Prophages block cell surface receptors to preserve their viral progeny

Sims, A. et al. Superinfection exclusion creates spatially distinct influenza virus populations. PLoS Biol. 21, e3001941 (2023).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Puck, T. T. & Lee, H. H. Mechanism of cell wall penetration by viruses: II. Demonstration of cyclic permeability change accompanying virus infection of Escherichia coli B cells. J. Exp. Med. 101, 151–175 (1955).

CAS 
PubMed 
PubMed Central 

Google Scholar 

McAllister, W. T. & Barrett, C. L. Superinfection exclusion by bacteriophage T7. J. Virol. 24, 709–711 (1977).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Zhang, X.-F. et al. A self-perpetuating repressive state of a viral replication protein blocks superinfection by the same virus. PLoS Pathog. 13, e1006253 (2017).

PubMed 
PubMed Central 

Google Scholar 

Laliberte, J. P. & Moss, B. A novel mode of poxvirus superinfection exclusion that prevents fusion of the lipid bilayers of viral and cellular membranes. J. Virol. 88, 9751–9768 (2014).

PubMed 
PubMed Central 

Google Scholar 

Doceul, V., Hollinshead, M., van der Linden, L. & Smith, G. L. Repulsion of superinfecting virions: a mechanism for rapid virus spread. Science 327, 873–876 (2010).

ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Pedruzzi, I., Rosenbusch, J. P. & Locher, K. P. Inactivation in vitro of the Escherichia coli outer membrane protein FhuA by a phage T5-encoded lipoprotein. FEMS Microbiol. Lett. 168, 119–125 (1998).

CAS 
PubMed 

Google Scholar 

Lu, M. J. & Henning, U. Superinfection exclusion by T-even-type coliphages. Trends Microbiol. 2, 137–139 (1994).

CAS 
PubMed 

Google Scholar 

Cumby, N., Edwards, A. M., Davidson, A. R. & Maxwell, K. L. The bacteriophage HK97 gp15 moron element encodes a novel superinfection exclusion protein. J. Bacteriol. 194, 5012–5019 (2012).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Cumby, N., Reimer, K., Mengin-Lecreulx, D., Davidson, A. R. & Maxwell, K. L. The phage tail tape measure protein, an inner membrane protein and a periplasmic chaperone play connected roles in the genome injection process of E. coli phage HK97. Mol. Microbiol. 96, 437–447 (2015).

CAS 
PubMed 

Google Scholar 

Kuzio, J. & Kropinski, A. M. O-antigen conversion in Pseudomonas aeruginosa PAO1 by bacteriophage D3. J. Bacteriol. 155, 203–212 (1983).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Newton, G. J. et al. Three-component-mediated serotype conversion in Pseudomonas aeruginosa by bacteriophage D3. Mol. Microbiol. 39, 1237–1247 (2001).

CAS 
PubMed 

Google Scholar 

Chung, I.-Y., Jang, H.-J., Bae, H.-W. & Cho, Y.-H. A phage protein that inhibits the bacterial ATPase required for type IV pilus assembly. Proc. Natl Acad. Sci. USA 111, 11503–11508 (2014).

ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Shah, M. et al. A phage-encoded anti-activator inhibits quorum sensing in Pseudomonas aeruginosa. Mol. Cell 81, 571–583 (2021).

CAS 
PubMed 

Google Scholar 

Burrows, L. L. Pseudomonas aeruginosa twitching motility: type IV pili in action. Annu. Rev. Microbiol. 66, 493–520 (2012).

CAS 
PubMed 

Google Scholar 

O’Toole, G. A. & Kolter, R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30, 295–304 (1998).

PubMed 

Google Scholar 

Bondy-Denomy, J. et al. Prophages mediate defense against phage infection through diverse mechanisms. ISME J. 10, 2854–2866 (2016).

PubMed 
PubMed Central 

Google Scholar 

Tsao, Y.-F. et al. Phage morons play an important role in Pseudomonas aeruginosa phenotypes. J. Bacteriol. 200, e00189-18 (2018).

PubMed 
PubMed Central 

Google Scholar 

Battesti, A. & Bouveret, E. The bacterial two-hybrid system based on adenylate cyclase reconstitution in Escherichia coli. Methods 58, 325–334 (2012).

CAS 
PubMed 

Google Scholar 

Alm, R. A., Bodero, A. J., Free, P. D. & Mattick, J. S. Identification of a novel gene, pilZ, essential for type 4 fimbrial biogenesis in Pseudomonas aeruginosa. J. Bacteriol. 178, 46–53 (1996).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Kus, J. V., Tullis, E., Cvitkovitch, D. G. & Burrows, L. L. Significant differences in type IV pilin allele distribution among Pseudomonas aeruginosa isolates from cystic fibrosis (CF) versus non-CF patients. Microbiology 150, 1315–1326 (2004).

