The phage λ rexA and rexB genes are expressed from the PRM promoter in λ lysogens along with the cI repressor gene. RexB is also expressed from a second promoter, PLIT, embedded in rexA. The combined expression of rexA and rexB causes Escherichia coli to be more ultraviolet (UV) sensitive. Sensitivity is further increased when RexB levels are reduced by a defect in the PLIT promoter, thus the degree of sensitivity can be modulated by the ratio of RexA/RexB. Expression of the phage λ ren gene rescues this host UV sensitive phenotype; Ren also rescues an aberrant lysis phenotype caused by RexA and RexB. We screened an E. coli two-hybrid library to identify bacterial proteins with which each of these phage proteins physically interact. The results extend previous observations concerning λ Rex exclusion and show the importance of E. coli electron transport and sulfur assimilation pathways for the phage.
Get full access to this article
View all access options for this article.
References
1.
HayesS, BullHJ, TullochJ. The Rex phenotype of altruistic cell death following infection of a λ lysogen by T4rII mutants is suppressed by plasmids expressing OOP RNA. Gene, 1997; 189(1):35–42; doi: 10.1016/s0378-1119(96)00824-4.
2.
HayesS, SzybalskiW. Control of short leftward transcripts from the immunity and ori regions in induced coliphage lambda. Mol Gen Genet, 1973; 126(4):275–290; doi: 10.1007/BF00269438.
3.
LandsmannJ, KrogerM, HobomG. The rex region of bacteriophage lambda: Two genes under three-way control. Gene, 1982; 20(1):11–24; doi: 10.1016/0378-1119(82)90083-x.
4.
PirrottaV, IneichenK, WalzA. An unusual RNA polymerase binding site in the immunity region of phage lambda. Mol Gen Genet, 1980; 180(2):369–376; doi: 10.1007/BF00425850.
5.
ThomasonLC, SchiltzCJ, CourtC, et al.Bacteriophage λ RexA and RexB functions assist the transition from lysogeny to lytic growth. Mol Microbiol, 2021; 116(4):1044–1063; doi: 10.1111/mmi.14792.
6.
ParmaDH, SnyderM, SobolevskiS, et al.The Rex system of bacteriophage λ: Tolerance and altruistic cell death. Genes Dev, 1992; 6(3):497–510; doi: 10.1101/gad.6.3.497.
7.
SnyderL, McWilliamsK. The rex genes of bacteriophage lambda can inhibit cell function without phage superinfection. Gene, 1989; 81(1):17–24; doi: 10.1016/0378-1119(89)90332-6.
8.
LiBH, KwasniewskiM, KirchnerJ, et al.RexAB proteins of bacteriophage λ enhance the effect of photolyase-dimer complexes on lacZ gene expression in Escherichia coli. Mol Gen Genet, 1992; 231(3):480–484; doi: 10.1007/BF00292719.
9.
FixD.The rex genes of lambda prophage modify ultraviolet light and N-methyl-N-nitrosourea-induced responses to DNA damage in Escherichia coli. Mutat Res, 1993; 303(4):143–150; doi: 10.1016/0165-7992(93)90015-n.
10.
ThomasonLC, MorrillK, MurrayG, et al.Elements in the λ immunity region regulate phage development: Beyond the ‘Genetic Switch’. Mol Microbiol, 2019; 112(6):1798–1813; doi: 10.1111/mmi.14394.
11.
BenzerS.Fine structure of a genetic region in bacteriophage. Proc Natl Acad Sci USA, 1955; 41(6):344–354; doi: 10.1073/pnas.41.6.344.
12.
GarenA.Physiological effects of rII mutations in bacteriophage T4. Virology, 1961; 14:151–163; doi: 10.1016/0042-6822(61)90190-8.
13.
SekiguchiM.Studies on the physiological defect in rII mutants of bacteriophage T4. J Mol Biol, 1966; 16(2):503–522; doi: 10.1016/s0022-2836(66)80188-2.
14.
WeintraubSB, FrankelFR. Identification of the T4rIIB gene product as a membrane protein. J Mol Biol, 1972; 70(3):589–615; doi: 10.1016/0022-2836(72)90561-x.
