1887

Abstract

Bacteriophages are the most prevalent biological entities impacting on the ecosystem and are characterized by their extensive diversity. However, there are two aspects of phages that have remained largely unexplored: genetic flux by recombination between phage populations and characterization of specific phages in terms of the pan-genome. Here, we examined the recombination and pan-genome in prophages at both the genome and gene level. In the genome-level analysis, we applied, for the first time, chromosome painting and fineSTRUCTURE algorithms to a phage species, and showed novel trends in inter-population genetic flux. Notably, hpEastAsia is a phage population that imported a higher proportion of DNA fragments from other phages, whereas the hpSWEurope phages showed weaker signatures of inter-population recombination, suggesting genetic isolation. The gene-level analysis showed that, after parameter tuning of the prokaryote pan-genome analysis program, phages have a pan-genome consisting of 75 genes and a soft-core genome of 10 genes, which includes genes involved in the lytic and lysogenic life cycles. Quantitative analysis of recombination events of the soft-core genes showed no substantial variation in the intensity of recombination across the genes, but rather equally frequent recombination among housekeeping genes that were previously reported to be less prone to recombination. The signature of frequent recombination appears to reflect the host–phage evolutionary arms race, either by contributing to escape from bacterial immunity or by protecting the host by producing defective phages.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000282
2019-08-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/mgen/5/8/mgen000282.html?itemId=/content/journal/mgen/10.1099/mgen.0.000282&mimeType=html&fmt=ahah

References

  1. Eppinger M, Baar C, Linz B, Raddatz G, Lanz C et al. Who ate whom? adaptive Helicobacter genomic changes that accompanied a host jump from early humans to large felines. PLoS Genet 2006; 2:e120 [View Article]
    [Google Scholar]
  2. Uchiyama J, Takeuchi H, Kato S-ichiro, Takemura-Uchiyama I, Ujihara T et al. Complete genome sequences of two Helicobacter pylori bacteriophages isolated from Japanese patients. J Virol 2012; 86:11400–11401 [View Article]
    [Google Scholar]
  3. Luo C-H, Chiou P-Y, Yang C-Y, Lin N-T. Genome, integration, and transduction of a novel temperate phage of Helicobacter pylori . J Virol 2012; 86:8781–8792 [View Article]
    [Google Scholar]
  4. Vale FF, Nunes A, Oleastro M, Gomes JP, Sampaio DA et al. Genomic structure and insertion sites of Helicobacter pylori prophages from various geographical origins. Sci Rep 2017; 7:42471 [View Article]
    [Google Scholar]
  5. Lehours P, Vale FF, Bjursell MK, Melefors O, Advani R et al. Genome sequencing reveals a phage in Helicobacter pylori . mBio 2011; 2:pii: e00239–11 [View Article]
    [Google Scholar]
  6. Vale FF, Vadivelu J, Oleastro M, Breurec S, Engstrand L et al. Dormant phages of Helicobacter pylori reveal distinct populations in Europe. Sci Rep 2015; 5:14333 [View Article]
    [Google Scholar]
  7. Thorell K, Yahara K, Berthenet E, Lawson DJ, Mikhail J et al. Rapid evolution of distinct Helicobacter pylori subpopulations in the Americas. PLoS Genet 2017; 13:e1006546 [View Article]
    [Google Scholar]
  8. Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M et al. Uncovering earth's virome. Nature 2016; 536:425–430 [View Article]
    [Google Scholar]
  9. Paez-Espino D, Sharon I, Morovic W, Stahl B, Thomas BC et al. CRISPR immunity drives rapid phage genome evolution in Streptococcus thermophilus . mBio 2015; 6:e00262-15 [View Article]
    [Google Scholar]