CAS 
PubMed 

Google Scholar 

Llontop, E. E. et al. The PilB-PilZ-FimX regulatory complex of the type IV pilus from Xanthomonas citri. PLoS Pathog. 17, e1009808 (2021).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Koch, M. D., Black, M. E., Han, E., Shaevitz, J. W. & Gitai, Z. Pseudomonas aeruginosa distinguishes surfaces by stiffness using retraction of type IV pili. Proc. Natl Acad. Sci. USA 119, e2119434119 (2022).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Chang, Y.-W. et al. Architecture of the type IVa pilus machine. Science 351, aad2001 (2016).

ADS 
PubMed 
PubMed Central 

Google Scholar 

Koch, M. D., Fei, C., Wingreen, N. S., Shaevitz, J. W. & Gitai, Z. Competitive binding of independent extension and retraction motors explains the quantitative dynamics of type IV pili. Proc. Natl Acad. Sci. USA 118, e2014926118 (2021).

CAS 
PubMed 
PubMed Central 

Google Scholar 

González-Valdez, A., Servín-González, L., Juárez, K., Hernandez-Aligio, A. & Soberón-Chávez, G. The effect of specific rhlA-las-box mutations on DNA binding and gene activation by Pseudomonas aeruginosa quorum-sensing transcriptional regulators RhlR and LasR. FEMS Microbiol. Lett. 356, 217–225 (2014).

PubMed 

Google Scholar 

Whiteley, M. & Greenberg, E. P. Promoter specificity elements in Pseudomonas aeruginosa quorum-sensing-controlled genes. J. Bacteriol. 183, 5529–5534 (2001).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Siehnel, R. et al. A unique regulator controls the activation threshold of quorum-regulated genes in Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 107, 7916–7921 (2010).

ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Sztanko, K. M. et al. Prophages express a type IV pilus component to provide anti-phage defence. Preprint at bioRxiv (2024).

Hao, Y., Murphy, K., Lo, R. Y., Khursigara, C. M. & Lam, J. S. Single-nucleotide polymorphisms found in the migA and wbpX glycosyltransferase genes account for the intrinsic lipopolysaccharide defects exhibited by Pseudomonas aeruginosa PA14. J. Bacteriol. 197, 2780–2791 (2015).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Robbins, P. W. & Uchida, T. Studies on the chemical basis of the phage conversion of O-antigens in the E-group Salmonellae. Biochemistry 1, 323–335 (1962).

CAS 
PubMed 

Google Scholar 

Kupczok, A., Bailey, Z. M., Refardt, D. & Wendling, C. C. Co-transfer of functionally interdependent genes contributes to genome mosaicism in lambdoid phages. Microb. Genom. 8, mgen000915 (2022).

PubMed 
PubMed Central 

Google Scholar 

Egido, J. E., Costa, A. R., Aparicio-Maldonado, C., Haas, P.-J. & Brouns, S. J. J. Mechanisms and clinical importance of bacteriophage resistance. FEMS Microbiol. Rev. 46, fuab048 (2022).

CAS 
PubMed 

Google Scholar 

Labrie, S. J., Samson, J. E. & Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8, 317–327 (2010).

CAS 
PubMed 

Google Scholar 

Taylor, V. L., Fitzpatrick, A. D., Islam, Z. & Maxwell, K. L. The diverse impacts of phage morons on bacterial fitness and virulence. Adv. Virus Res. 103, 1–31 (2019).

CAS 
PubMed 

Google Scholar 

Berryhill, B. A. et al. The book of Lambda does not tell us that naturally occurring lysogens of Escherichia coli are likely to be resistant as well as immune. Proc. Natl Acad. Sci. USA 120, e2212121120 (2023).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Hancock, R. E., Hantke, K. & Braun, V. Iron transport of Escherichia coli K-12: involvement of the colicin B receptor and of a citrate-inducible protein. J. Bacteriol. 127, 1370–1375 (1976).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Samsonov, V. V., Samsonov, V. V. & Sineoky, S. P. DcrA and dcrB Escherichia coli genes can control DNA injection by phages specific for BtuB and FhuA receptors. Res. Microbiol. 153, 639–646 (2002).

CAS 
PubMed 

Google Scholar 

Scandella, D. & Arber, W. Phage λ DNA injection into Escherichia coli pel⁻ mutants is restored by mutations in phage genes V or H. Virology 69, 206–215 (1976).

