Phage tailspike modularity and horizontal gene transfer reveals specificity towards E. coli O-antigen serogroups

image
  • Arkin AP, Cottingham RW, Henry CS, Harris NL, Stevens RL, Maslov S, Dehal P, Ware D, Perez F, Canon S, Sneddon MW, Henderson ML, Riehl WJ, Murphy-Olson D, Chan SY, Kamimura RT, Kumari S, Drake MM, Brettin TS, Yu D. KBase: the United States department of energy systems biology knowledgebase. Nat Biotechnol. 2018;36(7):566–9. https://doi.org/10.1038/nbt.4163.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bobay L-M, Touchon M, Rocha EPC. Manipulating or superseding host recombination functions: a dilemma that shapes phage evolvability. PLoS Genet. 2013. https://doi.org/10.1371/journal.pgen.1003825.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Boon M, Holtappels D, Lood C, Van Noort V, Lavigne R. Host range expansion of Pseudomonas virus LUZ7 is driven by a conserved tail fiber mutation. PHAGE: Ther Appl Res. 2020;1(2):87–90. https://doi.org/10.1089/phage.2020.0006.

    Article 

    Google Scholar
     

  • Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomason JA, Stevens R, Vonstein V, Wattam AR, Xia F. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep. 2015;5(1):1–6. https://doi.org/10.1038/srep08365.

    Article 
    CAS 

    Google Scholar
     

  • Casjens SR, Grose JH. Contributions of P2- and P22-like prophages to understanding the enormous diversity and abundance of tailed bacteriophages. Virology. 2016;496:255–76. https://doi.org/10.1016/j.virol.2016.05.022.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Casjens SR, Winn-Stapley DA, Gilcrease EB, Morona R, Kühlewein C, Chua JEH, Manning PA, Inwood W, Clark AJ. The chromosome of shigella flexneri bacteriophage Sf6: complete nucleotide sequence, genetic mosaicism, and DNA packaging. J Mol Biol. 2004;339(2):379–94. https://doi.org/10.1016/J.JMB.2004.03.068.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen C, Bales P, Greenfield J, Heselpoth RD, Nelson DC. Crystal structure of ORF210 from E. coli O157:H1 phage CBA120 (TSP1), a putative tailspike protein. PLoS ONE. 2014;9(3):93156. https://doi.org/10.1371/journal.pone.0093156.

    Article 
    CAS 

    Google Scholar
     

  • Chiu J, Ng K. Escherichia coli O antigen serotype O16 is a restriction factor for bacteriophage T4 infection. J Exp Microbiol Immunol. 2017;3:38–44.


    Google Scholar
     

  • Clark AJ, Inwood W, Cloutier T, Dhillon TS. Nucleotide sequence of coliphage HK620 and the evolution of lambdoid phages. J Mol Biol. 2001;311(4):657–79. https://doi.org/10.1006/JMBI.2001.4868.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Community BO. Blender: a 3D modelling and rendering package (2018). http://www.blender.org

  • Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14(7):1394. https://doi.org/10.1101/GR.2289704.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dunne M, Prokhorov NS, Loessner MJ, Leiman PG. Reprogramming bacteriophage host range: design principles and strategies for engineering receptor binding proteins. Curr Opin Biotechnol. 2021;68:272–81. https://doi.org/10.1016/J.COPBIO.2021.02.006.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ecdc. STEC infection annual epidemiological report for 2020 key facts, (2020)

  • Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792. https://doi.org/10.1093/NAR/GKH340.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Food and Agriculture Organization of the United Nations, W. H. O. (2018). Shiga toxin-producing Escherichia coli (STEC) and food: attribution, characterization, and monitoring: report.

  • Food Safety Authority, E, Boelaert F, Stoicescu A, Amore G, Messens W, Hempen M, Rizzi V, Antoniou S-E, Baldinelli F, Dorbek-Kolin E, Van der Stede Y, ECDC Staff Members Taina Niskanen, the, Haussig J, Kaczmarek M, Gomes Dias J, Barco L, Mancin M, Mantovani C, Sardella A, Altieri I. The European union one health 2019 Zoonoses report. EFSA J. 2021;19(2):e06406. https://doi.org/10.2903/J.EFSA.2021.6406.

