Manipulating or Superseding Host Recombination Functions: A Dilemma That Shapes Phage Evolvability

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Phages, like many parasites, tend to have small genomes and may encode autonomous functions or manipulate those of their hosts'. Recombination functions are essential for phage replication and diversification. They are also nearly ubiquitous in bacteria. The E. coli genome encodes many copies of an octamer (Chi) motif that upon recognition by RecBCD favors repair of double strand breaks by homologous recombination. This might allow self from non-self discrimination because RecBCD degrades DNA lacking Chi. Bacteriophage Lambda, an E. coli parasite, lacks Chi motifs, but escapes degradation by inhibiting RecBCD and encoding its own autonomous recombination machinery. We found that only half of 275 lambdoid genomes encode recombinases, the remaining relying on the host's machinery. Unexpectedly, we found that some lambdoid phages contain extremely high numbers of Chi motifs concentrated between the phage origin of replication and the packaging site. This suggests a tight association between replication, packaging and RecBCD-mediated recombination in these phages. Indeed, phages lacking recombinases strongly over-represent Chi motifs. Conversely, phages encoding recombinases and inhibiting host recombination machinery select for the absence of Chi motifs. Host and phage recombinases use different mechanisms and the latter are more tolerant to sequence divergence. Accordingly, we show that phages encoding their own recombination machinery have more mosaic genomes resulting from recent recombination events and have more diverse gene repertoires, i.e. larger pan genomes. We discuss the costs and benefits of superseding or manipulating host recombination functions and how this decision shapes phage genome structure and evolvability.

Vyšlo v časopise: Manipulating or Superseding Host Recombination Functions: A Dilemma That Shapes Phage Evolvability. PLoS Genet 9(9): e32767. doi:10.1371/journal.pgen.1003825
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003825

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Zdroje

1. MichelB, GromponeG, FloresMJ, BidnenkoV (2004) Multiple pathways process stalled replication forks. Proc Natl Acad Sci USA 101 : 12783–12788.

2. PeralsK, CapiauxH, VincourtJB, LouarnJM, SherrattDJ, et al. (2001) Interplay between recombination, cell division and chromosome structure during chromosome dimer resolution in Escherichia coli. Mol Microbiol 39 : 904–913.

3. BartonNH, CharlesworthB (1998) Why sex and recombination? Science 281 : 1986–1990.

4. FeilEJ, HolmesEC, BessenDE, ChanMS, DayNP, et al. (2001) Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc Natl Acad Sci U S A 98 : 182–187.

5. OchmanH, LeratE, DaubinV (2005) Examining bacterial species under the specter of gene transfer and exchange. Proc Natl Acad Sci U S A 102 Suppl 1 : 6595–6599.

6. HendrixRW, SmithMCM, BurnsRN, FordME, HatfullGF (1999) Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage. Proc Natl Acad Sci USA 96 : 2192–2197.

7. JuhalaRJ, FordME, DudaRL, YoultonA, HatfullGF, et al. (2000) Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol 299 : 27–51.

8. MartinsohnJT, RadmanM, PetitMA (2008) The lambda Red proteins promote efficient recombination between diverged sequences: Implications for bacteriophage genome mosaicism. PLoS Genet 4: e1000065.

9. BotsteinD (1980) A theory of modular evolution for bacteriophages. Ann N Y Acad Sci 354 : 484–490.

10. BobayLM, RochaEP, TouchonM (2013) The Adaptation of Temperate Bacteriophages to Their Host Genomes. Mol Biol Evol 30 : 737–751.

11. Campbell A, Botstein D (1983) Evolution of the lambdoid phages. In: Hendrix RW, Roberts JW, Stahl FW, Weisberg RA, editors. Lambda II. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory pp. 365–380.

12. CasjensSR (2008) Diversity among the tailed-bacteriophages that infect the Enterobacteriaceae. Res Microbiol 159 : 340–348.

13. CasjensS, HendrixR (1974) Comments on the arrangement of the morphogenetic genes of bacteriophage lambda. J Mol Biol 90 : 20–25.

14. KashiwagiA, YomoT (2011) Ongoing phenotypic and genomic changes in experimental coevolution of RNA bacteriophage Qbeta and Escherichia coli. PLoS Genet 7: e1002188.

15. PetersenL, BollbackJP, DimmicM, HubiszM, NielsenR (2007) Genes under positive selection in Escherichia coli. Genome Res 17 : 1336–1343.

