 106 0.89 4.352 12,579
49.3 ⫺ 48131 47823 309 102 0.50 3.895 11,938
nrdC ⫺ 48391 48128 264 87 0.80 7.183 10,050
nrdC.1 ⫺ 48635 48393 243 80 0.97 8.342 9,444
nrdC.2 ⫺ 48936 48622 315 104 0.81 6.586 12,159
nrdC.3 ⫺ 49859 48933 927 308 0.92 9.01 36,297
nrdC.4 ⫺ 50915 49914 1,002 333 0.95 7.63 38,996
Pe (50.0) ⫺ 50937
nrdC.5 ⫺ 51995 50973 1,023 340 0.92 9.327 39,670
nrdC.6 ⫺ 52893 52066 828 275 0.96 9.20 31,725
nrdC.7 ⫺ 53302 52901 402 133 0.84 6.41 15,309
nrdC.8 ⫺ 53885 53358 528 175 0.88 6.11 20,758
Pe (54.0) ⫺ 53907
nrdC.9 ⫺ 54248 53946 303 100 0.75 9.68 11,979
nrdC.10 ⫺ 55320 54343 978 325 0.93 4.85 36,691
Pe (54.4) ⫺ 55348
Term ⫺ 55432
nrdC.11 ⫺ 56445 55435 1,011 336 0.92 6.89 38,899
mobD ⫺ 57208 56429 780 259 0.79 9.957 30,456
mobD.1 ⫺ 57828 57283 546 181 0.95 6.01 21,179
mobD.2 ⫺ 57932 57828 105 34 ⫺0.05 9.49 4,205
Pe ⫺ 57954
mobD.2a ⫺ 58165 58049 117 38 0.68 8.85 4,516
mobD.3 ⫺ 58349 58155 195 64 0.91 4.95 7,605
mobD.4 ⫺ 58534 58352 183 60 0.94 4.41 6,858
mobD.5 ⫺ 58722 58534 189 62 0.82 4.061 7,122
Pe (57.9) ⫺ 58744
Term ⫺ 58813
rI.-1 ⫺ 59205 58819 387 128 0.97 5.61 14,649
rI ⫺ 59495 59202 294 97 0.76 4.83 11,125
rI.1 ⫺ 59720 59508 213 70 0.73 10.225 8,273
Pl ⫺ 59740
tk ⫺ 60344 59763 582 193 0.95 6.49 21,624
tk.1 ⫺ 60534 60346 189 62 0.77 3.989 7,238
tk.2 ⫺ 60716 60531 186 61 0.67 4.194 7,134
tk.3 ⫺ 60925 60713 213 70 0.78 8.628 8,507
Term ⫺ 61369
tk.4 ⫺ 61389 60922 468 155 0.94 6.124 17,491
vs ⫺ 61733 61386 348 115 0.67 8.744 13,057
vs.1 ⫺ 62271 61726 546 181 0.95 9.798 20,683
regB ⫺ 62740 62279 462 153 0.85 8.444 17,978
Pe (62.2) ⫺ 62761
vs.3 ⫺ 63078 62800 279 92 0.87 5.378 10,904
vs.4 ⫺ 63344 63078 267 88 0.95 4.555 10,211
vs.5 ⫺ 63557 63381 177 58 0.17 9.52 6,611
vs.6 ⫺ 63919 63557 363 120 0.93 5.902 13,814
vs.7 ⫺ 64256 63927 330 109 0.75 9.031 12,836
vs.8 ⫺ 64912 64253 660 219 0.87 9.21 25,029
denV ⫺ 65355 64939 417 138 0.94 9.393 16,080
Pe (64.6) ⫺ 65378
ipII ⫺ 65718 65416 303 100 0.94 9.349 11,086
Pe (65.0) ⫺ 65763
ipIII ⫺ 66415 65834 582 194 0.89 9.557 21,689
Pe ⫺ 66462
e ⫺ 66997 66503 495 164 0.97 9.599 18,693
Pl ⫺ 67005
Pl ⫺ 67018
Pl ⫺ 67234
nudE ⫽ e.1 ⫺ 67490 67035 456 151 0.95 5.141 17,025
e.2 ⫺ 67960 67652 309 102 0.96 6.485 12,156
e.3 ⫺ 68319 67957 363 120 0.85 8.784 14,156
e.4 ⫺ 68693 68301 393 130 0.60 9.647 15,139
e.5 ⫺ 69270 68662 609 202 0.97 5.72 23,816
Term ⫺ 69306
e.6 ⫺ 69905 69312 594 197 0.99 6.162 22,045
Pe (69.9) ⫺ 69931
e.7 ⫺ 70303 69968 336 111 0.83 4.214 13,070
Continued on following page
92 MILLER ET AL. M
ICROBIOL.MOL.BIOL.REV.

