A novel vieuvirus from multidrug-resistant Acinetobacter baumannii

Abstract

Bacteriophages are considered the most abundant biological entities on earth, and they are able to modulate the populations of their bacterial hosts. Although the potential of bacteriophages has been accepted as an alternative strategy to combat multidrug-resistant pathogenic bacteria, there still exists a considerable knowledge gap regarding their genetic diversity, which hinders their use as antimicrobial agents. In this study, we undertook a genomic and phylogenetic characterization of the phage Ab11510-phi, which was isolated from a multidrug-resistant Acinetobacter baumannii strain (Ab11510). We found that Ab11510-phi has a narrow host range and belongs to a small group of transposable phages of the genus Vieuvirus that have only been reported to infect Acinetobacter bacteria. Finally, we showed that Ab11510-phi (as well as other vieuvirus phages) has a high level of mosaicism. On a broader level, we demonstrate that comparative genomics and phylogenetic analysis are necessary tools for the proper characterization of phage diversity.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. 1.

    Myers J (2016) This is how many people antibiotic resistance could kill every year by 2050 if nothing is done. World Economic Forum

  2. 2.

    O’Neill J (2014) Review on Antimicrobial Resistance Antimicrobial Resistance: Tackling a crisis for the health and wealth of nations. London: Review on Antimicrobial Resistance

  3. 3.

    Peleg AY, Seifert H, Paterson DL (2008) Acinetobacter baumannii: emergence of a successful pathogen. Clin Microbiol Rev 21:538–582

    CAS  Article  Google Scholar 

  4. 4.

    Grana-Miraglia L, Evans BA, Lopez-Jacome LE, Hernandez-Duran M, Colin-Castro CA, Volkow-Fernandez P, Cevallos MA, Franco-Cendejas R, Castillo-Ramirez S (2020) Origin of OXA-23 Variant OXA-239 from a Recently Emerged Lineage of Acinetobacter baumannii International Clone V. mSphere 5

  5. 5.

    Grana-Miraglia L, Lozano LF, Velazquez C, Volkow-Fernandez P, Perez-Oseguera A, Cevallos MA, Castillo-Ramirez S (2017) Rapid gene turnover as a significant source of genetic variation in a recently seeded population of a healthcare-associated pathogen. Front Microbiol 8

  6. 6.

    Xie R, Zhang XD, Zhao Q, Peng B, Zheng J (2018) Analysis of global prevalence of antibiotic resistance in Acinetobacter baumannii infections disclosed a faster increase in OECD countries. Emerg Microbes Infect 7:31

    PubMed  PubMed Central  Google Scholar 

  7. 7.

    Opazo-Capurro A, San Martin I, Quezada-Aguiluz M, Morales-Leon F, Dominguez-Yevenes M, Lima CA, Esposito F, Cerdeira L, Bello-Toledo H, Lincopan N, Gonzalez-Rocha G (2019) Evolutionary dynamics of carbapenem-resistant Acinetobacter baumannii circulating in Chilean hospitals. Infect Genet Evol 73:93–97

    CAS  Article  Google Scholar 

  8. 8.

    Santos-Lopez A, Marshall CW, Scribner MR, Snyder DJ, Cooper VS (2019) Evolutionary pathways to antibiotic resistance are dependent upon environmental structure and bacterial lifestyle. Elife 8

  9. 9.

    Wright MS, Iovleva A, Jacobs MR, Bonomo RA, Adams MD (2016) Genome dynamics of multidrug-resistant Acinetobacter baumannii during infection and treatment. Genome Med 8:26

    Article  Google Scholar 

  10. 10.

    Costa AR, Monteiro R, Azeredo J (2018) Genomic analysis of Acinetobacter baumannii prophages reveals remarkable diversity and suggests profound impact on bacterial virulence and fitness. Sci Rep 8:15346

    Article  Google Scholar 

  11. 11.

    Lopez-Leal G, Santamaria RI, Cevallos MA, Gonzalez V, Castillo-Ramirez S (2020) Prophages encode antibiotic resistance genes in Acinetobacter baumannii. Microb Drug Resist

  12. 12.

    Lopez-Leal G, Zuniga-Moya JC, Castro-Jaimes S, Grana-Miraglia L, Perez-Oseguera A, Reyes-Garcia HS, Gough-Coto SD, Pavon-Madrid R, Bejarano SA, Ferrera A, Castillo-Ramirez S, Cevallos MA (2019) Unexplored genetic diversity of multidrug- and extremely drug-resistant Acinetobacter baumannii Isolates from tertiary hospitals in Honduras. Microb Drug Resist 25:690–695

    CAS  Article  Google Scholar 

  13. 13.