  10. Pedulla ML, Ford ME, Houtz JM, Karthikeyan T, Wadsworth C et al. Origins of highly mosaic mycobacteriophage genomes. Cell 2003; 113:171–182 [View Article]
    [Google Scholar]
  11. Moodley Y, Linz B, Bond RP, Nieuwoudt M, Soodyall H et al. Age of the association between Helicobacter pylori and man. PLoS Pathog 2012; 8:e1002693 [View Article]
    [Google Scholar]
  12. Thorell K, Lehours P, Vale FF. Genomics of Helicobacter pylori . Helicobacter 2017; 22:hel.12409 [View Article]
    [Google Scholar]
  13. Berthenet E, Sheppard S, Vale FF. Recent "omics" advances in Helicobacter pylori . Helicobacter 2016; 21:14–18 [View Article]
    [Google Scholar]
  14. Secka O, Vale FF, Buissonnière A, Thomas JE, Mégraud F et al. Phylogeographic agreement between prophage and bacterial housekeeping genes in Helicobacter pylori strains from The Gambia. Helicobacter 2017; 22:hel.12394 [View Article]
    [Google Scholar]
  15. Vale FF, Matos APA, Carvalho P, Vítor JMB. Helicobacter pylori Phage Screening. Microsc Microanal 2008; 14:150–151 [View Article]
    [Google Scholar]
  16. Vitoriano I, Vítor JMB, Oleastro M, Roxo-Rosa M, Vale FF. Proteome variability among Helicobacter pylori isolates clustered according to genomic methylation. J Appl Microbiol 2013; 114:1817–1832 [View Article]
    [Google Scholar]
  17. Silva B, Nunes A, Vale FF, Rocha R, Gomes JP et al. The expression of Helicobacter pylori tfs plasticity zone cluster is regulated by pH and adherence, and its composition is associated with differential gastric IL-8 secretion. Helicobacter 2017; 22:hel.12390 [View Article]
    [Google Scholar]
  18. Delahay RM, Croxall NJ, Stephens AD. Phylogeographic diversity and mosaicism of the Helicobacter pylori tfs integrative and conjugative elements. Mob DNA 2018; 9:5 [View Article]
    [Google Scholar]
  19. Kyrillos A, Arora G, Murray B, Rosenwald AG. The presence of phage orthologous genes in Helicobacter pylori correlates with the presence of the virulence factors CagA and VacA . Helicobacter 2016; 21:226–233 [View Article]
    [Google Scholar]
  20. Yahara K, Furuta Y, Oshima K, Yoshida M, Azuma T et al. Chromosome painting in silico in a bacterial species reveals fine population structure. Mol Biol Evol 2013; 30:1454–1464 [View Article]
    [Google Scholar]
  21. Meier-Kolthoff JP, Uchiyama J, Yahara H, Paez-Espino D, Yahara K. Investigation of recombination-intense viral groups and their genes in the earth's virome. Sci Rep 2018; 8:11496 [View Article]
    [Google Scholar]
  22. Hu B, Xie G, Lo C-C, Starkenburg SR, Chain PSG. Pathogen comparative genomics in the next-generation sequencing era: genome alignments, pangenomics and metagenomics. Brief Funct Genomics 2011; 10:322–333 [View Article]
    [Google Scholar]
  23. Clokie MR, Millard AD, Letarov AV, Heaphy S. Phages in nature. Bacteriophage 2011; 1:31–45 [View Article]
    [Google Scholar]
  24. Pope WH, Bowman CA, Russell DA, Jacobs-Sera D, Asai DJ et al. Whole genome comparison of a large collection of mycobacteriophages reveals a continuum of phage genetic diversity. Elife 2015; 4:e06416 [View Article]
    [Google Scholar]
  25. Uchiyama J, Takeuchi H, Kato S-ichiro, Gamoh K, Takemura-Uchiyama I et al. Characterization of Helicobacter pylori bacteriophage KHP30. Appl Environ Microbiol 2013; 79:3176–3184 [View Article]
    [Google Scholar]
  26. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article]
    [Google Scholar]
  27. Song W, Sun H-X, Zhang C, Cheng L, Peng Y et al. Prophage Hunter: an integrative hunting tool for active prophages. Nucleic Acids Res 2019; 47:W74–W80 [View Article]
    [Google Scholar]
  28. Lawson DJ, Hellenthal G, Myers S, Falush D. Inference of population structure using dense haplotype data. PLoS Genet 2012; 8:e1002453 [View Article]
    [Google Scholar]