TABLE 1—Continued
Gene
a
Strand
b
Start
c
Stop
c
Length (bp)
d
Length (aa)
d
Correlation
e
coefficient
pI
f
M
r
f
Pe (69.4) ⫺ 70323
e.8 ⫺ 70623 70360 264 87 0.74 4.324 10,199
Pe (69.8) ⫺ 70660
Term ⫺ 70856
rnaC ⫺ 71046 70908 139
rnaD ⫺ 71171 71053 119
tRNAR ⫺ 71247 71173 75
segB ⫺ 71918 71253 666 221 0.96 9.320 26,146
tRNAI ⫺ 72033 71960 74
tRNAT ⫺ 72110 72035 76
tRNAS ⫺ 72204 72118 87
tRNAP ⫺ 72280 72203 78
tRNAG ⫺ 72364 72291 74
tRNAL ⫺ 72456 72369 88
tRNAE ⫺ 72530 72456 75
Pm ⫺ 72593
Pl ⫺ 72863
tRNA.2 ⫺ 72915 72628 288 95 0.96 5.031 11,285
tRNA.3 ⫺ 73328 72918 411 136 0.93 4.736 16,035
tRNA.4 ⫺ 73514 73329 186 61 0.69 7.996 6,558
Pe (72.6) ⫺ 73536
ipI ⫺ 73878 73591 288 95 0.90 8.973 10,177
Pe (73.0) ⫺ 73903
57B ⫺ 74410 73952 459 152 0.83 5.089 17,246
57A ⫺ 74649 74407 243 80 0.97 4.248 8,731
Pm ⫺ 74877
Pl ⫺ 74999
1 ⫺ 75374 74649 726 242 1.00 4.947 27,332
Pm ⫺ 75393
3 ⫺ 75954 75424 531 176 0.93 4.267 19,713
2 ⫽ 64 ⫺ 76885 76061 825 274 0.87 10.144 31,613
4 ⫽ 50 ⫽ 65 ⫺ 77337 76885 453 150 0.77 9.793 17,629
Pl ⫺ 77358
Pl ⫹ 77362
Pl ⫹ 77381
53 ⫹ 77385 77975 591 196 0.96 6.005 22,968
Pl ⫹ 77491
5 ⫹ 77959 79686 1,728 575 0.95 5.235 63,121
repEB ⫺ 78118 77981 138 45 0.35 5.19 5,483
repEA ⫺ 79237 79085 153 50 0.24 8.52 6,130
Pe ⫺ 79405
5.1 ⫹ 79721 80215 495 164 0.86 4.593 18,499
Pl ⫹ 79799
segC ⫹ 80196 80618 423 140 0.90 9.74 15,945
5.3 ⫹ 80621 80791 171 56 0.75 9.960 6,089
5.4 ⫹ 80779 81072 294 97 0.89 8.462 10,221
6 ⫹ 81081 83063 1,983 660 0.97 4.508 74,436
7 ⫹ 83060 86158 3,099 1,032 0.96 4.953 119,226
Pl ⫹ 85812
8 ⫹ 86151 87155 1,005 334 0.91 4.453 38,011
Term ⫹ 87161
Pl ⫹ 87200
9 ⫹ 87219 88085 867 288 0.91 4.929 31,000
Pl ⫹ 87885
10 ⫹ 88085 89893 1,809 602 0.94 4.275 66,238
11 ⫹ 89893 90552 660 219 0.91 5.066 23,708
12 ⫹ 90549 92132 1,584 527 0.91 6.072 56,220
wac ⫹ 92129 93592 1,464 487 0.95 4.445 51,876
13 ⫹ 93624 94553 930 309 0.92 4.917 34,745
14 ⫹ 94555 95325 771 256 0.92 4.468 29,575
Pl ⫹ 95337
15 ⫹ 95367 96185 819 272 0.94 4.772 31,558
Pl ⫹ 96153
16 ⫹ 96194 96688 495 164 0.90 4.423 18,388
Term ⫹ 93596
17 ⫹ 96672 98504 1,833 610 0.98 5.638 69,764
Pl ⫹ 96913
Continued on following page
V
OL. 67, 2003 BACTERIOPHAGE T4 GENOME 93

TABLE 1—Continued
Gene
a
Strand
b
Start
c
Stop
c
Length (bp)
d
Length (aa)
d
Correlation
e
coefficient
pI
f
M
r
f
17⬘A ⫹ 96933 98504 1,572 523 5.16 59,245
17⬘B ⫹ 96987 98504 1,518 505 5.02 57,108
17⬙⫹97254 98504 1,251 416 4.67 46,841
Pl ⫹ 98513
18 ⫹ 98536 100515 1,980 659 0.95 4.795 71,338
Pl ⫹ 100564
Pl ⫹ 100623
19 ⫹ 100632 101123 492 163 0.99 4.546 18,462
Term ⫹ 101131
Pl ⫹ 101184
20 ⫹ 101207 102781 1,575 524 0.99 5.341 61,037
Pl ⫹ 102539
67 ⫹ 102781 103023 243 80 0.77 3.662 9,106
68 ⫹ 103023 103448 426 141 0.98 10.108 15,874
Pl ⫹ 103146
21 ⫹ 103448 104086 639 212 0.95 4.725 23,253
21⬘⫹103514 104086 573 190 5.134 20,834
Pl ⫹ 104095
22 ⫹ 104117 104926 810 269 0.92 4.498 29,906
Pl ⫹ 104787
Pl ⫹ 104816
23 ⫹ 104945 106510 1,566 521 0.97 5.29 56,023
Term ⫹ 106537
segD ⫺ 107232 106561 672 223 0.99 9.740 25,619
Pl ⫹ 107301
24 ⫹ 107323 108606 1,284 427 0.92 4.618 46,998
Term ⫹ 108613
Term ⫹ 108668
rnlB ⫽ 24.1 ⫺ 109640 108636 1,005 334 0.99 5.666 37,631
24.2 ⫺ 109928 109650 279 92 0.87 4.923 11,003
24.3 ⫺ 110085 109915 171 56 0.85 10.22 6,550
Term ⫺ 110180
hoc ⫺ 111317 110187 1,317 376 0.93 4.626 40,388
inh ⫺ 112007 111327 681 226 0.97 4.304 25,570
Pl ⫺ 112029
Pl ⫹ 112034
segE ⫹ 112057 112674 618 205 0.92 4.559 22,896
Pl ⫹ 112588
uvsW ⫹ 112677 114440 1,764 587 0.93 10.304 67,526
Term ⫺ 114472
uvsY.-2 ⫺ 114663 114496 168 55 0.91 4.323 6,062
Pl ⫺ 114681
uvsY.-1 ⫺ 114914 114690 225 74 0.74 4.939 8,963
uvsY ⫺ 115327 114914 414 137 0.88 8.53 15,840
Pm ⫺ 115371
25 ⫺ 115802 115404 399 132 0.95 4.49 15,096
26⬘⫺116089 115802 288 95 5.27 10,856
Pl ⫺ 116412
26 ⫺ 116428 115802 627 208 0.86 5.748 23,883
Pl ⫺ 116436
Pl ⫺ 116444
Pl ⫹ 116467
51 ⫹ 116479 117228 750 249 0.91 6.229 29,340
27 ⫹ 117228 118403 1,176 391 0.97 5.24 44,462
28 ⫹ 118348 118881 534 177 0.94 5.75 20,122
29 ⫹ 118878 120650 1,773 590 0.95 4.931 64,416
48 ⫹ 120659 121753 1,095 364 0.76 8.715 39,738
54 ⫹ 121753 122715 963 320 0.87 5.383 34,981
Term ⫹ 122720
alt.-3 ⫺ 123032 122742 291 96 0.93 4.58 10,704
Pe ⫺ 123057
alt.-2 ⫺ 123268 123065 204 67 0.70 9.81 7,382
alt.-1 ⫺ 123450 123265 186 61 0.95 5.71 6,622
alt ⫺ 125502 123454 2,049 682 0.95 6.158 75,819
Pl ⫺ 125525
Term ⫺ 125558
alt.1 ⫺ 125748 125560 189 62 0.89 4.371 7,153
Continued on following page
94 MILLER ET AL. M
ICROBIOL.MOL.BIOL.REV.