16. PatersonS, VogwillT, BucklingA, BenmayorR, SpiersAJ, et al. (2010) Antagonistic coevolution accelerates molecular evolution. Nature 464 : 275–278.

17. WeinbauerMG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28 : 127–181.

18. Smith GR (1983) General Recombination. In: Hendrix RW, Roberts JW, Stahl FW, Weisberg RA, editors. Lambda II. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory. pp. 175–210.

19. EnquistLW, SkalkaA (1973) Replication of Bacteriophage-Lambda DNA-Dependent on Function of Host and Viral Genes .1. Interaction of Red, Gam and Rec. J Mol Biol 75 : 185–212.

20. KuzminovA (1999) Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol Mol Biol Rev 63 : 751–813.

21. MarescaM, ErlerA, FuJ, FriedrichA, ZhangYM, et al. (2010) Single-stranded heteroduplex intermediates in lambda Red homologous recombination. BMC Mol Biol 11 : 54.

22. UngerRC, ClarkAJ (1972) Interaction of the recombination pathways of bacteriophage lambda and its host Escherichia coli K12: effects on exonuclease V activity. J Mol Biol 70 : 539–548.

23. IyerLM, KooninEV, AravindL (2002) Classification and evolutionary history of the single-strand annealing proteins, RecT, Redbeta, ERF and RAD52. BMC Genomics 3 : 8.

24. LopesA, Amarir-BouhramJ, FaureG, PetitMA, GueroisR (2010) Detection of novel recombinases in bacteriophage genomes unveils Rad52, Rad51 and Gp2.5 remote homologs. Nucleic Acids Res 38 : 3952–3962.

25. MyersRS, StahlFW (1994) Chi and the RecBC D enzyme of Escherichia coli. Annu Rev Genet 28 : 49–70.

26. DillinghamMS, KowalczykowskiSC (2008) RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiology and molecular biology reviews : MMBR 72 : 642–671.

27. El KarouiM, BiaudetV, SchbathS, GrussA (1999) Characteristics of Chi distribution on different bacterial genomes. Res Microbiol 150 : 579–587.

28. HalpernD, ChiapelloH, SchbathS, RobinS, Hennequet-AntierC, et al. (2007) Identification of DNA motifs implicated in maintenance of bacterial core genomes by predictive modeling. PLoS Genet 3 : 1614–1621.

29. KuzminovA, SchabtachE, StahlFW (1994) Chi sites in combination with RecA protein increase the survival of linear DNA in Escherichia coli by inactivating exoV activity of RecBCD nuclease. Embo J 13 : 2764–2776.

30. AndersonDG, KowalczykowskiSC (1998) Reconstitution of an SOS response pathway: derepression of transcription in response to DNA breaks. Cell 95 : 975–979.

31. KobayashiI (1998) Selfishness and death: raison d'être of restriction, recombination and mitochondria. Trends Genet 14 : 368–374.

32. BullJJ, BadgettMR, SpringmanR, MolineuxIJ (2004) Genome properties and the limits of adaptation in bacteriophages. Evolution 58 : 692–701.

33. De PaepeM, TaddeiF (2006) Viruses' Life History: Towards a Mechanistic Basis of a Trade-Off between Survival and Reproduction among Phages. PLoS Biol 4: e193.

34. CapaldoFN, RamseyG, BarbourSD (1974) Analysis of Growth of Recombination-Deficient Strains of Escherichia-Coli-K-12. J Bacteriol 118 : 242–249.

35. MurphyKC (2012) Phage Recombinases and Their Applications. Advances in Virus Research, Vol 83: Bacteriophages, Pt B 83 : 367–414.

36. ThomsonN, BakerS, PickardD, FookesM, AnjumM, et al. (2004) The role of prophage-like elements in the diversity of Salmonella enterica serovars. J Mol Biol 339 : 279–300.

37. HandaN, IchigeA, KusanoK, KobayashiI (2000) Cellular responses to postsegregational killing by restriction-modification genes. J Bacteriol 182 : 2218–2229.

38. NoirotP, GuptaRC, RaddingCM, KolodnerRD (2003) Hallmarks of homology recognition by RecA-like recombinases are exhibited by the unrelated Escherichia coli RecT protein. Embo J 22 : 324–334.

39. RochaEPC, CornetE, MichelB (2005) Comparative and Evolutionary Analysis of the Bacterial Homologous Recombination Systems. PLoS Genet 1: e15.