CAS 
PubMed 

Google Scholar 

De Smet, J. et al. High coverage metabolomics analysis reveals phage-specific alterations to Pseudomonas aeruginosa physiology during infection. ISME J. 10, 1823–1835 (2016).

PubMed 
PubMed Central 

Google Scholar 

Høyland-Kroghsbo, N. M. et al. Quorum sensing controls the Pseudomonas aeruginosa CRISPR-Cas adaptive immune system. Proc. Natl Acad. Sci. USA 114, 131–135 (2017).

ADS 
PubMed 

Google Scholar 

Silpe, J. E. & Bassler, B. L. A host-produced quorum-sensing autoinducer controls a phage lysis-lysogeny decision. Cell 176, 268–280 (2019).

CAS 
PubMed 

Google Scholar 

Hunter, M. & Fusco, D. Superinfection exclusion: a viral strategy with short-term benefits and long-term drawbacks. PLoS Comput. Biol. 18, e1010125 (2022).

ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Weller, S. K. & Sawitzke, J. A. Recombination promoted by DNA viruses: phage λ to herpes simplex virus. Annu. Rev. Microbiol. 68, 237–258 (2014).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Read, A. F. The evolution of virulence. Trends Microbiol. 2, 73–76 (1994).

CAS 
PubMed 

Google Scholar 

Guy, B. et al. HIV F/3′ orf encodes a phosphorylated GTP-binding protein resembling an oncogene product. Nature 330, 266–269 (1987).

ADS 
CAS 
PubMed 

Google Scholar 

Kwon, Y. et al. Structural basis of CD4 downregulation by HIV-1 Nef. Nat. Struct. Mol. Biol. 27, 822–828 (2020).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Doron, S. et al. Systematic discovery of antiphage defense systems in the microbial pangenome. Science 359, eaar4120 (2018).

ADS 
PubMed 
PubMed Central 

Google Scholar 

Georjon, H. & Bernheim, A. The highly diverse antiphage defence systems of bacteria. Nat. Rev. Microbiol. 21, 686–700 (2023).

CAS 
PubMed 

Google Scholar 

Hampton, H. G., Watson, B. N. J. & Fineran, P. C. The arms race between bacteria and their phage foes. Nature 577, 327–336 (2020).

ADS 
CAS 
PubMed 

Google Scholar 

Aziz, R. K. et al. The RAST server: rapid annotations using subsystems technology. BMC Genom. 9, 75 (2008).

Google Scholar 

Qiu, D., Damron, F. H., Mima, T., Schweizer, H. P. & Yu, H. D. PBAD-based shuttle vectors for functional analysis of toxic and highly regulated genes in Pseudomonas and Burkholderia spp. and other bacteria. Appl. Environ. Microbiol. 74, 7422–7426 (2008).

ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Csörgő, B. et al. A compact Cascade-Cas3 system for targeted genome engineering. Nat. Methods 17, 1183–1190 (2020).

PubMed 
PubMed Central 

Google Scholar 

Hmelo, L. R. et al. Precision-engineering the Pseudomonas aeruginosa genome with two-step allelic exchange. Nat. Protoc. 10, 1820–1841 (2015).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Jiang, W., Bikard, D., Cox, D., Zhang, F. & Marraffini, L. A. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat. Biotechnol. 31, 233–239 (2013).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Farinha, M. A. & Kropinski, A. M. Construction of broad-host-range plasmid vectors for easy visible selection and analysis of promoters. J. Bacteriol. 172, 3496–3499 (1990).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Liberati, N. T. et al. An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc. Natl Acad. Sci. USA 103, 2833–2838 (2006).

ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).

CAS 
PubMed 
PubMed Central 

Google Scholar 

McCallum, M. et al. PilN binding modulates the structure and binding partners of the Pseudomonas aeruginosa type IVa pilus protein PilM. J. Biol. Chem. 291, 11003–11015 (2016).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Sayers, E. W. et al. Database resources of the national center for biotechnology information. Nucleic Acids Res. 50, D20–D26 (2022).

CAS 
PubMed 

Google Scholar 

Xuan, G., Lin, H. & Wang, J. Expression of a phage-encoded Gp21 protein protects Pseudomonas aeruginosa against phage infection. J. Virol. 96, e01769-21 (2022).

PubMed 
PubMed Central 

Google Scholar 

Kozyrev, D., Svarchevskiĭ, A., Zaĭtsev, E. & Rybchin, V. Lysogenic conversion induced by phages phi 80. I. A description of the phenomenon and the cloning of the conversion gene. Genetika 18, 555–560 (1982).