TABLE 1—Continued
Gene
a
Strand
b
Start
c
Stop
c
Length (bp)
d
Length (aa)
d
Correlation
e
coefficient
pI
f
M
r
f
30 ⫺ 127208 125745 1,464 487 0.98 6.315 55,299
Pm 127234
30.1 ⫺ 127474 127205 270 89 0.82 8 10,833
30.2 ⫺ 128310 127474 837 278 0.94 6.241 32,433
Pm 128355
30.3⬘⫺128629 128402 228 75 ⫺0.17 10.4 8,945
30.3 ⫺ 128765 128307 459 152 0.85 8.849 17,088
30.4 ⫺ 128964 128758 207 68 0.95 4.535 8,064
30.5 ⫺ 129158 128961 198 65 0.82 5.091 7,252
30.6 ⫺ 129445 129158 288 95 0.88 7.19 10,814
30.7 ⫺ 129852 129487 366 121 0.82 7.305 14,131
Pe (128.2) ⫺ 129883
30.8 ⫺ 130253 129921 333 110 0.94 6.612 12,893
Pe (128.6) ⫺ 130274
Term ⫺ 130358
Term ⫺ 130402
30.9 ⫺ 130540 130364 177 58 0.92 11.44 6,519
rIII ⫺ 131033 130785 249 82 0.90 8.479 9,325
Pl ⫺ 131167
31 ⫺ 131516 131181 336 111 0.89 5.315 12,079
Pm 131540
31.1 ⫺ 131881 131573 309 102 0.84 9.113 11,520
31.2 ⫺ 132118 131882 237 78 0.71 9.806 9,397
cd ⫺ 132699 132118 582 193 0.90 7.833 21,200
cd.1 ⫺ 133034 132696 339 112 0.84 8.138 12,814
cd.2 ⫺ 133261 133031 231 76 0.69 4.823 10,131
Pe (131.7) ⫺ 133295
Term ⫺ 133376
cd.3 ⫺ 133609 133334 276 91 0.88 4.82 10,131
cd.4 ⫺ 133812 133612 201 66 0.83 4.19 7,918
cd.5 ⫺ 134032 133805 228 75 0.81 8.521 8,738
pseT ⫺ 134907 134002 906 301 0.96 8.671 34,622
pseT.1 ⫺ 135135 134908 228 75 0.74 8.455 8,833
pseT.2 ⫺ 135431 135132 300 99 0.75 8.577 11,645
pseT.3 ⫺ 135781 135428 354 117 0.90 8.947 13,136
alc ⫺ 136275 135772 504 167 0.94 7.23 18,962
Pe (134.4) ⫺ 136300
Pl ⫹ 136889
rnlA ⫽ 63 ⫺ 137464 136340 1,125 374 0.96 4.885 43,514
denA ⫺ 137951 137517 435 144 0.94 9.442 16,744
Term ⫺ 137950
nrdB⫹⫺138457 137955 503 388 0.92 4.924 45,357
I-TevIII ⫺ 138886 38593 294 97 0.78 9.011 11,331
Pl ⫺ 138933
Pm ⫺ 138939
nrdB⫹⫺139719 139056 664
Pm ⫺ 139878
nrdB.1 ⫺ 139967 139716 252 83 0.83 9.874 9,409
Term ⫺ 140384
mobE ⫺ 140416 139991 426 141 0.94 10.102 16,448
nrdA ⫺ 142680 140416 2,265 754 0.98 6.117 85,982
Pm ⫺ 142725
nrdA.1 ⫺ 142997 142671 327 108 0.70 9.035 12,362
nrdA.2 ⫺ 143214 142951 264 87 0.96 5.233 10,065
td⫹⫺143546 143235 312 286 0.89 8.617 33,077
I-TevI ⫺ 144431 143694 738 245 0.83 9.625 28,175
Pl ⫺ 144449
td⫹⫺145112 144564 549
Pm ⫺ 145142
frd ⫺ 145690 145109 582 193 0.98 6.35 21,714
frd.1 ⫺ 146004 145762 243 80 0.75 4.843 9,471
Term ⫺ 146051
frd.2 ⫺ 146529 146143 387 128 0.73 4.281 14,742
frd.3 ⫺ 146802 146575 228 75 0.85 3.699 8,820
Pe (144.6) ⫺ 146839 146833
Term ⫺ 146925
32 ⫺ 147853 146948 906 301 0.96 4.681 33,509
Pl ⫺ 147998
Pm ⫺ 148057
segG ⫽ 32.1 ⫺ 148541 147909 633 210 0.95 7.194 24,564
Continued on following page
V
OL. 67, 2003 BACTERIOPHAGE T4 GENOME 95

TABLE 1—Continued
Gene
a
Strand
b
Start
c
Stop
c
Length (bp)
d
Length (aa)
d
Correlation
e
coefficient
pI
f
M
r
f
59 ⫺ 149196 148543 654 217 0.89 9.387 26,000
33 ⫺ 149531 149193 339 112 0.93 4.38 12,831
dsbA ⫺ 149778 149509 270 89 0.96 4.969 10,379
Pm ⫺ 149873
rnh ⫺ 150704 149787 918 305 0.97 8.535 35,562
Pe (148.6) ⫺ 150727
Pl ⫹ 150780
34 ⫹ 150809 154678 3870 1289 0.94 5.206 140,416
Pm ⫺ 153011
35 ⫹ 154687 155805 1,119 372 0.84 4.96 40,123
Term ⫹ 155811
Pl ⫹ 155850
36 ⫹ 155868 156533 666 221 0.92 8.072 23,343
Pl ⫹ 156369
37 ⫹ 156542 159622 3,081 1,026 0.87 8.537 109,226
Term ⫹ 159628
38 ⫹ 159649 160200 552 183 0.88 6.633 22,311
Pl ⫹ 160209
t ⫹ 160221 160877 657 218 0.94 7.921 25,178
Term ⫹ 160924
asiA ⫺ 161150 160878 273 90 0.95 5.395 10,590
Pe (158.7) ⫺ 161175
asiA.1 ⫺ 161315 161163 153 50 0.89 4.51 5,935
arn ⫺ 161590 161312 279 92 0.81 4.351 10,903
arn.1 ⫺ 161805 161674 132 43 0.54 8.334 5,173
arn.2 ⫺ 162172 161876 297 98 0.59 5.243 12,402
arn.3 ⫺ 162630 162172 459 152 0.90 5.078 17,837
arn.4 ⫺ 162833 162627 207 68 0.99 9.24 12,802
motA ⫺ 163602 162967 636 211 0.96 8.772 23,577
Pe (161.1) ⫺ 163637
Term ⫺ 163724
motA.1 ⫺ 163879 163730 150 49 0.49 10.036 4,842
52 ⫺ 165204 163876 1,329 442 0.99 8.799 50,582
52.1 ⫺ 165349 165209 141 46 0.42 8.649 5,098
Term ⫺ 165332
ac ⫺ 165497 165342 156 51 0.51 3.916 5,472
stp ⫺ 165585 165505 81 26 ⫺0.14 10.28 3,184
ndd ⫺ 166040 165585 456 151 0.85 9.524 16,935
ndd.1 ⫺ 166316 166101 216 71 0.86 4.111 8,143
ndd.2 ⫺ 166435 166325 111 36 0.09 5.818 4,354
ndd.2a ⫺ 166554 166432 123 40 0.73 7.14 4,303
ndd.3 ⫺ 166628 166548 81 26 ⫺0.49 8.25 3,019
ndd.4 ⫺ 166764 166636 129 42 0.11 8.622 4,954
Pe (164.2) ⫺ 166771
ndd.5 ⫺ 166913 166815 99 32 0.81 7.082 3,687
ndd.6 ⫺ 166996 166910 87 28 ⫺0.05 8.014 3,406
Pe (164.5) ⫺ 167050
denB ⫺ 167660 167103 558 185 0.91 7.232 21,162
Term ⫺ 167736
denB.1 ⫺ 167937 167743 195 64 0.52 8.134 7,452
rIIB ⫺ 168903 167965 939 312 0.96 6.24 35,544
End 168903
a
Genes are listed sequentially as they appear in the GenBank file (accession no. AF158101), clockwise on the circular map (by convention) starting with the first
base 5⬘ of rIIB. Recently renamed genes, or those with multiple names, are labeled with ⫽. Intron-containing or translational bypass genes (nrdB
⫹
, 60
⫹
) are noted with
a
⫹
for each reading frame. Genes marked with a prime (⬘) are overlapping with, or internal to, the designated gene. Transcription signals listed are Pe, Pm, and Pl
for early, middle and late promoters, respectively, and Ter for terminator. Pe entries in parentheses are promoter designations used in earlier literature.