  29. Yahara K, Didelot X, Ansari MA, Sheppard SK, Falush D. Efficient inference of recombination hot regions in bacterial genomes. Mol Biol Evol 2014; 31:1593–1605 [View Article]
    [Google Scholar]
  30. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article]
    [Google Scholar]
  31. Mills R, Rozanov M, Lomsadze A, Tatusova T, Borodovsky M. Improving gene annotation of complete viral genomes. Nucleic Acids Res 2003; 31:7041–7055 [View Article]
    [Google Scholar]
  32. Hudson RR, Kaplan NL. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 1985; 111:147–164
    [Google Scholar]
  33. Cai JJ. PGEToolbox: a Matlab toolbox for population genetics and evolution. J Hered 2008; 99:438–440 [View Article]
    [Google Scholar]
  34. Librado P, Rozas J. DnaSP V5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009; 25:1451–1452 [View Article]
    [Google Scholar]
  35. Yahara K, Furuta Y, Morimoto S, Kikutake C, Komukai S et al. Genome-wide survey of codons under diversifying selection in a highly recombining bacterial species, Helicobacter pylori . DNA Res 2016; 23:135–143 [View Article]
    [Google Scholar]
  36. Goerke C, Pantucek R, Holtfreter S, Schulte B, Zink M et al. Diversity of prophages in dominant Staphylococcus aureus clonal lineages. J Bacteriol 2009; 191:3462–3468 [View Article]
    [Google Scholar]
  37. Ackermann HW, Elzanowski A, Fobo G, Stewart G. Relationships of tailed phages: a survey of protein sequence identity. Arch Virol 1995; 140:1871–1884 [View Article]
    [Google Scholar]
  38. Reuter S, Corander J, de Been M, Harris S, Cheng L et al. Directional gene flow and ecological separation in Yersinia enterocolitica . Microb Genom 2015; 1:e000030 [View Article]
    [Google Scholar]
  39. Hatfull GF, Hendrix RW. Bacteriophages and their genomes. Curr Opin Virol 2011; 1:298–303 [View Article]
    [Google Scholar]
  40. Ali A, Naz A, Soares SC, Bakhtiar M, Tiwari S et al. Pan-genome analysis of human gastric pathogen H. pylori: comparative genomics and pathogenomics approaches to identify regions associated with pathogenicity and prediction of potential core therapeutic targets. Biomed Res Int 2015; 2015:13958017 [View Article]
    [Google Scholar]
  41. Chan JZ-M, Millard AD, Mann NH, Schäfer H. Comparative genomics defines the core genome of the growing N4-like phage genus and identifies N4-like Roseophage specific genes. Front Microbiol 2014; 5:506 [View Article]
    [Google Scholar]
  42. Geng P, Tian S, Yuan Z, Hu X. Identification and genomic comparison of temperate bacteriophages derived from emetic Bacillus cereus . PLoS One 2017; 12:e0184572 [View Article]
    [Google Scholar]
  43. Petrov VM, Ratnayaka S, Nolan JM, Miller ES, Karam JD. Genomes of the T4-related bacteriophages as windows on microbial genome evolution. Virol J 2010; 7:292 [View Article]
    [Google Scholar]
  44. Ramírez-Vargas G, Goh S, Rodríguez C. The novel phages phicd5763 and phicd2955 represent two groups of big plasmidial siphoviridae phages of Clostridium difficile . Front Microbiol 2018; 9:26 [View Article]
    [Google Scholar]
  45. Uchiyama I, Albritton J, Fukuyo M, Kojima KK, Yahara K et al. A novel approach to Helicobacter pylori pan-genome analysis for identification of genomic islands. PLoS One 2016; 11:e0159419 [View Article]
    [Google Scholar]
  46. Vale FF, Mégraud F, Vítor JMB. Geographic distribution of methyltransferases of Helicobacter pylori: evidence of human host population isolation and migration. BMC Microbiol 2009; 9:193 [View Article]
    [Google Scholar]
  47. Vale FF, Vítor JMB. Genomic methylation: a tool for typing Helicobacter pylori isolates. Appl Environ Microbiol 2007; 73:4243–4249 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000282
Loading
/content/journal/mgen/10.1099/mgen.0.000282
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error