Skip to main content
SpringerLink
Log in

The saclayvirus Aci01-1 very long and complex fiber and its receptor at the Acinetobacter baumannii surface

  • Brief Report
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

The Acinetobacter baumannii bacteriophage Aci01-1, which belongs to the genus Saclayvirus of the order Caudoviricetes, has an icosahedral head and a contractile rigid tail. We report that Aci01-1 has, attached to the tail conical tip, a remarkable 146-nm-long flexible fiber with seven beads and a terminal knot. Its putative gene coding for a 241.36-kDa tail fiber protein is homologous to genes in Aci01-1-related and unrelated phages. Analysis of its 3D structure using AlphaFold provides a structural model for the fiber observed by electron microscopy. We also identified a putative receptor of the phage on the bacterial capsule that is hypothesized to interact with the Aci01-1 long fiber.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Data availability

The data presented in this study are available in Supplementary Figures S2–S3. The nucleotide sequences reported in this work have been deposited in the GenBank database under accession numbers NC_048074 and Genbank ID NC_048080, for Aci01-1 and Aci05 respectively. The raw reads archives of phages Aci01-1 (ERR2822810) and phage Aci05 (ERR2822812) have been deposited in the European Nucleotide Archive (ENA) under study PRJEB28456. The read archives of strain Ab09 (ERR10922808) and of the phage-resistant variants (ERR10922809 and ERR10922810) have been deposited under study PRJEB60153.

References

  1. Asif M, Alvi IA, Rehman SU (2018) Insight into Acinetobacter baumannii: pathogenesis, global resistance, mechanisms of resistance, treatment options, and alternative modalities. Infect Drug Resist 11:1249–1260. https://doi.org/10.2147/IDR.S166750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M, Monnet DL et al (2018) Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis 18:318–327. https://doi.org/10.1016/S1473-3099(17)30753-3

    Article  PubMed  Google Scholar 

  3. Kortright KE, Chan BK, Koff JL, Turner PE (2019) Phage therapy: A renewed approach to combat antibiotic-resistant bacteria. Cell Host Microbe 25:219–232. https://doi.org/10.1016/j.chom.2019.01.014

    Article  CAS  PubMed  Google Scholar 

  4. Rai S, Kumar A (2022) Bacteriophage therapeutics to confront multidrug-resistant Acinetobacter baumannii—a global health menace. Environ Microbiol Rep 14:347–364. https://doi.org/10.1111/1758-2229.12988

    Article  CAS  PubMed  Google Scholar 

  5. Essoh C, Vernadet JP, Vergnaud G, Coulibaly A, Kakou-N’Douba A, N’Guetta AS et al (2019) Complete genome sequences of five Acinetobacter baumannii phages from Abidjan Cote d’Ivoire. Microbiol Resour Announc. https://doi.org/10.1128/MRA.01358-18

    Article  PubMed  PubMed Central  Google Scholar 

  6. Hauck Y, Soler C, Jault P, Merens A, Gerome P, Nab CM et al (2012) Diversity of Acinetobacter baumannii in Four French Military Hospitals, as Assessed by Multiple Locus Variable Number of Tandem Repeats Analysis. PLoS One 7:e44597. https://doi.org/10.1371/journal.pone.0044597

  7. Jakutyte L, Baptista C, Sao-Jose C, Daugelavicius R, Carballido-Lopez R, Tavares P (2011) Bacteriophage infection in rod-shaped gram-positive bacteria: evidence for a preferential polar route for phage SPP1 entry in Bacillus subtilis. J Bacteriol 193:4893–4903. https://doi.org/10.1128/JB.05104-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Steven AC, Trus BL, Maizel JV, Unser M, Parry DA, Wall JS et al (1988) Molecular substructure of a viral receptor-recognition protein. The gp17 tail-fiber of bacteriophage T7. J Mol Biol 200:351–365