    Article 

    Google Scholar
     

  • Gebhart D, Williams SR, Scholl D. Bacteriophage SP6 encodes a second tailspike protein that recognizes Salmonella enterica serogroups C2 and C3. Virology. 2017;507:263–6. https://doi.org/10.1016/J.VIROL.2017.02.025.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gil J, Paulson J, Brown M, Zahn H, Nguyen MM, Eisenberg M, Erickson S. Tailoring the host range of ackermannviridae bacteriophages through chimeric tailspike proteins. Viruses. 2023;15:286. https://doi.org/10.3390/v15020286.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gilchrist CLM, Chooi YH. Clinker and clustermap.js: automatic generation of gene cluster comparison figures. Bioinformatics. 2021;37(16):2473–5. https://doi.org/10.1093/BIOINFORMATICS/BTAB007.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Golomidova AK, Efimov AD, Kulikov EE, Kuznetsov AS, Belalov IS, Letarov AV. O antigen restricts lysogenization of non-O157 Escherichia coli strains by Stx-converting bacteriophage phi24B. Sci Rep. 2021;11(1):3035. https://doi.org/10.1038/S41598-021-82422-X.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Greenfield J, Shang X, Luo H, Zhou Y, Linden SB, Heselpoth RD, Leiman PG, Nelson DC, Herzberg O. Structure and function of bacteriophage CBA120 ORF211 (TSP2), the determinant of phage specificity towards E. coli O157:H7. Sci Rep. 2020;10(1):1–14. https://doi.org/10.1038/s41598-020-72373-0.

    Article 
    CAS 

    Google Scholar
     

  • Hobman JL, Penn CW, Pallen MJ. Laboratory strains of Escherichia coli: model citizens or deceitful delinquents growing old disgracefully? Mol Microbiol. 2007;64(4):881–5. https://doi.org/10.1111/J.1365-2958.2007.05710.X.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hunter JD. Matplotlib: a 2D graphics environment. Comput Sci Eng. 2007;9(3):90–5. https://doi.org/10.1109/MCSE.2007.55.

    Article 

    Google Scholar
     

  • Joensen KG, Tetzschner AMM, Iguchi A, Aarestrup FM, Scheutz F. Rapid and easy in silico serotyping of Escherichia coli isolates by use of whole-genome sequencing data. J Clin Microbiol. 2015;53(8):2410–26. https://doi.org/10.1128/JCM.00008-15/SUPPL_FILE/ZJM999094355SD2.XLSX.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Juhala RJ, Ford ME, Duda RL, Youlton A, Hatfull GF, Hendrix RW. Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol. 2000;299(1):27–51. https://doi.org/10.1006/jmbi.2000.3729.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A, Bridgland A, Meyer C, Kohl SAA, Ballard AJ, Cowie A, Romera-Paredes B, Nikolov S, Jain R, Adler J, Hassabis D. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596(7873):583–9. https://doi.org/10.1038/s41586-021-03819-2.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Katoh K, Standley DM. A simple method to control over-alignment in the MAFFT multiple sequence alignment program. Bioinformatics. 2016;32(13):1933–42. https://doi.org/10.1093/BIOINFORMATICS/BTW108.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kim JS, Lee MS, Kim JH. Recent updates on outbreaks of shiga toxin-producing Escherichia coli and its potential reservoirs. Front Cell Infect Microbiol. 2020. https://doi.org/10.3389/FCIMB.2020.00273.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Knirel YA, Prokhorov NS, Shashkov AS, Ovchinnikova OG, Zdorovenko EL, Liu B, Kostryukova ES, Larin AK, Golomidova AK, Letarov AV. Variations in O-antigen biosynthesis and O-acetylation associated with altered phage sensitivity in Escherichia coli 4s. J Bacteriol. 2015;197(5):905–12. https://doi.org/10.1128/JB.02398-14.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kuhnert P, Nicolet J, Frey J. Rapid and accurate identification of Escherichia coli K-12 Strains. Appl Environ Microbiol. 1995;61(11):4135–9.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Latka A, Leiman PG, Drulis-Kawa Z, Briers Y. Modeling the architecture of depolymerase-containing receptor binding proteins in klebsiella phages. Fronti Microbiol. 2019. https://doi.org/10.3389/fmicb.2019.02649.

