Virus Satellites Drive Viral Evolution and Ecology
Satellites are defined as viruses that have a life cycle dependent on a helper virus. Thus, they can be considered as parasites of parasites. In addition to their fascinating life cycle, these widespread infectious elements, present both in eukaryotic and prokaryotic cells, have a dramatic role in virulence by controlling the symptoms induced by their eukaryotic helper viruses or by encoding key bacterial virulence genes. While satellites can play an important role in the ecology of the viruses they parasitise, the evolutionary impact on their helper viruses is unclear. Here we show that staphylococcal pathogenicity islands (SaPIs), an example of a virus satellite, are a major selective force on the viruses (bacteriophages) they parasitise. Using both bioinformatic and experimental evolution data we have been able to confirm that pathogenicity islands are a major selective pressure enhancing the diversity of both genes and gene content in Staphylococcus aureus phages. Since SaPIs exploit the life cycle of their helper phages to enable their rapid replication and promiscuous spread, these strategies are mechanisms that reduce SaPI interference, thus facilitating the infectivity and dissemination of the helper phages in nature.
Vyšlo v časopise:
Virus Satellites Drive Viral Evolution and Ecology. PLoS Genet 11(10): e32767. doi:10.1371/journal.pgen.1005609
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005609
Souhrn
Satellites are defined as viruses that have a life cycle dependent on a helper virus. Thus, they can be considered as parasites of parasites. In addition to their fascinating life cycle, these widespread infectious elements, present both in eukaryotic and prokaryotic cells, have a dramatic role in virulence by controlling the symptoms induced by their eukaryotic helper viruses or by encoding key bacterial virulence genes. While satellites can play an important role in the ecology of the viruses they parasitise, the evolutionary impact on their helper viruses is unclear. Here we show that staphylococcal pathogenicity islands (SaPIs), an example of a virus satellite, are a major selective force on the viruses (bacteriophages) they parasitise. Using both bioinformatic and experimental evolution data we have been able to confirm that pathogenicity islands are a major selective pressure enhancing the diversity of both genes and gene content in Staphylococcus aureus phages. Since SaPIs exploit the life cycle of their helper phages to enable their rapid replication and promiscuous spread, these strategies are mechanisms that reduce SaPI interference, thus facilitating the infectivity and dissemination of the helper phages in nature.
Zdroje
1. Huang Y-W, Hu C-C, Lin N-S, Hsu Y-H. Mimicry of molecular pretenders: the terminal structures of satellites associated with plant RNA viruses. RNA Biol. 2010;7: 162–171. 20139733
2. Nawaz-ul-Rehman MS, Fauquet CM. Evolution of geminiviruses and their satellites. FEBS Lett. 2009;583: 1825–1832. doi: 10.1016/j.febslet.2009.05.045 19497325
3. Simon AE, Roossinck MJ, Havelda Z. Plant virus satellite and defective interfering RNAs: new paradigms for a new century. Annu Rev Phytopathol. 2004;42: 415–437. 15283672
4. Christie GE, Dokland T. Pirates of the Caudovirales. Virology. 2012;434: 210–221. doi: 10.1016/j.virol.2012.10.028 23131350
5. Ram G, Chen J, Kumar K, Ross HF, Ubeda C, Damle PK, et al. Staphylococcal pathogenicity island interference with helper phage reproduction is a paradigm of molecular parasitism. Proc Natl Acad Sci USA. 2012;109: 16300–16305. doi: 10.1073/pnas.1204615109 22991467
6. Ram G, Chen J, Ross HF, Novick RP. Precisely modulated pathogenicity island interference with late phage gene transcription. Proc Natl Acad Sci USA. 2014;111: 14536–14541. doi: 10.1073/pnas.1406749111 25246539
7. Fuhrman JA. Marine viruses and their biogeochemical and ecological effects. Nature. 1999;399: 541–548. 10376593
8. Alves C, Branco C, Cunha C. Hepatitis delta virus: a peculiar virus. Adv Virol. 2013;2013: 560105. doi: 10.1155/2013/560105 24198831
9. Viana D, Blanco J, Tormo-Más MÁ, Selva L, Guinane CM, Baselga R, et al. Adaptation of Staphylococcus aureus to ruminant and equine hosts involves SaPI-carried variants of von Willebrand factor-binding protein. Mol Microbiol. 2010;77: 1583–1594. 20860091
10. Novick RP, Christie GE, Penadés JR. The phage-related chromosomal islands of Gram-positive bacteria. Nat Rev Microbiol. 2010;8: 541–551. doi: 10.1038/nrmicro2393 20634809
11. Hassan F, Kamruzzaman M, Mekalanos JJ, Faruque SM. Satellite phage TLCφ enables toxigenic conversion by CTX phage through dif site alteration. Nature. 2010;467: 982–985. doi: 10.1038/nature09469 20944629
12. Davis BM, Waldor MK. Filamentous phages linked to virulence of Vibrio cholerae. Curr Opin Microbiol. 2003;6: 35–42. 12615217
13. Buckling A, Rainey PB. Antagonistic coevolution between a bacterium and a bacteriophage. Proc Biol Sci. 2002;269: 931–936. 12028776
14. Ubeda C, Maiques E, Barry P, Matthews A, Tormo MA, Lasa I, et al. SaPI mutations affecting replication and transfer and enabling autonomous replication in the absence of helper phage. Mol Microbiol. 2008;67: 493–503. 18086210