    Article  CAS  PubMed  Google Scholar 

  9. Wang Y, Xue H, Pourcel C, Du Y, Gautheret D (2021) 2-kupl: mapping-free variant detection from DNA-seq data of matched samples. BMC Bioinformatics 22:304. https://doi.org/10.1186/s12859-021-04185-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Mirdita M, Schutze K, Moriwaki Y, Heo L, Ovchinnikov S, Steinegger M (2022) ColabFold: making protein folding accessible to all. Nat Methods 19:679–682. https://doi.org/10.1038/s41592-022-01488-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Mirdita M, von den Driesch L, Galiez C, Martin MJ, Soding J, Steinegger M (2017) Uniclust databases of clustered and deeply annotated protein sequences and alignments. Nucleic Acids Res 45:D170–D176. https://doi.org/10.1093/nar/gkw1081

    Article  CAS  PubMed  Google Scholar 

  12. Senior AW, Evans R, Jumper J, Kirkpatrick J, Sifre L, Green T et al (2019) Protein structure prediction using multiple deep neural networks in the 13th Critical Assessment of Protein Structure Prediction (CASP13). Proteins 87:1141–1148. https://doi.org/10.1002/prot.25834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O et al (2021) Highly accurate protein structure prediction with AlphaFold. Nature 596:583–589. https://doi.org/10.1038/s41586-021-03819-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Varadi M, Anyango S, Deshpande M, Nair S, Natassia C, Yordanova G et al (2022) AlphaFold Protein Structure Database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res 50:D439–D444. https://doi.org/10.1093/nar/gkab1061

    Article  CAS  PubMed  Google Scholar 

  15. Evans R, O’Neill M, Pritzel A, Antropova N, Senior A, Green T et al (2022) Protein complex prediction with AlphaFold-Multimer. bioRxiv. https://doi.org/10.1101/2021.10.04.463034

    Article  PubMed  PubMed Central  Google Scholar 

  16. Katsura I (1981) Structure and function of the major tail protein of bacteriophage lambda. Mutants having small major tail protein molecules in their virion. J Mol Biol 146:493–512. https://doi.org/10.1016/0022-2836(81)90044-9

    Article  CAS  PubMed  Google Scholar 

  17. Zivanovic Y, Confalonieri F, Ponchon L, Lurz R, Chami M, Flayhan A et al (2014) Insights into bacteriophage T5 structure from analysis of its morphogenesis genes and protein components. J Virol 88:1162–1174. https://doi.org/10.1128/JVI.02262-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Vinga I, Baptista C, Auzat I, Petipas I, Lurz R, Tavares P et al (2012) Role of bacteriophage SPP1 tail spike protein gp21 on host cell receptor binding and trigger of phage DNA ejection. Mol Microbiol 83:289–303. https://doi.org/10.1111/j.1365-2958.2011.07931.x

    Article  CAS  PubMed  Google Scholar 

  19. Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N et al (2019) The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res 47:W636–W641. https://doi.org/10.1093/nar/gkz268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Gruber M, Soding J, Lupas AN (2005) REPPER—repeats and their periodicities in fibrous proteins. Nucleic Acids Res 33:W239-243. https://doi.org/10.1093/nar/gki405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858. https://doi.org/10.1038/nprot.2015.053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Holm L (2022) Dali server: structural unification of protein families. Nucleic Acids Res 50:W210-215. https://doi.org/10.1093/nar/gkac387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Schulz EC, Dickmanns A, Urlaub H, Schmitt A, Muhlenhoff M, Stummeyer K et al (2010) Crystal structure of an intramolecular chaperone mediating triple-beta-helix folding. Nat Struct Mol Biol 17:210–215. https://doi.org/10.1038/nsmb.1746

    Article  CAS  PubMed  Google Scholar 

  24. Lee YC, Huang YT, Tan CK, Kuo YW, Liao CH, Lee PI et al (2011) Acinetobacter baumannii and Acinetobacter genospecies 13TU and 3 bacteraemia: comparison of clinical features, prognostic factors and outcomes. J Antimicrob Chemother 66:1839–1846. https://doi.org/10.1093/jac/dkr200

