1887

Abstract

In Bacteria, a working consensus of species circumscription may have been reached and one of the most prominent criteria is high average nucleotide identity (ANI). ANI in effect groups strains that may recombine more or less frequently, depending on their biology, as opposed to rare interspecies gene transfer. For bacteriophages, which show various lifestyles, the nature of the fundamental natural unit, if it exists in a biological sense, is not well understood and defined. The approaches based on dot-plots are useful to group similar bacteriophages, yet are not quantitative and use arbitrarily set cut-offs. Here, we focus on lytic Myoviridae and test the ANI metric for group delineation. We show that ANI-based groups are in agreement with the International Committee on Taxonomy of Viruses (ICTV) classification and already established dot-plot groups, which are occasionally further refined owing to higher resolution of ANI analysis. Furthermore, these groups are separated among themselves by clear ANI discontinuities. Their members readily exchange core genes with each other while they do not with bacteriophages of other ANI groups, not even with the most similar. Thus, ANI-delineated groups may represent the natural units in lytic Myoviridae evolution with features that resemble those encountered in bacterial species.

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2018-03-27
2019-10-22
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References

  1. Rosselló-Móra R, Amann R. Past and future species definitions for Bacteria and Archaea. Syst Appl Microbiol 2015;38:209–216 [CrossRef][PubMed]
    [Google Scholar]
  2. Konstantinidis KT, Ramette A, Tiedje JM. The bacterial species definition in the genomic era. Philos Trans R Soc Lond B Biol Sci 2006;361:1929–1940 [CrossRef][PubMed]
    [Google Scholar]
  3. Konstantinidis KT, Rosselló-Móra R. Classifying the uncultivated microbial majority: a place for metagenomic data in the Candidatus proposal. Syst Appl Microbiol 2015;38:223–230 [CrossRef][PubMed]
    [Google Scholar]
  4. Caro-Quintero A, Konstantinidis KT. Bacterial species may exist, metagenomics reveal. Environ Microbiol 2012;14:347–355 [CrossRef][PubMed]
    [Google Scholar]
  5. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009;106:19126–19131 [CrossRef][PubMed]
    [Google Scholar]
  6. Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP. The bacterial species challenge: making sense of genetic and ecological diversity. Science 2009;323:741–746 [CrossRef][PubMed]
    [Google Scholar]
  7. Caro-Quintero A, Deng J, Auchtung J, Brettar I, Höfle MG et al. Unprecedented levels of horizontal gene transfer among spatially co-occurring Shewanella bacteria from the Baltic Sea. Isme J 2011;5:131–140 [CrossRef][PubMed]
    [Google Scholar]
  8. Shapiro BJ. How clonal are bacteria over time?. Curr Opin Microbiol 2016;31:116–123 [CrossRef][PubMed]
    [Google Scholar]
  9. Vos M, Didelot X. A comparison of homologous recombination rates in bacteria and archaea. Isme J 2009;3:199–208 [CrossRef][PubMed]
    [Google Scholar]
  10. Fraser C, Hanage WP, Spratt BG. Recombination and the nature of bacterial speciation. Science 2007;315:476–480 [CrossRef][PubMed]
    [Google Scholar]
  11. Ackermann HW. 5500 Phages examined in the electron microscope. Arch Virol 2007;152:227–243 [CrossRef][PubMed]
    [Google Scholar]
  12. Lopes A, Tavares P, Petit MA, Guérois R, Zinn-Justin S. Automated classification of tailed bacteriophages according to their neck organization. BMC Genomics 2014;15:1027 [CrossRef][PubMed]
    [Google Scholar]
  13. Adriaenssens EM, Edwards R, Nash JH, Mahadevan P, Seto D et al. Integration of genomic and proteomic analyses in the classification of the Siphoviridae family. Virology 2015;477:144–154 [CrossRef][PubMed]
    [Google Scholar]
  14. Lavigne R, Seto D, Mahadevan P, Ackermann HW, Kropinski AM. Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools. Res Microbiol 2008;159:406–414 [CrossRef][PubMed]
    [Google Scholar]
  15. Lavigne R, Darius P, Summer EJ, Seto D, Mahadevan P et al. Classification of Myoviridae bacteriophages using protein sequence similarity. BMC Microbiol 2009;9:224 [CrossRef][PubMed]
    [Google Scholar]