b
The coding strand is noted as either the GenBank deposited (⫹) sequence or the complement (⫺).
c
Start and stop coordinates denote the first base of the coding region (usually the A of the initiator ATG) and the last base of the stop codon. Promoter coordinates
given are either the mapped or predicted transcript start sites (the “⫹1” position), and terminator coordinates are the first 5⬘ base of the hairpin.
d
The length (bp) entry includes the stop codon of each coding sequence. Only the mature protein length (aa) is given for those proteins that arise from spliced or
bypassed genes.
e
The correlation coefficient given for each gene is the probability of an ORF being a T4 gene based on the codon usage in characterized T4 genes. The program
was written by Gary Stormo and is available at the web site: http://www.lecb.ncifcrf.gov/⬃toms/delila/frame.html.
f
pI and M
r
are calculated values.
96 MILLER ET AL. MICROBIOL.MOL.BIOL.REV.

TABLE 2. Functions and mutant phenotypes of T4 gene products
Gene
a
Function of gene product
b
Size (kDa)
b
Mutant phenotype
Restrictive host or
condition
c
Reference(s)
rIIA Membrane-associated protein; affect
host membrane ATPase
82.9 Rapid lysis; suppress T4 30 and
some 32 mutations
Auxiliary; rex
⫹
␭
lysogens; P2-like
HK239 lysogen; tabR
2–4, 56, 59, 95, 96, 106, 121, 159, 181, 184,
191, 198, 216, 224, 263, 292, 293, 365,
375, 441, 430, 431, 451, 504, 582, 768,
769, 774, 793, 810, 811, 834, 851, 874,
940, 1007, 1021, 1059, 1114b, 1159,
60 DNA topoisomerase subunit 18.6 DNA delay; rc ⫽ acriflavine
resistance
Essential; 25°C or below 447, 450, 451, 452, 653, 654, 681, 801, 968,
1037
mobA Pseudogene of Mob site-specific DNA
endonuclease
4.2 Nonessential E. Thomas, F. Zucker, and E. Kutter,
unpublished data
39 DNA topoisomerase subunit; DNA-
dependent ATPase; membrane-
associated protein
58.0 DNA delay; rc ⫽ acriflavine
resistance
Essential; 25°C or below;
synthetic lethal with
T4 49 and 17
mutations, or when
host topoisomerase IV
is poisoned with
novobiocin
264, 297, 295, 296, 432, 447, 448, 449, 451,
452, 454, 571, 589, 653, 654, 708, 789,
768, 769, 801, 834, 853, 1006, 1037,
1047, 1059, 1216, 1236
goF ⫽ comC-␣⫽go9H Affects mRNA metabolism 16.7 Allows T4 growth in rho (nusD)
hosts
Auxiliary 144, 431, 474, 879, 925, 956, 1028, 1044,
1045, 1062, 1154, 1241
cef ⫽ mb ⫽ M1 ⫽ motC Processing of T4 tRNAs 8.5 Auxiliary; CT439; roc
⫺
hosts
431, 869, 870, 878, 937, 956
pseF ⫽ plaCTr5x? 5⬘ phosphatase Auxiliary 956
motB 18.2 Affects middle transcription Auxiliary 956
dexA Exonuclease A 26.0 Auxiliary; restricted on
optA hosts
308, 355, 431, 604, 737, 780, 956, 1152
dda ⫽ sud DNA helicase; DNA-dependent ATPase 49.9 Suppress certain T4 32 mutations Auxiliary; synthetic lethal
with T4 59 mutations
45, 309, 369, 431, 481, 546, 547, 587, 588,
649, 680, 769, 780, 783, 956, 970; P.