    Article  CAS  PubMed  Google Scholar 

  25. Casjens SR, Gilcrease EB, Huang WM, Bunny KL, Pedulla ML, Ford ME et al (2004) The pKO2 linear plasmid prophage of Klebsiella oxytoca. J Bacteriol 186:1818–1832. https://doi.org/10.1128/JB.186.6.1818-1832.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Berkane E, Orlik F, Stegmeier JF, Charbit A, Winterhalter M, Benz R (2006) Interaction of bacteriophage lambda with its cell surface receptor: an in vitro study of binding of the viral tail protein gpJ to LamB (Maltoporin). Biochemistry 45:2708–2720. https://doi.org/10.1021/bi051800v

    Article  CAS  PubMed  Google Scholar 

  27. Goulet A, Lai-Kee-Him J, Veesler D, Auzat I, Robin G, Shepherd DA et al (2011) The opening of the SPP1 bacteriophage tail, a prevalent mechanism in Gram-positive-infecting siphophages. J Biol Chem 286:25397–25405. https://doi.org/10.1074/jbc.M111.243360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hua H, Liang Q, Fang L, He J, Wang M, Hong W et al (2020) Bautype: capsule and lipopolysaccharide serotype prediction for Acinetobacter baumannii Genome. Infect Microbes Dis 2:18–25

    Article  CAS  Google Scholar 

  29. Latino L, Midoux C, Hauck Y, Vergnaud G, Pourcel C (2016) Pseudolysogeny and sequential mutations build multiresistance to virulent bacteriophages in Pseudomonas aeruginosa. Microbiology 162:748–763. https://doi.org/10.1099/mic.0.000263

    Article  CAS  PubMed  Google Scholar 

  30. Latino L, Midoux C, Vergnaud G, Pourcel C (2019) Investigation of Pseudomonas aeruginosa strain PcyII-10 variants resisting infection by N4-like phage Ab09 in search for genes involved in phage adsorption. PloS one 14:e0215456. https://doi.org/10.1371/journal.pone.0215456

  31. Dunstan RA, Pickard D, Dougan S, Goulding D, Cormie C, Hardy J et al (2019) The flagellotropic bacteriophage YSD1 targets Salmonella Typhi with a Chi-like protein tail fibre. Mol Microbiol 112:1831–1846. https://doi.org/10.1111/mmi.14396

    Article  CAS  PubMed  Google Scholar 

  32. Tomaras AP, Dorsey CW, Edelmann RE, Actis LA (2003) Attachment to and biofilm formation on abiotic surfaces by Acinetobacter baumannii: involvement of a novel chaperone-usher pili assembly system. Microbiology 149:3473–3484. https://doi.org/10.1099/mic.0.26541-0

    Article  CAS  PubMed  Google Scholar 

  33. de Breij A, Gaddy J, van der Meer J, Koning R, Koster A, van den Broek P et al (2009) CsuA/BABCDE-dependent pili are not involved in the adherence of Acinetobacter baumannii ATCC19606(T) to human airway epithelial cells and their inflammatory response. Res Microbiol 160:213–218. https://doi.org/10.1016/j.resmic.2009.01.002

    Article  CAS  PubMed  Google Scholar 

  34. Geisinger E, Huo W, Hernandez-Bird J, Isberg RR (2019) Acinetobacter baumannii: envelope determinants that control drug resistance, virulence, and surface variability. Annu Rev Microbiol 73:481–506. https://doi.org/10.1146/annurev-micro-020518-115714

    Article  CAS  PubMed  Google Scholar 

  35. Gordillo Altamirano F, Forsyth JH, Patwa R, Kostoulias X, Trim M, Subedi D et al (2021) Bacteriophage-resistant Acinetobacter baumannii are resensitized to antimicrobials. Nat Microbiol 6:157–161. https://doi.org/10.1038/s41564-020-00830-7

    Article  CAS  PubMed  Google Scholar 

  36. Liu M, Hernandez-Morales A, Clark J, Le T, Biswas B, Bishop-Lilly KA et al (2022) Comparative genomics of Acinetobacter baumannii and therapeutic bacteriophages from a patient undergoing phage therapy. Nat Commun 13:3776. https://doi.org/10.1038/s41467-022-31455-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Oliveira H, Costa AR, Ferreira A, Konstantinides N, Santos SB, Boon M et al (2019) Functional analysis and antivirulence properties of a new depolymerase from a myovirus that infects Acinetobacter baumannii capsule K45. J Virol 93:1. https://doi.org/10.1128/JVI.01163-18