    Kropinski AM, Mazzocco A, Waddell TE, Lingohr E, Johnson RP (2009) Enumeration of bacteriophages by double agar overlay plaque assay. Methods Mol Biol 501:69–76

    CAS  Article  Google Scholar 

  14. 14.

    Santamaria RI, Bustos P, Sepulveda-Robles O, Lozano L, Rodriguez C, Fernandez JL, Juarez S, Kameyama L, Guarneros G, Davila G, Gonzalez V (2014) Narrow-host-range bacteriophages that infect Rhizobium etli associate with distinct genomic types. Appl Environ Microbiol 80:446–454

    CAS  Article  Google Scholar 

  15. 15.

    Vincze T, Posfai J, Roberts RJ (2003) NEBcutter: a program to cleave DNA with restriction enzymes. Nucleic Acids Res 31:3688–3691

    CAS  Article  Google Scholar 

  16. 16.

    Garneau JR, Depardieu F, Fortier LC, Bikard D, Monot M (2017) PhageTerm: a tool for fast and accurate determination of phage termini and packaging mechanism using next-generation sequencing data. Sci Rep 7:8292

    Article  Google Scholar 

  17. 17.

    Grissa I, Vergnaud G, Pourcel C (2007) CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35:W52-57

    Article  Google Scholar 

  18. 18.

    Shen W, Le S, Li Y, Hu F (2016) SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS ONE 11:e0163962

    Article  Google Scholar 

  19. 19.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  Article  Google Scholar 

  20. 20.

    Castro CJ, Marine RL, Ramos E, Ng TFF (2020) The effect of variant interference on de novo assembly for viral deep sequencing. BMC Genomics 21:421

    CAS  Article  Google Scholar 

  21. 21.

    Sutton TDS, Clooney AG, Ryan FJ, Ross RP, Hill C (2019) Choice of assembly software has a critical impact on virome characterisation. Microbiome 7:12

    Article  Google Scholar 

  22. 22.

    Coil D, Jospin G, Darling AE (2015) A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics 31:587–589

    CAS  Article  Google Scholar 

  23. 23.

    Arndt D, Grant JR, Marcu A, Sajed T, Pon A, Liang Y, Wishart DS (2016) PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44:W16-21

    CAS  Article  Google Scholar 

  24. 24.

    Roux S, Enault F, Hurwitz BL, Sullivan MB (2015) VirSorter: mining viral signal from microbial genomic data. PeerJ 3:e985

    Article  Google Scholar 

  25. 25.

    Antipov D, Raiko M, Lapidus A, Pevzner PA (2020) Metaviral SPAdes: assembly of viruses from metagenomic data. Bioinformatics 36:4126–4129

    CAS  Article  Google Scholar 

  26. 26.

    Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069

    CAS  Article  Google Scholar 

  27. 27.

    Potter SC, Luciani A, Eddy SR, Park Y, Lopez R, Finn RD (2018) HMMER web server: 2018 update. Nucleic Acids Res 46:W200–W204

    CAS  Article  Google Scholar 

  28. 28.

    Kristensen DM, Waller AS, Yamada T, Bork P, Mushegian AR, Koonin EV (2013) Orthologous gene clusters and taxon signature genes for viruses of prokaryotes. J Bacteriol 195:941–950

    CAS  Article  Google Scholar 

  29. 29.

    Lowe TM, Chan PP (2016) tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 44:W54-57

    CAS  Article  Google Scholar 

  30. 30.

    Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M, Edalatmand A, Huynh W, Nguyen AV, Cheng AA, Liu S, Min SY, Miroshnichenko A, Tran HK, Werfalli RE, Nasir JA, Oloni M, Speicher DJ, Florescu A, Singh B, Faltyn M, Hernandez-Koutoucheva A, Sharma AN, Bordeleau E, Pawlowski AC, Zubyk HL, Dooley D, Griffiths E, Maguire F, Winsor GL, Beiko RG, Brinkman FSL, Hsiao WWL, Domselaar GV, McArthur AG (2020) CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 48:D517–D525

    CAS  Article  Google Scholar 

  31. 31.

    Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MT, Fookes M, Falush D, Keane JA, Parkhill J (2015) Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31:3691–3693

    CAS  Article  Google Scholar 

  32. 32.

    Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5:113

    Article  Google Scholar 

  33. 33.

    Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    CAS  Article  Google Scholar 

  34. 34.

    Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105

    CAS  Article  Google Scholar 

  35. 35.

    Bruen TC, Philippe H, Bryant D (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics 172:2665–2681

    CAS  Article  Google Scholar 

  36. 36.

    Marcais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL, Zimin A (2018) MUMmer4: a fast and versatile genome alignment system. PLoS Comput Biol 14:e1005944

    Article  Google Scholar 

  37. 37.

    Bondy-Denomy J, Qian J, Westra ER, Buckling A, Guttman DS, Davidson AR, Maxwell KL (2016) Prophages mediate defense against phage infection through diverse mechanisms. ISME J 10:2854–2866

    Article  Google Scholar 

  38. 38.