15.
EnnisHL, KievittKD. Association of the rIIA protein with the bacterial membrane. Proc Natl Acad Sci USA, 1973; 70(5):1468–1472; doi: 10.1073/pnas.70.5.1468.
16.
ChiuCS, CookKS, GreenbergGR. Characteristics of a bacteriophage T4-induced complex synthesizing deoxyribonucleotides. J Biol Chem, 1982; 257(24):15087–15097.
17.
ColowickMS, ColowickSP. Membrane ATPase activation on infection of E. coli K (λ) cells with phage T4rII mutants. Trans N Y Acad Sci, 1983; 41:35–40; doi: 10.1111/j.2164-0947.1983.tb02781.x.
18.
ToothmanP, HerskowitzI. Rex-dependent exclusion of lambdoid phages. III. Physiology of the abortive infection. Virology, 1980; 102(1):161–171; doi: 10.1016/0042-6822(80)90078-1.
19.
ToothmanP, HerskowitzI. Rex-dependent exclusion of lambdoid phages. II. Determinants of sensitivity to exclusion. Virology, 1980; 102(1):147–160; doi: 10.1016/0042-6822(80)90077-x.
20.
ToothmanP, HerskowitzI. Rex-dependent exclusion of lambdoid phages. I. Prophage requirements for exclusion. Virology, 1980; 102(1):133–146; doi: 10.1016/0042-6822(80)90076-8.
21.
SignerER, WeilJ. Recombination in bacteriophage λ. I. Mutants deficient in general recombination. J Mol Biol, 1968; 34(2):261–271; doi: 10.1016/0022-2836(68)90251-9.
22.
ThomasonLC, CostantinoN, CourtDL. Examining a DNA replication requirement for bacteriophage λ Red- and Rac Prophage RecET-promoted recombination in Escherichia coli. mBio, 2016; 7(5):e01443; doi: 10.1128/mBio.01443-16.
23.
BetterM, FreifelderD. Studies on the replication of Escherichia coli phage λ DNA. I. The kinetics of DNA replication and requirements for the generation of rolling circles. Virology, 1983; 126(1):168–182; doi: 10.1016/0042-6822(83)90469-5.
24.
EnquistLW, SkalkaA. Replication of bacteriophage λ DNA dependent on the function of host and viral genes. I. Interaction of red, gam, and rec. J Mol Biol, 1973; 75(2):185–212; doi: 10.1016/0022-2836(73)90016-8.
25.
ThomasonLC, CourtD. Progress in Understanding Phage λ Rex Functions. 17th Annual Microbial Genomics Conference; Rocky Gap State Park, Cumberland, MD; 2009.
26.
StahlF, MyersR. Old and new concepts for the role of chi in bacterial recombination. J Hered, 1995; 86(5):327–329; doi: 10.1093/oxfordjournals.jhered.a111599.
27.
BattestiA, BouveretE. The bacterial two-hybrid system based on adenylate cyclase reconstitution in Escherichia coli. Methods, 2012; 58(4):325–334; doi: 10.1016/j.ymeth.2012.07.018.
KarimovaG, DautinN, LadantD. Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J Bacteriol, 2005; 187(7):2233–2243; doi: 10.1128/JB.187.7.2233-2243.2005.
30.
WongS, AlattasH, SlavcevRA. A snapshot of the lambda T4rII exclusion (Rex) phenotype in Escherichia coli. Curr Genet, 2021; 67(5):739–745; doi: 10.1007/s00294-021-01183-2.
31.
NakayashikiT, SaitoN, TakeuchiR, et al.The tRNA thiolation pathway modulates the intracellular redox state in Escherichia coli. J Bacteriol, 2013; 195(9):2039–2049; doi: 10.1128/JB.02180-12.
32.
LiXT, JunY, ErickstadMJ, et al.tCRISPRi: Tunable and reversible, one-step control of gene expression. Sci Rep, 2016; 6:39076; doi: 10.1038/srep39076.
33.
GaussP, ThomasonLC, RodriquezJ. The λ ren. gene suppresses rex restriction of T4 rII mutants. In: Evergreen International Phage Biology Meeting. (Kutter B. ed.) Evergreen State College: Olympia, Washington; 2009.