Gauss, personal communication
srd ⫽ dda.2 Postulated decoy of host ␴
70
or ␴
S
29.1 Auxiliary 780
modA Adenylribosylating enzyme 23.4 ␣ subunits of host RNA polymerase
are incompletely modified
Auxiliary 324, 431, 435, 780, 1011, 1077
modB Adenylribosylating enzyme 24.2 Auxiliary 780, 1077
srh ⫽ modA.5 Postulated decoy of host ␴
32
8.1 Delays early T4 gene expression at
high temperatures
Auxiliary 780
mrh Affects phosphorylation of host ␴
32
18.5 Allows T4 growth in a ␴
32
host Auxiliary 290, 780
soc Small outer capsid protein 9.1 Unstable T4 capsids Auxiliary 77, 89, 167, 431, 461, 462, 466, 675, 780,
916, 918
segF ⫽ 69 Intron-like endonuclease. A probable
fusion protein, generated from 56 and
69 by hopping of ribosomes across a
pseudoknot, is larger
26.2 Nonessential 51, 305, 677, 769, 780, 790, 783
56 dCTPase; dUTPase; dCDPase;
dUDPase
20.4 Little DNA synthesis; unstable
DNA
Essential 305, 347, 602, 605, 696, 769, 781, 783, 839,
1162
oriA DNA replication origin; cis-acting
sequences in 56, 69, and soc; primer
transcript same as transcript for these
genes
No DNA synthesis from oriA Auxiliary 160, 674, 678, 691, 791, 1215
dam DNA adenine methylase 30.4 No DNA adenine methylation Auxiliary 112, 139, 395, 676, 677, 683, 742, 743, 921,
960, 961, 1072
61 ⫽ 58 Primase; requires interaction with gp41
helicase for priming at unique
sequence
39.8 DNA delay Auxiliary; 25°C or below;
synthetic lethal with
T4 49 or 17 mutations
17, 47, 60, 123, 154, 380, 415, 416, 421,
422, 652, 653, 667, 761, 768, 769, 783,
788, 801, 829, 826, 831, 970, 996, 997,
998, 1216
sp ⫽ 61.3 ⫽ rIV Periplasmic protein 11.0 Rapid lysis; suppresses e lysozyme
mutations
Auxiliary 2, 261, 492, 585, 851, 971, 1208
dmd ⫽ 61.5 Discriminator of mRNA degradation 7.0 Excessive mRNA degradation Nonessential; suppressed
by motA mutations
491, 493, 971, 1102
Continued on following page
VOL. 67, 2003 BACTERIOPHAGE T4 GENOME 97

TABLE 2—Continued
41 Replicative and recombination DNA
helicase; GTPase; ATPase; dGTPase;
dATPase
53.6 DNA arrest; little DNA
displacement synthesis
Essential 17, 54, 60, 154, 155, 184, 197, 227, 228,
264, 309, 424, 415, 416, 421, 451, 478,
479, 554, 593, 653, 652, 651, 761, 768,
769, 826, 831, 838, 930, 931, 950, 970,
1029, 1064, 1122, 1220
40 Membrane-associated protein initiator
of head vertex
13.3 Polyheads Auxiliary; high
temperatures
89, 115, 116, 301, 416, 443, 500, 608, 693,
729
uvsX ⫽ fdsA RecA-like recombination protein; DNA-
ATPase
44.0 UV- and X-ray sensitive;
recombination deficient; suppress
49 mutations
Auxiliary 26, 80, 82, 165, 182, 213, 254, 282, 283,
281, 301, 351, 384, 386, 392, 416, 423,
549, 572, 589, 686, 723, 739, 762, 768,
769, 938, 949, 950, 970, 1047, 1088,
1138, 1222–1225
segA Site-specific intron-like DNA
endonuclease
25.3 Nonessential 986, 988
␤-gt ␤-Glucosyltransferase 40.7 No ␤-glucosylation of HMC DNA Auxiliary; Shigella 139, 316, 451, 615a, 757, 924, 1075, 1084,
1134
42 dCMP hydroxymethylase 28.5 Little or no DNA synthesis Essential 60, 68, 124, 184, 264, 320, 348, 383, 451,
476, 475, 477, 598, 611, 612, 695, 698,
834, 1027, 1076, 1114a, 1165, 1192
imm Inner membrane protein 9.3 No immunity to superinfection Auxiliary 2, 3, 4, 166, 188, 665, 666, 836, 1113, 1232
43 DNA polymerase; 3⬘-to-5⬘ exonuclease 103.6 No DNA synthesis; mutator or
antimutator activities of
conditional lethals under
semipermissive conditions
Essential; nonessential
dsd mutants do not
grow in optA hosts
1, 17, 20, 21, 23, 24, 36, 43, 53, 54, 57, 58,
60, 68, 94, 130, 212a, 229, 230, 231, 237,
264, 259, 289, 298, 334, 343, 394, 393,
451, 488, 495, 506, 507, 527, 529, 555,
581, 617, 645, 646, 653, 689, 768, 769,
826, 827, 828, 831, 834, 856, 857, 903,
904, 905, 906, 907, 908, 909, 910, 911,
912, 913, 914, 970, 978, 983, 1029, 1030,
1033, 1046, 1088, 1128, 1142, 1143,
1147, 1150, 1165, 1207
regA Translational repressor of several early
genes
14.6 Extended synthesis of several early
proteins
Auxiliary; restricted in E.
coli rpoB5081 at 42°C
9, 10, 19, 131, 320, 338, 484, 485, 503, 505,
637, 735–738, 835, 860, 951, 952, 953,
975, 1095, 1167, 1182
62 Clamp-loader subunit 21.4 No DNA synthesis Essential 17, 20, 57, 60, 264, 310, 311, 312, 320, 451,
469, 470, 486, 487, 488, 616, 619, 653,
679, 826, 831, 834, 865, 864, 901, 902,
1089, 1217, 1227
44 Clamp-loader subunit 35.8 No DNA synthesis Essential 20, 57, 310, 311, 312, 320, 469, 470, 486,
487, 488, 616, 618, 619, 679, 826, 831,
864, 865, 901, 902, 970, 1032, 1089,
1217, 1227
45 Processivity enhancing sliding clamp of
DNA polymerase; and mobile
enhancer of late promoters
24.9 No DNA synthesis; no late
transcription
Essential 17, 20, 22, 264, 299, 310, 311, 312, 320,
334, 404, 405, 451, 469, 552, 552a, 616,
617, 619, 618, 653, 673, 679, 747, 786,
826, 831, 834, 865, 901, 902, 951, 952,
953, 970, 983, 1031, 1079, 1080, 1081,
1082, 1091, 1092, 1186, 1217, 1227
rpbA RNAP-binding protein 14.7 Auxiliary 444, 552, 786, 1171, 1172, 1174
46 Recombination protein and nuclease
subunit
63.6 Recombination deficient; DNA
arrest; no host DNA degradation
Essential in B strains;
mutants are “leaky” in
some K strains
60, 68, 93, 111, 184, 195, 264, 345, 380,
403, 451, 605, 627, 668, 731, 740, 744,
768, 769, 775, 784, 1036, 1047, 1138,
1163, 1164
47 Recombination protein and nuclease
subunit
39.2 Recombination deficient; DNA
arrest; no host DNA degradation
Essential in B strains;
mutants are “leaky” in
some K strains
93, 345, 403, 605, 731, 744, 768, 769, 1036,
1164
␣-gt ␣-Glucosyltransferase 46.7 No ␣-glucosylation of HMC Auxiliary 140, 316, 345, 437, 924, 1072, 1084, 1191
mobB Putative site-specific intron-like DNA
endonuclease
30.4 Nonessential 48, 1072
55 ␴ factor recognizing late T4 promoters 21.5 No late transcription Essential 97, 98, 109, 310, 313, 311, 345, 404, 552,