    Article  Google Scholar 

  38. Glowacka-Rutkowska A, Gozdek A, Empel J, Gawor J, Zuchniewicz K, Kozinska A et al (2018) The ability of lytic staphylococcal podovirus vB_SauP_phiAGO1.3 to coexist in equilibrium with its host facilitates the selection of host mutants of attenuated virulence but does not preclude the phage antistaphylococcal activity in a nematode infection model. Front Microbiol 9:3227. https://doi.org/10.3389/fmicb.2018.03227

  39. Shkoporov AN, Khokhlova EV, Stephens N, Hueston C, Seymour S, Hryckowian AJ et al (2021) Long-term persistence of crAss-like phage crAss001 is associated with phase variation in Bacteroides intestinalis. BMC Biol 19:163. https://doi.org/10.1186/s12915-021-01084-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ripp S, Miller RV (1997) The role of pseudolysogeny in bacteriophage-host interactions in a natural freshwater environment. Virology 143:2065–2070. https://doi.org/10.1099/00221287-143-6-2065

    Article  CAS  Google Scholar 

  41. Bryan D, El-Shibiny A, Hobbs Z, Porter J, Kutter EM (2016) Bacteriophage T4 Infection of Stationary Phase E. coli: Life after Log from a Phage Perspective. Front Microbiol 7:1391. https://doi.org/10.3389/fmicb.2016.01391

  42. Mantynen S, Laanto E, Oksanen HM, Poranen MM, Diaz-Munoz SL (2021) Black box of phage-bacterium interactions: exploring alternative phage infection strategies. Open Biol 11:210188. https://doi.org/10.1098/rsob.210188

  43. Markwitz P, Lood C, Olszak T, van Noort V, Lavigne R, Drulis-Kawa Z (2022) Genome-driven elucidation of phage-host interplay and impact of phage resistance evolution on bacterial fitness. ISME J 16:533–542. https://doi.org/10.1038/s41396-021-01096-5

    Article  CAS  PubMed  Google Scholar 

  44. Heger A, Holm L (2000) Rapid automatic detection and alignment of repeats in protein sequences. Proteins 41:224–237. https://doi.org/10.1002/1097-0134(20001101)41:2%3c224::aid-prot70%3e3.0.co;2-z

    Article  CAS  PubMed  Google Scholar 

  45. Jones DT (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292:195–202. https://doi.org/10.1006/jmbi.1999.3091

    Article  CAS  PubMed  Google Scholar 

  46. Gruber M, Soding J, Lupas AN (2006) Comparative analysis of coiled-coil prediction methods. J Struct Biol 155:140–145. https://doi.org/10.1016/j.jsb.2006.03.009

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Gilles Vergnaud for help with bioinformatics analysis. This work benefited from the CryoEM platform of I2BC, supported by the French Infrastructure for Integrated Structural Biology (FRISBI) (ANR-10-INSB-05-05). We thank the BIOI2 platform for making the ColabFold pipeline easily accessible to the I2BC.

Funding

This article was funded by Agence Nationale de la Recherche (ANR-10-INSB-05-05).

Author information

Authors and Affiliations

  1. CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay, 91198, Gif-sur-Yvette, France

    Christine Pourcel, Malika Ouldali & Paulo Tavares

  2. Department of Biochemistry-Genetic, School of Biological Sciences, Université Peleforo Gon Coulibaly, Korhogo, Côte d’Ivoire

    Christiane Essoh

Authors
  1. Christine Pourcel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Malika Ouldali
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paulo Tavares
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christiane Essoh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by CP, MO, PT, and CE. The first draft of the manuscript was written by CP, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Christine Pourcel.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Additional information

Handling Editor: Johannes Wittmann .

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 313 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pourcel, C., Ouldali, M., Tavares, P. et al. The saclayvirus Aci01-1 very long and complex fiber and its receptor at the Acinetobacter baumannii surface. Arch Virol 168, 187 (2023). https://doi.org/10.1007/s00705-023-05817-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00705-023-05817-3

Search

Navigation