34.
OuelletteSP, KarimovaG, DaviM, et al.Analysis of membrane protein interactions with a bacterial adenylate cyclase-based two-hybrid (BACTH) technique. Curr Protoc Mol Biol, 2017; 118:20.12.1–20.12.24; doi: 10.1002/cpmb.36.
35.
ThomasonLC, MurphyKC. The Bacteriophage λ Red Recombination System and the Development of Recombineering Technologies. In: Reference Module in Life Sciences. Encyclopedia of Virology 4th edition (Dennis Bamford, and Mark Zuckerman, eds.), Elsevier; 2020.
SinhaPK, Nakamaru-OgisoE, Torres-BaceteJ, et al.Electron transfer in subunit NuoI (TYKY) of Escherichia coli NADH:quinone oxidoreductase (NDH-1). J Biol Chem, 2012; 287(21):17363–17373; doi: 10.1074/jbc.M111.329649.
38.
LeyhTS, TaylorJC, MarkhamGD. The sulfate activation locus of Escherichia coli K12: Cloning, genetic, and enzymatic characterization. J Biol Chem, 1988; 263(5):2409–2416.
39.
LevequeF, PlateauP, DessenP, et al.Homology of lysS and lysU, the two Escherichia coli genes encoding distinct lysyl-tRNA synthetase species. Nucleic Acids Res, 1990; 18(2):305–312; doi: 10.1093/nar/18.2.305.
40.
KozminSG, WangJ, SchaaperRM. Role for CysJ flavin reductase in molybdenum cofactor-dependent resistance of Escherichia coli to 6-N-hydroxylaminopurine. J Bacteriol, 2010; 192(8):2026–2033; doi: 10.1128/JB.01438-09.
41.
AsaiK, FujisakiS, NishimuraY, et al.The identification of Escherichia coli ispB (cel) gene encoding the octaprenyl diphosphate synthase. Biochem Biophys Res Commun, 1994; 202(1):340–345; doi: 10.1006/bbrc.1994.1933.
42.
PrussBM, NelmsJM, ParkC, et al.Mutations in NADH:ubiquinone oxidoreductase of Escherichia coli affect growth on mixed amino acids. J Bacteriol, 1994; 176(8):2143–2150; doi: 10.1128/jb.176.8.2143-2150.1994.
43.
MitchellP.Keilin's respiratory chain concept and its chemiosmotic consequences. Science (New York, NY), 1979; 206(4423):1148–1159; doi: 10.1126/science.388618.
44.
LehmanIR.DNA ligase: Structure, mechanism, and function. Science (New York, NY), 1974; 186(4166):790–797; doi: 10.1126/science.186.4166.790.
45.
EdgarRS, DenhardtGH, EpsteinRH. A comparative genetic study of conditional lethal mutations of bacteriophage T4d. Genetics, 1964; 49:635–648; doi: 10.1093/genetics/49.4.635.
46.
KaramJD.DNA replication of phage T4 rII mutants without polynucleotide ligase (gene 30). Biochem Biophys Res Commun, 1969; 37(3):416–422; doi: 10.1016/0006-291x(69)90931-0.
47.
BergerH, KozinskiAW. Suppression of T4D ligase mutations by rIIA and rIIB mutations. Proc Natl Acad Sci USA, 1969; 64(3):897–904; doi: 10.1073/pnas.64.3.897.
48.
ZimmermanSB, LittleJW, OshinskyCK, et al.Enzymatic joining of DNA strands: A novel reaction of diphosphopyridine nucleotide. Proc Natl Acad Sci USA, 1967; 57(6):1841–1848; doi: 10.1073/pnas.57.6.1841.
49.
SekowskaA, KungHF, DanchinA. Sulfur metabolism in Escherichia coli and related bacteria: Facts and fiction. J Mol Microbiol Biotechnol, 2000; 2(2):145–177.
50.
KrogerM, HobomG. A chain of interlinked genes in the ninR region of bacteriophage lambda. Gene, 1982; 20(1):25–38; doi: 10.1016/0378-1119(82)90084-1.
51.