635, 834, 895, 1038, 1082, 1171, 1173,
1174, 1186
98 MILLER ET AL. MICROBIOL.MOL.BIOL.REV.

nrdH ⫽ 55.7 Anaerobic nucleotide reductase subunit 11.7 Auxiliary 257, 368, 1085
nrdG ⫽ 55.9 Anaerobic nucleotide reductase subunit 18.2 Auxiliary 660, 1228
mobC ⫽ 55.10 Putative intron-like DNA endonuclease 24.0 Auxiliary 1072
nrdD ⫽ sunY Anaerobic ribonucleotide reductase
subunit; RNA contains a self-splicing
intron
68.0 Anaerobic growth 39, 342, 882, 1053, 1086, 1203, 1229, 1237;
M. Ohman-Heden, personal
communication
I-TevII Endonuclease for nrdD-intron homing 30.4 Nonessential 52, 178, 251, 342, 661, 662, 882, 993, 991,
1085
49 Recombination endonuclease VII 18.1 No resolution of recombination
junctions; incomplete packaging
of DNA; reduced heteroduplex
repair, reduced DNA synthesis
Essential 39, 70, 79, 81, 82, 172, 213, 249, 250, 278,
300, 285, 330, 331, 332, 333, 350, 522,
523, 524, 525, 526, 541, 559, 669, 670,
740, 768, 769, 783, 788, 792, 793, 817,
883, 1025, 1030, 1029, 1047, 1083, 1085,
1226; G. Mosig and D. Powell, Abstr.
Annu. Meet. ASM, p. 209, 1985
49⬘ Internal translation initiation product 11.9 39, 784, 788
pin Inhibitor of host Lon protease 18.8 Degradation of amber peptides Auxiliary 1005, 1012, 1085
nrdC Thioredoxin, glutaredoxin 10.1 Auxiliary 64, 257, 341, 460, 632, 815, 816, 1066,
1085
mobD Putative site-specific DNA
endonucleasee
30.5 Nonessential 1072
rI ⫽ tk.-2 Membrane protein 11.1 No lysis inhibition Auxiliary 3, 56, 224, 236, 851
tk Thymidine kinase 21.6 Auxiliary 156, 157, 348, 604, 696, 733, 1112; Thomas
et al., unpublished
vs Modifier of valyl-tRNA synthetase 13.1 Auxiliary 688, 713, 842, 843, 1112
regB Site-specific RNase 18.0 Misregulation of early genes;
specific mRNAs stabilized
Auxiliary 156, 736, 942, 943, 955, 1106, 1112
denV Endonuclease V; N-glycosidase 16.1 UV sensitive Auxiliary 35, 219, 222, 223, 232, 304, 339, 575, 604,
620, 621, 622, 623, 656, 657, 685, 714,
715, 716, 718, 758, 806, 812, 813, 832,
862, 884, 885, 899, 969, 1110, 1111,
1112, 1117, 1120, 1151, 1212, 1213
ipII Internal protein II 11.1ⴱ 9.9 Auxiliary 84, 88, 89, 442, 595, 604, 1093, 1112
ipIII Internal protein III 21.7ⴱ 20.4 Auxiliary 84, 88, 89, 442, 434, 451, 595, 604, 802,
803, 804, 1093, 1112, 1114a
e Soluble lysozyme; endolysin 18.7 No cell lysis Essential, except when
suppressed by sp and
5 mutations
2, 3, 4, 50, 261, 268, 346, 500, 594, 604,
704, 720, 787, 850, 871, 872, 948, 1050,
1099, 1158, 1193
nudE ⫽ e.1 Nudix hydrolase 17.0 Auxiliary 1204
goF3 Allow T4 growth in nusD rho hosts Auxiliary 720, 1045
rnaC ⫽ species 1 Stable RNA Nonessential 110, 302, 707, 870, 962
rnaD ⫽ species 2 Stable RNA Nonessential 110, 302, 707, 870, 962
tRNA
Arg
psu
4
opal suppressor Auxiliary; CT439 5, 110, 284, 302, 328, 361, 366, 367, 501,
707, 710–712, 870, 962, 964, 1178, 1179,
1180
segB Probable site-specific intron-like DNA
endonuclease
26.2 Nonessential 110, 302, 604, 772, 988
tRNA
Ile
Auxiliary; CT439 302, 707, 962
tRNA
Thr
Auxiliary; CT439 302, 707, 962
tRNA
Ser
psu
a
; psu
b
; psu
t
; amber suppressors Auxiliary; CT439 302, 707, 962
tRNA
Pro
Auxiliary; CT439 302, 707, 962
tRNA
Gly
Auxiliary; CT439 302, 707, 962
tRNA
Leu
psu
3
Auxiliary; CT439 302, 707, 962
tRNA
Gln
psu
2
; SB Auxiliary; CT439 302, 707, 962
ip1 Internal protein 1 10.2ⴱ 8.5 Auxiliary; CT596 6, 84, 87, 88, 89, 110, 442, 543, 595, 1093,
1112
57B 17.3 ? 110, 280, 409, 410, 922
57A Chaperone of long and short tail fiber
assembly
8.7 Defective tail fiber assembly Essential; bypassed by
certain host mutations
110, 122, 186, 319, 391, 401, 409, 410, 699,
922
1 dNMP kinase 27.3 No DNA synthesis Essential 110, 184, 241, 264, 348, 543, 696, 834
Continued on following page
VOL. 67, 2003 BACTERIOPHAGE T4 GENOME 99

TABLE 2—Continued
3 Head-proximal tip of tail tube 19.7 Unstable tails Essential 7, 186, 264, 535, 536, 543, 648, 1124
2 ⫽ 64 Protein protecting DNA ends 31.6 Noninfectious particles with filled
heads
Essential, except in
recBCD hosts
28, 89, 186, 249, 250, 264, 543, 647, 1000,
1001, 1074, 1144
4 ⫽ 50 ⫽ 65 Head completion protein 17.6 Noninfectious particles with filled
heads but tails attached at wrong
angles
Essential 89, 249, 250, 264, 543, 787
53 Base plate wedge component 23.0 Defective tails Essential 186, 249, 250, 530, 531, 532, 787, 1155,
1157
5 Base plate lysozyme; hub component 63.1ⴱ 44* 19 Defective tails Essential 2, 186, 249, 264, 497, 500, 530, 531, 532,
787, 807, 1063, 1119, 1157
oriE DNA replication origin; cis-acting
sequences in genes 4, 53, 5; primer
transcript in opposite orientation of
gene 5 transcripts