  16. Grose JH, Casjens SR. Understanding the enormous diversity of bacteriophages: the tailed phages that infect the bacterial family Enterobacteriaceae. Virology 2014;468:421–443 [CrossRef][PubMed]
    [Google Scholar]
  17. Hatfull GF, Jacobs-Sera D, Lawrence JG, Pope WH, Russell DA et al. Comparative genomic analysis of 60 Mycobacteriophage genomes: genome clustering, gene acquisition, and gene size. J Mol Biol 2010;397:119–143 [CrossRef][PubMed]
    [Google Scholar]
  18. Kwan T, Liu J, Dubow M, Gros P, Pelletier J. The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc Natl Acad Sci USA 2005;102:5174–5179 [CrossRef][PubMed]
    [Google Scholar]
  19. Pope WH, Mavrich TN, Garlena RA, Guerrero-Bustamante CA, Jacobs-Sera D et al. Bacteriophages of Gordonia spp. display a spectrum of diversity and genetic relationships. MBio 2017;8:e01069-17 [CrossRef][PubMed]
    [Google Scholar]
  20. Bolduc B, Jang HB, Doulcier G, You ZQ, Roux S et al. vConTACT: an iVirus tool to classify double-stranded DNA viruses that infect Archaea and Bacteria. PeerJ 2017;5:e3243 [CrossRef][PubMed]
    [Google Scholar]
  21. Meier-Kolthoff JP, Göker M. VICTOR: genome-based phylogeny and classification of prokaryotic viruses. Bioinformatics 2017;33:3396–3404 [CrossRef][PubMed]
    [Google Scholar]
  22. Hatfull GF, Hendrix RW. Bacteriophages and their genomes. Curr Opin Virol 2011;1:298–303 [CrossRef][PubMed]
    [Google Scholar]
  23. Mavrich TN, Hatfull GF. Bacteriophage evolution differs by host, lifestyle and genome. Nat Microbiol 2017;2:17112 [CrossRef][PubMed]
    [Google Scholar]
  24. Bruen TC, Philippe H, Bryant D. A simple and robust statistical test for detecting the presence of recombination. Genetics 2006;172:2665–2681 [CrossRef][PubMed]
    [Google Scholar]
  25. Zhao Y, Wu J, Yang J, Sun S, Xiao J et al. PGAP: pan-genomes analysis pipeline. Bioinformatics 2012;28:416–418 [CrossRef][PubMed]
    [Google Scholar]
  26. Katoh K, Asimenos G, Toh H. Multiple alignment of DNA sequences with MAFFT. In Posada D. (editor) Bioinformatics for DNA Sequence Analysis Totowa, NJ: Humana Press; pp.39–64
    [Google Scholar]
  27. Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010;27:221–224 [CrossRef][PubMed]
    [Google Scholar]
  28. Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 2004;20:289–290 [CrossRef][PubMed]
    [Google Scholar]
  29. Jombart T, Archer F, Schliep K, Kamvar Z, Harris R et al. apex: phylogenetics with multiple genes. Mol Ecol Resour 2017;17:19–26 [CrossRef][PubMed]
    [Google Scholar]
  30. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2006;23:254–267 [CrossRef][PubMed]
    [Google Scholar]
  31. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015;43:e15 [CrossRef][PubMed]
    [Google Scholar]
  32. 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 [CrossRef][PubMed]
    [Google Scholar]
  33. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014;30:2068–2069 [CrossRef][PubMed]
    [Google Scholar]
  34. 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 [CrossRef][PubMed]
    [Google Scholar]
  35. Dykhuizen DE, Green L. Recombination in Escherichia coli and the definition of biological species. J Bacteriol 1991;173:7257–7268 [CrossRef][PubMed]
    [Google Scholar]
  36. Feil EJ, Holmes EC, Bessen DE, Chan MS, Day NP et al. Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc Natl Acad Sci USA 2001;98:182–187 [CrossRef][PubMed]
    [Google Scholar]
  37. Milkman R. Recombination and population structure in Escherichia coli. Genetics 1997;146:745–750[PubMed]
    [Google Scholar]
  38. Wertz JE, Goldstone C, Gordon DM, Riley MA. A molecular phylogeny of enteric bacteria and implications for a bacterial species concept. J Evol Biol 2003;16:1236–1248 [CrossRef][PubMed]
    [Google Scholar]
  39. Leigh JW, Lapointe FJ, Lopez P, Bapteste E. Evaluating phylogenetic congruence in the post-genomic era. Genome Biol Evol 2011;3:571–587 [CrossRef][PubMed]
    [Google Scholar]
  40. Holland B, Moulton V. Consensus networks: a method for visualising incompatibilities in collections of trees. In Algorithms in Bioinformatics Berlin, Heidelberg: Springer; pp.165–176
    [Google Scholar]
  41. Holland BR, Huber KT, Moulton V, Lockhart PJ. Using consensus networks to visualize contradictory evidence for species phylogeny. Mol Biol Evol 2004;21:1459–1461 [CrossRef][PubMed]
    [Google Scholar]
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