    Article 

    Google Scholar
     

  • Latka A, Sebastien L, Dennis G, Dorien D, Barbara M, Timothy L, Zuzanna D-K, Yves B. Engineering the modular receptor-binding proteins of klebsiella phages switches their capsule serotype specificity. MBio. 2021;12(3):e00455-e521. https://doi.org/10.1128/mBio.00455-21.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Le S, He X, Tan Y, Huang G, Zhang L, Lux R, Shi W, Hu F. Mapping the tail fiber as the receptor binding protein responsible for differential host specificity of Pseudomonas aeruginosa bacteriophages PaP1 and JG004. PLoS ONE. 2013. https://doi.org/10.1371/JOURNAL.PONE.0068562.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Leiman PG, Battisti AJ, Bowman VD, Stummeyer K, Mühlenhoff M, Gerardy-Schahn R, Scholl D, Molineux IJ. The structures of bacteriophages K1E and K1–5 explain processive degradation of polysaccharide capsules and evolution of new host specificities. J Mol Biol. 2007;371(3):836–49. https://doi.org/10.1016/j.jmb.2007.05.083.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Leiman PG, Molineux IJ. Evolution of a new enzyme activity from the same motif fold. Mol Microbiol. 2008;69(2):287. https://doi.org/10.1111/J.1365-2958.2008.06241.X.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Letunic I, Bork P. Interactive tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021. https://doi.org/10.1093/nar/gkab301.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liu B, Furevi A, Perepelov AV, Guo X, Cao H, Wang Q, Reeves PR, Knirel YA, Wang L, Widmalm G. Structure and genetics of Escherichia coli O antigens. FEMS Microbiol Rev. 2020;44(6):655–83. https://doi.org/10.1093/femsre/fuz028.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mavrich TN, Hatfull GF. Bacteriophage evolution differs by host, lifestyle and genome. Nat Microbiol. 2017. https://doi.org/10.1038/nmicrobiol.2017.112.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Meier-Kolthoff JP, Göker M. VICTOR: genome-based phylogeny and classification of prokaryotic viruses. Bioinformatics. 2017;33(21):3396–404. https://doi.org/10.1093/BIOINFORMATICS/BTX440.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Müller JJ, Barbirz S, Heinle K, Freiberg A, Seckler R, Heinemann U. An intersubunit active site between supercoiled parallel β helices in the trimeric tailspike endorhamnosidase of shigella flexneri phage Sf6. Structure. 2008;16(5):766–75. https://doi.org/10.1016/J.STR.2008.01.019.

    Article 
    PubMed 

    Google Scholar
     

  • Ouyang R, Costa AR, Cassidy CK, Otwinowska A, Williams VCJ, Latka A, Stansfeld PJ, Drulis-Kawa Z, Briers Y, Pelt DM, Brouns SJJ, Briegel A. High-resolution reconstruction of a Jumbo-bacteriophage infecting capsulated bacteria using hyperbranched tail fibers. Nat Commun. 2022. https://doi.org/10.1038/s41467-022-34972-5.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pearson WR. An introduction to sequence similarity (‘Homology’) searching. Curr Protoc Bioinform. 2013. https://doi.org/10.1002/0471250953.bi0301s42.

    Article 

    Google Scholar
     

  • Peng Q, Yuan Y. Characterization of a newly isolated phage infecting pathogenic Escherichia coli and analysis of its mosaic structural genes. Sci Rep. 2018;8(1):1–10. https://doi.org/10.1038/s41598-018-26004-4.

    Article 
    CAS 

    Google Scholar
     

  • Perry LL, SanMiguel P, Minocha U, Terekhov AI, Shroyer ML, Farris LA, Bright N, Reuhs BL, Applegate BM. 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. 2009;292(2):182–6. https://doi.org/10.1111/J.1574-6968.2009.01511.X.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Plattner M, Shneider MM, Arbatsky NP, Shashkov AS, Chizhov AO, Nazarov S, Prokhorov NS, Taylor NMI, Buth SA, Gambino M, Gencay YE, Brøndsted L, Kutter EM, Knirel YA, Leiman PG. Structure and function of the branched receptor-binding complex of bacteriophage CBA120. J Mol Biol. 2019;431(19):3718–39. https://doi.org/10.1016/j.jmb.2019.07.022.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Prokhorov NS, Riccio C, Zdorovenko EL, Shneider MM, Browning C, Knirel YA, Leiman PG, Letarov AV. Function of bacteriophage G7C esterase tailspike in host cell adsorption. Mol Microbiol. 2017;105(3):385–98. https://doi.org/10.1111/MMI.13710.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Recktenwald J, Schmidt H. The nucleotide sequence of Shiga toxin (Stx) 2e-encoding phage φP27 is not related to other Stx phage genomes, but the modular genetic structure is conserved. Infect Immun. 2002;70(4):1896–908. https://doi.org/10.1128/IAI.70.4.1896-1908.2002.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sayers EW, Bolton EE, Brister JR, Canese K, Chan J, Comeau DC, Connor R, Funk K, Kelly C, Kim S, Madej T, Marchler-Bauer A, Lanczycki C, Lathrop S, Lu Z, Thibaud-Nissen F, Murphy T, Phan L, Skripchenko Y, Sherry ST. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2022;50(D1):D20. https://doi.org/10.1093/NAR/GKAB1112.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Scholl D, Cooley M, Williams SR, Gebhart D, Martin D, Bates A, Mandrell R. An engineered R-type pyocin is a highly specific and sensitive bactericidal agent for the food-borne pathogen Escherichia coli O157:H7. Antimicrob Agents Chemother. 2009;53(7):3074–80. https://doi.org/10.1128/AAC.01660-08.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Scholl D, Gebhart D, Williams SR, Bates A, Mandrell R. Genome sequence of E. coli O104:H4 leads to rapid development of a targeted antimicrobial agent against this emerging pathogen. PLoS ONE. 2012;7(3):e33637. https://doi.org/10.1371/journal.pone.0033637.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Scholl D, Merril C. The genome of bacteriophage K1F, a T7-like phage that has acquired the ability to replicate on K1 strains of Escherichia coli †. Bacteriology. 2005;187(24):8499–503. https://doi.org/10.1128/JB.187.24.8499.