No DNA synthesis from oriE Auxiliary 378, 563, 641, 779, 1109, 1215; G. Lin and
G. Mosig, unpublished data
repEB Protein required for initiation from oriE 5.48 No DNA replication from oriE Auxiliary; synthetic lethal
with motA mutation
1109
repEA Protein auxiliary for initiation from oriE 6.13 Anomalous DNA replication from
oriE
Auxiliary 1109
segC Site-specific intron-like DNA
endonuclease
16.0 Nonessential 490, 641, 988, 989a; Lin and Mosig,
unpublished
6 Base plate wedge component 74.4 Defective tails; permit plating of
fiberless phage
Essential 186, 193, 249, 253, 264, 537, 1119, 1157;
R. Marsh, personal communication
7 Base plate wedge component 119.2 Defective tails; permit plating of
fiberless phage
Essential 186, 193, 249, 250, 253, 264, 537, 1119,
1156, 1157; Marsh, personal
communication
8 Base plate wedge component 38.0 Defective tails Essential 186, 250, 249, 253, 264, 537, 1119, 1156,
1157
9 Base plate wedge component, tail fiber
socket, trigger for tail sheath
contraction
31.0 No attachment of tail fibers Essential 186, 250, 264, 535, 537, 562, 876, 1114a,
1155, 1157
10 Base plate wedge component, tail pin 66.2 Defective tails Essential 186, 249, 250, 264, 272, 537, 726, 867, 868,
876, 1119, 1155, 1156, 1157, 1239
11 Base plate wedge component, tail pin,
interface with short tail fibers, gp12
23.7 Defective tails Essential 186, 249, 250, 264, 535, 537, 633, 868, 867,
876, 1119, 1155, 1157, 1239
12 Short tail fibers 56.2 Defective tails Essential 122, 186, 391, 521, 535, 537, 745, 972,
1114a, 1155, 1157
wac Whiskers, facilitate long tail fiber
attachment
51.9 No whiskers Auxiliary 186, 214, 745, 877, 1024, 1065, 1114a, 1188
13 Head completion 34.7 Inactive, but filled heads Essential 89, 249, 250, 264, 973, 1114a
14 Head completion 29.6 Inactive, but filled heads Essential 89, 250, 249, 264, 973, 1114a
15 Proximal tail sheath stabilizer, connector
to gp3 and/or gp19
31.6 Defective tails Essential 249, 250, 264, 272, 535, 537, 973, 1114a
16 Terminase subunit, binds dsDNA 18.4 Empty heads Nearly essential 85, 86, 89, 90, 249, 250, 264, 286, 287, 642,
643, 644, 669, 802, 803, 873, 891, 1194
16⬘ Truncated C-terminal end
17 Terminase subunit with nuclease and
ATPase activity; binds single-stranded
DNA, gp16 and gp20
69.8 Empty heads Essential 75, 85, 86, 89, 90, 249, 250, 264, 286, 287,
288, 433, 586, 631, 642, 643, 669, 746,
769, 784, 785, 873, 891, 892, 893, 1194,
1195, 1196
17⬘A Terminase subunits with nuclease and 59.2 ? 286, 287, 288, 333, 784
17⬘B ATPase activity; internal transcription
and translation in frame; does not
bind ssDNA
57.1
17⬙ Terminase subunit with nuclease and
ATPase activity (transcript processing
and internal initiation of translation
in frame); does not bind ssDNA;
several additional proteins most likely
initiated from internal ribosome
binding sites of the 17 transcripts
46.8 ? 286, 287, 288
100 MILLER ET AL. MICROBIOL.MOL.BIOL.REV.

18 Tail sheath monomer 71.3 Defective tails Essential 29, 31, 186, 249, 250, 264, 272, 535, 537,
1096, 1119, 1157
19 Tail tube monomer 18.5 Defective tails Essential 30, 186, 249, 250, 264, 272, 535, 536, 537,
1119, 1157, 1194
20 Portal vertex protein of the head 61.0 Polyheads Essential 86, 89, 90, 238, 250, 264, 333, 608, 642,
643, 694, 990, 1114a
pip ⫽ 67 Prohead core protein; precursor to
internal peptides
9.1ⴱ small peptides Defective heads Essential 89, 519, 1130, 1131
68 Prohead core protein 15.9 Isometric heads Essential 89, 516, 518, 520
21 Prohead core protein and protease 23.3ⴱ small peptides No or defective heads Essential 89, 250, 264, 329, 414, 516, 517, 606, 608,
844, 845, 990, 1116
21⬘ Prohead core protein and protease
(internal initiation of translation)
20.8ⴱ small peptides Defective heads 414
22 Prohead core protein; precursor to
internal peptides
29.9ⴱ small peptides No or faulty heads Essential 89, 250, 264, 270, 518, 595, 608, 728, 805,
844, 845, 990, 1094, 1093, 1114a
23 Precursor of major head subunit 56.0ⴱ 48.7ⴱ 43 No or faulty heads; gol mutations in
gene 23 allow growth in lit hosts
(CTR5x)
Essential; Gol peptide
together with E. coli
Lit, cleaves host EF-
Tu
27, 65, 86, 89, 90, 158, 218, 225, 226, 250,
256, 260, 264, 270, 315, 396, 461, 466,
606, 608, 684, 719, 754, 825, 841, 854,
936, 1021, 1093, 1094, 1119, 1231
segD Probable site-specific intron-like DNA
endonuclease
25.6 Nonessential 490, 988
24 ⫽ os Precursor of head vertex subunit 47.0ⴱ 46 No or faulty heads, osmotic shock
resistance
Essential; bypassed by
certain gene 23
mutations
8, 76, 89, 250, 262, 264, 396, 461, 606, 608,
634, 719, 1114a; G. Yasuda, G. A.