CAS 
PubMed 

Google Scholar 

Vostrov, A. A., Vostrukhina, O. A., Svarchevsky, A. N. & Rybchin, V. N. Proteins responsible for lysogenic conversion caused by coliphages N15 and phi80 are highly homologous. J. Bacteriol. 178, 1484–1486 (1996).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Kulikov, E. E. et al. Equine intestinal O-Seroconverting temperate coliphage Hf4s: genomic and biological characterization. Appl. Environ. Microbiol. 87, e01124-21 (2021).

PubMed 
PubMed Central 

Google Scholar 

Perry, L. L. et al. Sequence analysis of Escherichia coli O157:H7 bacteriophage ΦV10 and identification of a phage-encoded immunity protein that modifies the O157 antigen. FEMS Microbiol. Lett. 292, 182–186 (2009).

CAS 
PubMed 

Google Scholar 

Wollin, R., Stocker, B. A. & Lindberg, A. A. Lysogenic conversion of Salmonella typhimurium bacteriophages A3 and A4 consists of O-acetylation of rhamnose of the repeating unit of the O-antigenic polysaccharide chain. J. Bacteriol. 169, 1003–1009 (1987).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Villafane, R., Zayas, M., Gilcrease, E. B., Kropinski, A. M. & Casjens, S. R. Genomic analysis of bacteriophage ε34 of Salmonella enterica serovar Anatum (15+). BMC Microbiol. 8, 227 (2008).

PubMed 
PubMed Central 

Google Scholar 

Kim, M. & Ryu, S. Spontaneous and transient defence against bacteriophage by phase-variable glucosylation of O-antigen in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 86, 411–425 (2012).

CAS 
PubMed 

Google Scholar 

Kintz, E. et al. A BTP1 prophage gene present in invasive non-typhoidal Salmonella determines composition and length of the O-antigen of the lipopolysaccharide. Mol. Microbiol. 96, 263–275 (2015).

CAS 
PubMed 
PubMed Central 

Google Scholar 

Woods, D. E., Jeddeloh, J. A. & Fritz, D. L. & DeShazer, D. Burkholderia thailandensisE125 harbors a temperate bacteriophage specific for Burkholderia mallei. J. Bacteriol. 184, 4003–4017 (2002).

Allison, G. E. & Verma, N. K. Serotype-converting bacteriophages and O-antigen modification in Shigella flexneri. Trends Microbiol. 8, 17–23 (2000).

CAS 
PubMed 

Google Scholar 

Clark, C. A., Beltrame, J. & Manning, P. A. The oac gene encoding a lipopolysaccharide O-antigen acetylase maps adjacent to the integrase-encoding gene on the genome of Shigella flexneri bacteriophage Sf6. Gene 107, 43–52 (1991).

CAS 
PubMed 

Google Scholar 

Steiger, H., Müller, U. & Bauer, G. Non-receptivity for ϰ phage of ϰ-lysogenic Serratia and reactions to superinfection of receptive cells with a mutant prophage. Mol. Gen. Genet. 114, 358–367 (1972).

CAS 
PubMed 

Google Scholar 

Coetzee, J. N. Lysogenic conversion in the genus proteus. Nature 189, 946–947 (1961).

ADS 
CAS 
PubMed 

Google Scholar 

Bielmann, R. et al. Receptor binding proteins of Listeria monocytogenes bacteriophages A118 and P35 recognize serovar-specific teichoic acids. Virology 477, 110–118 (2015).

CAS 
PubMed 

Google Scholar 

Williamson, S. J., McLaughlin, M. R. & Paul, J. H. Interaction of the ΦHSIC virus with its host: lysogeny or pseudolysogeny? Appl. Environ. Microbiol. 67, 1682–1688 (2001).

ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Bisen, P. S., Bagchi, S. N. & Audholia, S. Nitrate reductase activity of a cyanobacterium Phormidium uncinatum after cyanophage LPP-1 infection. FEMS Microbiol. Lett. 33, 69–72 (1986).

CAS 

Google Scholar 

Ingmer, H., Gerlach, D. & Wolz, C. Temperate phages of Staphylococcus aureus. Microbiol. Spectr. (2019).

Sun, X., Göhler, A., Heller, K. J. & Neve, H. The ltp gene of temperate Streptococcus thermophilus phage TP-J34 confers superinfection exclusion to Streptococcus thermophilus and Lactococcus lactis. Virology 350, 146–157 (2006).

CAS 
PubMed 

Google Scholar