40. SouriceS, BiaudetV, KarouiME, EhrlichSD, GrussA (1998) Identification of the Chi site of Haemophilus influenzae as several sequences related to the Escherichia coli Chi site. Mol Microbiol 27 : 1021–1029.

41. MyungH, CalendarR (1995) The Old Exonuclease of Bacteriophage-P2. J Bacteriol 177 : 497–501.

42. BouchardJD, MoineauS (2004) Lactococcal phage genes involved in sensitivity to AbiK and their relation to single-strand annealing proteins. J Bacteriol 186 : 3649–3652.

43. OhnishiM, KurokawaK, HayashiT (2001) Diversification of Escherichia coli genomes: are bacteriophages the major contributors? Trends Microbiol 9 : 481–485.

44. RaskoDA, WebsterDR, SahlJW, BashirA, BoisenN, et al. (2011) Origins of the E. coli Strain Causing an Outbreak of Hemolytic-Uremic Syndrome in Germany. N Engl J Med 365 : 709–717.

45. OliverKM, DegnanPH, HunterMS, MoranNA (2009) Bacteriophages Encode Factors Required for Protection in a Symbiotic Mutualism. Science 325 : 992–994.

46. StahlFW (2005) Chi: a little sequence controls a big enzyme. Genetics 170 : 487–493.

47. CanchayaC, FournousG, BrussowH (2004) The impact of prophages on bacterial chromosomes. Mol Microbiol 53 : 9–18.

48. Hendrix RW, Casjens S (2006) Bacteriophage Lambda and its Genetic Neighborhood. In: Abedon ST, Calendar RL, editors. The Bacteriophages. 2nd ed. New York: Oxford University Press. pp. 409–447.

49. Bailly-BechetM, VergassolaM, RochaE (2007) Causes for the intriguing presence of tRNAs in phages. Genome Res 17 : 1486–1495.

50. DavisBM, LawsonEH, SandkvistM, AliA, SozhamannanS, et al. (2000) Convergence of the secretory pathways for cholera toxin and the filamentous phage, CTX phi. Science 288 : 333–335.

51. BrownSP (2005) Do all parasites manipulate their hosts? Behav Process 68 : 237–240.

52. FoutsDE (2006) Phage_Finder: automated identification and classification of prophage regions in complete bacterial genome sequences. Nucleic Acids Res 34 : 5839–5851.

53. ZhouY, LiangY, LynchKH, DennisJJ, WishartDS (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39: W347–352.

54. Lima-MendezG, Van HeldenJ, ToussaintA, LeplaeR (2008) Prophinder: a computational tool for prophage prediction in prokaryotic genomes. Bioinformatics 24 : 863–865.

55. TouchonM, RochaEP (2007) Causes of insertion sequences abundance in prokaryotic genomes. Mol Biol Evol 24 : 969–981.

56. EnrightAJ, Van DongenS, OuzounisCA (2002) An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 30 : 1575–1584.

57. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 : 1792–1797.

58. RemmertM, BiegertA, HauserA, SodingJ (2012) HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nat Methods 9 : 173–175.

59. EddySR (2011) Accelerated Profile HMM Searches. PLoS Comput Biol 7: e1002195.

60. Schbath S, Hoebeke M (2011) R'MES: a tool to find motifs with a significantly unexpected frequency in biological sequences. Elnitski L, Piontkivska O, Welch L, editors. Singapore: World Scientific.

61. RochaEPC, DanchinA (2002) Competition for scarce resources might bias bacterial genome composition. Trends Genet 18 : 291–294.

62. SchbathS, PrumB, TurckheimEd (1995) Exceptional motifs in different Markov chain models for a statistical analysis of DNA sequences. J Comput Biol 2 : 417–437.

63. ChengKC, SmithGR (1987) Cutting of chi-like sequences by the RecBCD enzyme of Escherichia coli. J Mol Biol 194 : 747–750.

64. NovichkovPS, OmelchenkoMV, GelfandMS, MironovAA, WolfYI, et al. (2004) Genome-wide molecular clock and horizontal gene transfer in bacterial evolution. J Bacteriol 186 : 6575–6585.

65. CriscuoloA, GribaldoS (2010) BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 10 : 210.

66. SchmidtHA, StrimmerK, VingronM, von HaeselerA (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18 : 502–504.