The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.
Phage tailspike modularity and horizontal gene transfer reveals specificity towards E. coli O-antigen serogroups
Open accessPublished version of a preprint
Abstract
Background: The interaction between bacteriophages and their hosts is intricate and highly specific. Receptor-binding proteins (RBPs) of phages such as tail fibers and tailspikes initiate the infection process. These RBPs bind to diverse outer membrane structures, including the O-antigen, which is a serogroup-specific sugar-based component of the outer lipopolysaccharide layer of Gram-negative bacteria. Among the most virulent Escherichia coli strains is the Shiga toxin-producing E. coli (STEC) pathotype dominated by a subset of O-antigen serogroups. Methods: Extensive phylogenetic and structural analyses were used to identify and validate specificity correlations between phage RBP subtypes and STEC O-antigen serogroups, relying on the principle of horizontal gene transfer as main driver for RBP evolution. Results: We identified O-antigen specific RBP subtypes for seven out of nine most prevalent STEC serogroups (O26, O45, O103, O104, O111, O145 and O157) and seven additional E. coli serogroups (O2, O8, O16, O18, 4s/O22, O77 and O78). Eight phage genera ( Gamaleya-, Justusliebig-, Kaguna-, Kayfuna-, Kutter-, Lederberg-, Nouzilly- and Uetakeviruses ) emerged for their high proportion of serogroup-specific RBPs. Additionally, we reveal sequence motifs in the RBP region, potentially serving as recombination hotspots between lytic phages. Conclusion: The results contribute to a better understanding of mosaicism of phage RBPs, but also demonstrate a method to identify and validate new RBP subtypes for current and future emerging serogroups.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764
Flagged first, then by citations
Research works printed but not linked: 61
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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.
- 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. · DOI
- 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. · DOI · Paper page
- 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. · DOI
- 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. · DOI · Paper page
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- Hunter JD. Matplotlib: a 2D graphics environment. Comput Sci Eng. 2007;9(3):90–5. https://doi.org/10.1109/MCSE.2007.55. · DOI · Paper page
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- Kuhnert P, Nicolet J, Frey J. Rapid and accurate identification of Escherichia coli K-12 Strains. Appl Environ Microbiol. 1995;61(11):4135–9. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- Mavrich TN, Hatfull GF. Bacteriophage evolution differs by host, lifestyle and genome. Nat Microbiol. 2017. https://doi.org/10.1038/nmicrobiol.2017.112. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI · Paper page
- Pearson WR. An introduction to sequence similarity (‘Homology’) searching. Curr Protoc Bioinform. 2013. https://doi.org/10.1002/0471250953.bi0301s42. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI · Paper page
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- Silva JB, Storms Z, Sauvageau D. Host receptors for bacteriophage adsorption. FEMS Microbiol Lett. 2016;363:2. https://doi.org/10.1093/femsle/fnw002. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- 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. · DOI
- Van Rossum G, Drake FL. Python 3 reference manual. CreateSpace. 2009;121:242.
- 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 · DOI
- 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. · DOI
- Xiang Z. Advances in homology protein structure modeling. Curr Protein Pept Sci. 2006;7(3):217–27. https://doi.org/10.2174/138920306777452312. · DOI
- 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. · DOI
Cited by
Sorted by citations
Gaborieau, B., Vaysset, H., Tesson, F., Charachon, I., Dib, N., Bernier, J., Dequidt, T., Georjon, H., Clermont, O., Hersen, P., et al. (2024) · Nature Microbiology · doi:10.1038/s41564-024-01832-5 · Cited by 141
Metadata
- Authors
- Pas, C., Latka, A., Fieseler, L., & Briers, Y.
- Affiliations
- Ghent University (BE)
- ZHAW Zurich University of Applied Sciences (CH)
- Corresponding author
- Briers, Yves
- Venue
- Virology Journal
- Published
- 2023-08-07
- Volume
- 20
- Issue
- 1
- Pages
- 174-174
- ISSN
- 1743-422X (ISSN-L)
- PMC
- PMC10408124
- OpenAlex
- W4385636902
- Cited by
- 52
- References
- 1
- Citations by year
- 2026: 22 · 2025: 13 · 2024: 15 · 2023: 2
- FWCI
- 8.41
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Virology Journal (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Fonds Wetenschappelijk Onderzoek (1S79422N, 1240021N)
- Topics
- Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
- Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- receptor binding protein, horizontal gene transfer, Shiga toxin-producing Escherichia coli, phage-host specificity, phage tail fiber, recombination hotspots, phage evolution, lytic phages
- MeSH terms
- Escherichia coli Infections, Feces, Humans, Phylogeny, O Antigens, Gene Transfer, Horizontal, Shiga-Toxigenic Escherichia coli, Serogroup
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review