    Turner D, Ackermann HW, Kropinski AM, Lavigne R, Sutton JM, Reynolds DM (2017) Comparative analysis of 37 acinetobacter bacteriophages. Viruses 10

  39. 39.

    Turner D, Wand ME, Sutton JM, Centron D, Kropinski AM, Reynolds DM (2016) Genome sequence of vB_AbaS_TRS1, a viable prophage isolated from Acinetobacter baumannii Strain A118. Genome Announc 4

  40. 40.

    Campbell A (2003) Prophage insertion sites. Res Microbiol 154:277–282

    CAS  Article  Google Scholar 

  41. 41.

    Xu J, Li X, Kang G, Bai L, Wang P, Huang H (2020) Isolation and Characterization of AbTJ, an Acinetobacter baumannii Phage, and Functional Identification of Its Receptor-Binding Modules. Viruses 12

  42. 42.

    Tisza MJ, Pastrana DV, Welch NL, Stewart B, Peretti A, Starrett GJ, Pang Y-YS, Krishnamurthy SR, Pesavento PA, McDermott DH, Murphy PM, Whited JL, Miller B, Brenchley J, Rosshart SP, Rehermann B, Doorbar J, Ta'ala BA, Pletnikova O, Troncoso JC, Resnick SM, Bolduc B, Sullivan MB, Varsani A, Segall AM, Buck CB (2020) Discovery of several thousand highly diverse circular DNA viruses. eLife 9:e51971

  43. 43.

    Meier-Kolthoff JP, Goker M (2017) VICTOR: genome-based phylogeny and classification of prokaryotic viruses. Bioinformatics 33:3396–3404

    CAS  Article  Google Scholar 

  44. 44.

    Jeon J, Kim JW, Yong D, Lee K, Chong Y (2012) Complete genome sequence of the podoviral bacteriophage YMC/09/02/B1251 ABA BP, which causes the lysis of an OXA-23-producing carbapenem-resistant Acinetobacter baumannii isolate from a septic patient. J Virol 86:12437–12438

    CAS  Article  Google Scholar 

  45. 45.

    Jeon J, D’Souza R, Pinto N, Ryu CM, Park JH, Yong D, Lee K (2015) Complete genome sequence of the siphoviral bacteriophage Betavarphi-R3177, which lyses an OXA-66-producing carbapenem-resistant Acinetobacter baumannii isolate. Arch Virol 160:3157–3160

    CAS  Article  Google Scholar 

  46. 46.

    Chan JZ, Millard AD, Mann NH, Schafer H (2014) Comparative genomics defines the core genome of the growing N4-like phage genus and identifies N4-like Roseophage specific genes. Front Microbiol 5:506

    PubMed  PubMed Central  Google Scholar 

  47. 47.

    Sazinas P, Redgwell T, Rihtman B, Grigonyte A, Michniewski S, Scanlan DJ, Hobman J, Millard A (2018) Comparative genomics of bacteriophage of the genus seuratvirus. Genome Biol Evol 10:72–76

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work was partially supported by “Programa de Apoyo a Proyectos de Investigación e Inovación Tecnológica PAPIIT’’ (grant no. IN206019) and CONACyT Ciencia Básica 2016 (grant no. 284276). G.L.L. received a postdoctoral fellowship (2019-000012-01EXTV-00488) from CONACyT. We are thankful to Ismael Hernández-González for discussions on the assembly of the phage genome sequence. We also thank Victor González for his helpful comments, Adriana Carolina Hernández-Morales for her recommendations on the phage isolation protocol, and Alfredo Hernández-Alvarez, Víctor Del Moral-Chávez, and Juan Manuel Hurtado-Ramírez for technical support. GLL thanks Juan Sebastian Andrade Martinez, Laura Carolina Camelo Valera, Luis Alberto Chica Cárdenas, Laura Milena Forero Junco, Ruth Hernandez Reyes, Leonardo Moreno Gallego, Guillermo Rangel, and Laura Avellaneda Franco, members of the viromics group within the Max Planck Tandem Group in Computational Biology, for the general discussion of the results presented in this manuscript. We thank the reviewers for their helpful input, as our article was significantly improved by their comments. We also thank reviewer 1 for his/her observation about the circular permutation of the genome of Ab11510-phi.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Gamaliel López-Leal.

Additional information

Publisher's Note

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

Handling Editor: Johannes Wittmann.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 1408 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

López-Leal, G., Reyes-Muñoz, A., Santamaria, R.I. et al. A novel vieuvirus from multidrug-resistant Acinetobacter baumannii. Arch Virol 166, 1401–1408 (2021). https://doi.org/10.1007/s00705-021-05010-4

Download citation