Churchill, M. Parker, and D. Moorey,
personal communication
rnlB ⫽ 24.1 Second RNA ligase 37.6 ? 426
hoc ⫽ eph Large outer capsid protein 40.4 Unstable capsids Auxiliary 89, 167, 164, 168, 461, 462, 496, 916, 917,
1205
inh ⫽ lip Minor capsid protein; inhibitor of gp21
protease
25.6 Auxiliary 496
segE Probable site-specific intron-like DNA
endonuclease
22.9 Nonessential 489, 490, 988
uvsW ⫽ dar RNA-DNA- and DNA-helicase; DNA-
dependent ATPase
67.5 UV sensitive; fail to unwind
R-loops; suppress T4 59 uvsX,
uvsY, and 46 mutations
Auxiliary 132, 195, 196, 207, 208, 212, 244, 722, 737,
768, 769, 1061, 1191, 1197, 1199, 1222,
1240
uvsY ⫽ fdsB ssDNA binding, recombination and
repair protein; helper of UvsX,
inhibitor of endoVII
15.8 UV sensitive;
recombination-deficient; repair-
deficient, DNA arrest; suppress
T4 49 mutations
Auxiliary 25, 44, 82, 182, 183, 195, 212, 213, 232,
357, 358, 380, 387, 392, 522, 542, 548,
589, 723, 724, 739, 768, 769, 1013, 1047,
1054, 1055, 1060, 1061, 1138, 1191,
1199, 1210, 1225, 1222, 1223, 1240
oriF ⫽ oriuvsY DNA replication origin; cis-acting
sequences in genes uvsY, uvsY.-1 and
uvsY.-2; primer transcript same as
uvsY, uvsY.-1 and uvsY.-2 transcript
No DNA synthes from oriF Auxiliary 46, 133, 357, 378, 563, 574, 573, 576, 577,
678, 724, 779, 830, 1109, 1215
25 Base plate wedge subunit 15.1 Defective tails Essential 186, 249, 250, 264, 356, 358, 357, 530, 531,
532, 540, 822, 819, 1057, 1155, 1157; B.
Szewczyk and J. Nieradko, personal
communication; E. Tourkin and B.
Poglozov,
26 Base plate hub subunit 23.9 Defective tails Essential 186, 250, 264, 357, 531, 540, 567, 820, 958,
1108, 1157, 1240
26⬘ Internal in-frame translation initiation 12 ? 357, 823
26⬙ Internal out-of-frame translation
initiation
10.9 ? 1108
51 Base plate hub assembly catalyst? 29.3 Defective tails Essential 186, 249, 250, 264, 357, 540, 567, 821, 958,
1157; Szewczyk and Nieradko, personal
communication
27 Base plate hub subunit 44.5 Defective tails; permit plating of
fiberless phage
Essential 104, 186, 193, 249, 250, 264, 532, 1157,
1240
Continued on following page
VOL. 67, 2003 BACTERIOPHAGE T4 GENOME 101

TABLE 2—Continued
28 Base plate distal hub subunit 20.1 Defective tails Essential 186, 249, 250, 264, 532, 565, 566, 568,
1157, 1240
29 Base plate hub; determinant of tail
length
64.4 Defective tails Essential 7, 186, 242, 243, 249, 250, 264, 532, 463,
464, 537, 1114a, 1157, 1240
48 Base plate; tail tube associated 39.7 Defective tails Essential 61, 186, 242, 243, 249, 250, 264, 463, 464,
535, 536, 1114a, 1157
54 Base plate-tail tube initiator 35.0 Defective tails Essential 61, 186, 243, 250, 249, 264, 463, 464, 530,
531, 535, 536, 1155, 1157
alt Adenosylribosyltransferase (packaged
and injected with DNA)
75.8 Synthetic defective with modA and
modB deletions
Auxiliary 323, 324, 413, 435, 544, 545, 552, 937a,
1170
30 ⫽ lig DNA ligase 55.3 DNA arrest; hyperrecombination Essential; can be by-
passed by functioning
host ligase, when T4
rII is defective
32, 68, 184, 269, 439, 504, 580, 734, 776,
769, 821, 826, 1177, 1235; Thomas et
al., unpublished
rIII Unknown 9.3 Rapid lysis Auxiliary 2, 3, 4, 224, 851, 875, 896, 897, 898, 923,
1235
31 Cochaperonin for GroEL 12.1 Head assembly; gp23 forms lumps;
T4 topoisomerase is defective
Essential 27, 89, 226, 250, 264, 318, 319, 528, 607,
613, 693, 818, 824, 875, 896, 897, 898,
926, 927, 928, 1004, 1093, 1094, 1115
cd dCMP deaminase 21.2 Auxiliary 170, 347, 376, 377, 682, 696, 717, 755, 756
pseT Deoxyribonucleotide3⬘ phosphatase, 5⬘
polynucleotide kinase
34.6 Auxiliary; CTr5x (lit) 129, 185, 203, 512, 513, 514, 732, 734,
1008, 1021; Thomas et al., unpublished
alc ⫽ unf RNA polymerase- and DNA-binding
protein; transcription terminator on
dC-containing DNA
19.0 Allow transcript elongation on C-
DNA; no unfolding of host
nucleoid
E. coli (pR386) 239, 406, 407, 511, 550, 597, 603, 786, 976,
1009, 1019, 1020, 1022
rnlA ⫽ 63 RNA ligase; catalyst of tail fiber
attachment
43.5 Defective tail fiber attachment Auxiliary 319, 362, 374, 467, 721, 734, 889, 944,
1014, 1114a
denA Endonuclease II that restricts dC-
containing DNA
16.7 Defective in host DNA degradation Auxiliary; restricted in E.
coli B rpoB5081
137, 139, 134, 136, 135, 431, 569, 734, 737,
1149, 1153
nrdB Ribonucleotide reductase ␤ subunit
(contains intron)
45.4 Reduced DNA synthesis Auxiliary; nrd-defective
hosts
63, 169, 173, 247, 341, 342, 348, 349, 382,
398, 696, 734, 1010, 1097, 1191, 1218,
1219
I-TevIII Defective intron homing endonuclease 11.3 Nonessential 178, 247, 342, 609, 882, 991, 993, 1010
mobE Putative mobile endonuclease 16.5 Nonessential Thomas et al., unpublished
nrdA Ribonucleotide reductase ␣ subunit 86.0 Reduced DNA synthesis Auxiliary; nrd-defective
hosts
63, 169, 348, 349, 382, 398, 604, 696, 734,
1098, 1097, 1218, 1219
td Thymidylate synthetase (contains intron) 33.1 Reduced DNA synthesis Auxiliary; td-defective
hosts
114, 162, 173, 179, 255, 274, 341, 342, 348,
349, 373, 377, 397, 431, 604, 695, 698,
717, 881, 882, 991, 1002, 1157
I-TevI Intron-homing endonuclease 28.2 Nonessential 52, 114, 119, 120, 174, 175, 178, 206, 251,
252, 342, 348, 349, 453, 661, 662, 796,
797, 798, 882, 991, 993
frd Dihydrofolate reductase 21.7 Reduced DNA synthesis Auxiliary 162, 173, 347, 349, 377, 381, 431, 604, 734,
763, 880, 881, 882
32 ssDNA-binding protein, scaffold of
DNA replication, recombination and
DNA precursor-synthesizing protein
machines
33.5 DNA arrest, UV sensitive,
recombination and excision
repair deficient
Essential; Tab32 for ts
mutants; 32 am
mutations in ochre-
suppressor-containing
hosts are suppressed