AltschulSF, GishW, MillerW, et al.Basic local alignment search tool. J Mol Biol, 1990; 215(3):403–410; doi: 10.1016/S0022-2836(05)80360-2.
52.
MaynardND, BirchEW, SanghviJC, et al.A forward-genetic screen and dynamic analysis of lambda phage host-dependencies reveals an extensive interaction network and a new anti-viral strategy. PLoS Genet, 2010; 6(7):e1001017; doi: 10.1371/journal.pgen.1001017.
53.
MaynardND, MacklinDN, KirkegaardK, et al.Competing pathways control host resistance to virus via tRNA modification and programmed ribosomal frameshifting. Mol Syst Biol, 2012; 8:567; doi: 10.1038/msb.2011.101.
54.
BabaT, AraT, HasegawaM, et al.Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection. Mol Syst Biol, 2006; 2:2006; doi: 10.1038/msb4100050.
55.
LauhonCT.Requirement for IscS in biosynthesis of all thionucleosides in Escherichia coli. J Bacteriol, 2002; 184(24):6820–6829; doi: 10.1128/JB.184.24.6820-6829.2002.
56.
SchwartzCJ, DjamanO, ImlayJA, et al.The cysteine desulfurase, IscS, has a major role in in vivo Fe-S cluster formation in Escherichia coli. Proc Natl Acad Sci USA, 2000; 97(16):9009–9014; doi: 10.1073/pnas.160261497.
57.
LevinME, HendrixRW, CasjensSR. A programmed translational frameshift is required for the synthesis of a bacteriophage λ tail assembly protein. J Mol Biol, 1993; 234(1):124–139; doi: 10.1006/jmbi.1993.1568.
58.
KwongTC, SteegeD, LawlerD, et al.Bacteriophage lambda induction causes increased production of E. coli lysine transfer RNA. Arch Biochem Biophys, 1975; 170(2):651–658; doi: 10.1016/0003-9861(75)90161-7.
59.
CourtD, OppenheimAB. Phage lambda's accessory genes. In: Lambda II. (Hendrix RW, Roberts JW, Stahl FW, et al. eds.) Cold Spring Harbor Laboratory: Cold Spring Harbor, NY; 1983; pp. 251–277.
60.
DanielsDL, SchroederJL, SzybalskiW, et al. Complete annotated lambda sequence. In: Lambda II. (Hendrix RW, Roberts JW, Stahl FW, et al. eds.) Cold Spring Harbor Press: Cold Spring Harbor, NY; 1983; pp. 519–676.
61.
Castano-CerezoS, BernalV, PostH, et al.Protein acetylation affects acetate metabolism, motility and acid stress response in Escherichia coli. Mol Syst Biol, 2014; 10:762.
KoyuncuE, BudayevaHG, MitevaYV, et al.Sirtuins are evolutionarily conserved viral restriction factors. mBio, 2014; 5(6):e02249; doi: 10.1128/mBio.02249-14.
64.
GnandtE, DörnerK, StrampraadMFJ, et al.The multitude of iron-sulfur clusters in respiratory complex I. Biochim Biophys Acta, 2016; 1857(8):1068–1072; doi: 10.1016/j.bbabio.2016.02.018.
65.
BartonJK, SilvaRMB, O'BrienE. Redox chemistry in the genome: Emergence of the [4Fe4S] cofactor in repair and replication. Annu Rev Biochem, 2019; 88:163–190; doi: 10.1146/annurev-biochem-013118-110644.
66.
StarkC, BreitkreutzBJ, RegulyT, et al.BioGRID: A general repository for interaction datasets. Nucleic Acids Res, 2006; 34(Database Issue):D535–D539; doi: 10.1093/nar/gkj109.
67.
CampbellJH, RolfeBG. Evidence for a dual control of the initiation of host-cell lysis caused by phage lambda. Mol Gen Genet, 1975; 139(1):1–8; doi: 10.1007/BF00267990.
68.
SvenningsenSL, CostantinoN, CourtDL, et al.On the role of Cro in λ prophage induction. Proc Natl Acad Sci USA, 2005; 102(12):4465–4469; doi: 10.1073/pnas.0409839102.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