    Article 
    CAS 

    Google Scholar
     

  • Schrödinger LLC (2015). The PyMOL molecular graphics system, Version~1.8

  • Schwarzer D, Buettner FFR, Browning C, Nazarov S, Rabsch W, Bethe A, Oberbeck A, Bowman VD, Stummeyer K, Muhlenhoff M, Leiman PG, Gerardy-Schahn R. A multivalent adsorption apparatus explains the broad host range of phage phi92: a comprehensive genomic and structural analysis. J Virol. 2012;86(19):10384–98. https://doi.org/10.1128/jvi.00801-12.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Silva JB, Storms Z, Sauvageau D. Host receptors for bacteriophage adsorption. FEMS Microbiol Lett. 2016;363:2. https://doi.org/10.1093/femsle/fnw002.

    Article 
    CAS 

    Google Scholar
     

  • Song W, Sun HX, Zhang C, Cheng L, Peng Y, Deng Z, Wang D, Wang Y, Hu M, Liu W, Yang H, Shen Y, Li J, You L, Xiao M. Prophage Hunter: an integrative hunting tool for active prophages. Nucleic Acids Res. 2019;47(W1):W74–80. https://doi.org/10.1093/nar/gkz380.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sørensen AN, Woudstra C, Sørensen MCH, Brøndsted L. Subtypes of tail spike proteins predicts the host range of Ackermannviridae phages. Comput Struct Biotechnol J. 2021;19:4854–67. https://doi.org/10.1016/j.csbj.2021.08.030.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Squeglia F, Maciejewska B, Łątka A, Ruggiero A, Briers Y, Drulis-Kawa Z, Berisio R. Structural and functional studies of a klebsiella phage capsule depolymerase tailspike: mechanistic insights into capsular degradation. Structure. 2020;28(6):613-624.e4. https://doi.org/10.1016/J.STR.2020.04.015.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Steinbacher S, Baxa U, Miller S, Weintraub A, Seckler R, Huber R. Crystal structure of phage P22 tailspike protein complexed with Salmonella sp. O-antigen receptors. Proc Natl Acad Sci USA. 1996;93(20):10584. https://doi.org/10.1073/PNAS.93.20.10584.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stummeyer K, Schwarzer D, Claus H, Vogel U, Gerardy-Schahn R, Mühlenhoff M. Evolution of bacteriophages infecting encapsulated bacteria: lessons from Escherichia coli K1-specific phages. Mol Microbiol. 2006;60(5):1123–35. https://doi.org/10.1111/J.1365-2958.2006.05173.X.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Taslem Mourosi J, Awe A, Guo W, Batra H, Ganesh H, Wu X, Zhu J. Understanding bacteriophage tail fiber interaction with host surface receptor: the key “Blueprint” for reprogramming phage host range. Int J Mol Sci. 2022;23(20):12146. https://doi.org/10.3390/IJMS232012146.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tétart F, Desplats C, Krisch HM. Genome plasticity in the distal tail fiber locus of the T-even bacteriophage: recombination between conserved motifs swaps adhesin specificity. J Mol Biol. 1998;282(3):543–56. https://doi.org/10.1006/JMBI.1998.2047.

    Article 
    PubMed 

    Google Scholar
     

  • Van Rossum G, Drake FL. Python 3 reference manual. CreateSpace. 2009;121:242.


    Google Scholar
     

  • Vieira M, Duarte J, Domingues R, Oliveira H, Dias O (n.d.). PhageDPO: phage depolymerase finder. https://doi.org/10.1101/2023.02.24.529883

  • Walter M, Fiedler C, Grassl R, Biebl M, Rachel R, Hermo-Parrado XL, Llamas-Saiz AL, Seckler R, Miller S, van Raaij MJ. Structure of the receptor-binding protein of bacteriophage det7: a podoviral tail spike in a myovirus. J Virol. 2008;82(5):2265–73. https://doi.org/10.1128/JVI.01641-07.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Xiang Z. Advances in homology protein structure modeling. Curr Protein Pept Sci. 2006;7(3):217–27. https://doi.org/10.2174/138920306777452312.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yehl K, Lemire S, Yang AC, Ando H, Mimee M, Torres MDT, de la Fuente-Nunez C, Lu TK. Engineering phage host-range and suppressing bacterial resistance through phage tail fiber mutagenesis. Cell. 2019;179(2):459-469.e9. https://doi.org/10.1016/j.cell.2019.09.015.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Leave a Reply