15. Tormo-Más MÁ, Mir I, Shrestha A, Tallent SM, Campoy S, Lasa I, et al. Moonlighting bacteriophage proteins derepress staphylococcal pathogenicity islands. Nature. 2010;465: 779–782. doi: 10.1038/nature09065 20473284
16. Tormo-Más MÁ, Donderis J, García-Caballer M, Alt A, Mir-Sanchis I, Marina A, et al. Phage dUTPases control transfer of virulence genes by a proto-oncogenic G protein-like mechanism. Mol Cell. 2013;49: 947–958. doi: 10.1016/j.molcel.2012.12.013 23333307
17. Quiles-Puchalt N, Martínez-Rubio R, Ram G, Lasa I, Penadés JR. Unravelling bacteriophage ϕ11 requirements for packaging and transfer of mobile genetic elements in Staphylococcus aureus. Mol Microbiol. 2014;91: 423–437. doi: 10.1111/mmi.12445 24283262
18. Tormo MA, Ferrer MD, Maiques E, Ubeda C, Selva L, Lasa I, et al. Staphylococcus aureus pathogenicity island DNA is packaged in particles composed of phage proteins. J Bacteriol. 2008;190: 2434–2440. doi: 10.1128/JB.01349-07 18223072
19. 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. 15788529
20. Liu J, Dehbi M, Moeck G, Arhin F, Bauda P, Bergeron D, et al. Antimicrobial drug discovery through bacteriophage genomics. Nat Biotechnol. 2004;22: 185–191. 14716317
21. Matos RC, Lapaque N, Rigottier-Gois L, Debarbieux L, Meylheuc T, Gonzalez-Zorn B, et al. Enterococcus faecalis prophage dynamics and contributions to pathogenic traits. PLoS Genet. 2013;9: e1003539. doi: 10.1371/journal.pgen.1003539 23754962
22. Martínez-Rubio R. PICs: una nueva familia de elementos móviles bacterianos en movimiento. PhD thesis. Universidad CEU Cardenal Herrera. 2013. http://catalogo.ceu.es/Record/uchceu589288?library=fuspceu.
23. Lindsay JA, Ruzin A, Ross HF, Kurepina N, Novick RP. The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol Microbiol. 1998;29: 527–543. 9720870
24. Ubeda C, Maiques E, Knecht E, Lasa I, Novick RP, Penadés JR. Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol Microbiol. 2005;56: 836–844. 15819636
25. Maiques E, Ubeda C, Tormo MA, Ferrer MD, Lasa I, Novick RP, et al. Role of staphylococcal phage and SaPI integrase in intra- and interspecies SaPI transfer. J Bacteriol. 2007;189: 5608–5616. 17545290
26. Quiles-Puchalt N, Tormo-Más MÁ, Campoy S, Toledo-Arana A, Monedero V, Lasa I, et al. A super-family of transcriptional activators regulates bacteriophage packaging and lysis in Gram-positive bacteria. Nucleic Acids Res. 2013;41: 7260–7275. doi: 10.1093/nar/gkt508 23771138
27. Ferrer MD, Quiles-Puchalt N, Harwich MD, Tormo-Más MÁ, Campoy S, Barbé J, et al. RinA controls phage-mediated packaging and transfer of virulence genes in Gram-positive bacteria. Nucleic Acids Res. 2011;39: 5866–5878. doi: 10.1093/nar/gkr158 21450808
28. Quiles-Puchalt N, Carpena N, Alonso JC, Novick RP, Marina A, Penadés JR. Staphylococcal pathogenicity island DNA packaging system involving cos-site packaging and phage-encoded HNH endonucleases. Proc Natl Acad Sci USA. 2014;111: 6016–6021. doi: 10.1073/pnas.1320538111 24711396
29. Chen J, Carpena N, Quiles-Puchalt N, Ram G, Novick RP, Penadés JR. Intra- and inter-generic transfer of pathogenicity island-encoded virulence genes by cos phages. ISME J. 2015;9: 1260–1263. doi: 10.1038/ismej.2014.187 25314321
30. Penadés JR, Donderis J, García-Caballer M, Tormo-Más MÁ, Marina A. dUTPases, the unexplored family of signalling molecules. Curr Opin Microbiol. 2013;16: 163–170. doi: 10.1016/j.mib.2013.02.005 23541339
31. Lopez Pascua L, Hall AR, Best A, Morgan AD, Boots M, Buckling A. Higher resources decrease fluctuating selection during host-parasite coevolution. Ecol Lett. 2014;17: 1380–1388. doi: 10.1111/ele.12337 25167763
32. Gómez P, Ashby B, Buckling A. Population mixing promotes arms race host-parasite coevolution. Proc Biol Sci. 2015;282: 20142297. doi: 10.1098/rspb.2014.2297 25429018
33. Buckling A, Brockhurst M. Bacteria-virus coevolution. Adv Exp Med Biol. 2012;751: 347–370. doi: 10.1007/978-1-4614-3567-9_16 22821466
34. Ubeda C, Maiques E, Tormo MA, Campoy S, Lasa I, Barbé J, et al. SaPI operon I is required for SaPI packaging and is controlled by LexA. Mol Microbiol. 2007;65: 41–50. 17581119
35. Charpentier E, Anton AI, Barry P, Alfonso B, Fang Y, Novick RP. Novel cassette-based shuttle vector system for gram-positive bacteria. Appl Environ Microbiol. 2004;70: 6076–6085. 15466553
36. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28: 2731–2739. doi: 10.1093/molbev/msr121 21546353
37. Martin D, Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics. 2000;16: 562–563. 10980155
38. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SDW. Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol. 2006;23: 1891–1901. 16818476
39. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14: 1394–1403. 15231754
40. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23: 254–267. 16221896
41. Bawono P, Heringa J. PRALINE: a versatile multiple sequence alignment toolkit. Methods Mol Biol. Totowa, NJ: Humana Press; 2014;1079: 245–262. doi: 10.1007/978-1-62703-646-7_16 24170407
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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