Widespread Genome Reorganization of an Obligate Virus Mutualist
Microorganisms form obligate associations with multicellular organisms that range from antagonistic (parasitic) to beneficial (mutualists). Although numerous examples of obligate, mutualistic bacteria, fungi, and protozoans exist, viruses are thought to usually form parasitic associations. An exception is the family Polydnaviridae, which consists of large DNA viruses that have evolved into mutualists of insects called parasitoid wasps. Each wasp species relies on its associated polydnavirus to parasitize hosts while each polydnavirus relies on its wasp for transmission. Polydnaviruses in the genus Bracovirus evolved approximately 100 million years ago from a group of viruses called nudiviruses, which are closely related to another large family of viruses called baculoviruses that are virulent pathogens of insects. Bracoviruses are of interest, therefore, because they provide a study system for examining how evolution into mutualists affects the structure and function of viral genomes. In this study, we sequenced the genome of the wasp Microplitis demolitor to characterize the proviral genome of M. demolitor bracovirus (MdBV). While the viral ancestor of bracoviruses possessed an independent circular genome, the proviral genome of MdBV is widely dispersed in the genome of M. demolitor. Our results also provide new insights into how the MdBV genome functions to produce virus particles that wasps rely upon to parasitize host insects.
Vyšlo v časopise:
Widespread Genome Reorganization of an Obligate Virus Mutualist. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004660
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004660
Souhrn
Microorganisms form obligate associations with multicellular organisms that range from antagonistic (parasitic) to beneficial (mutualists). Although numerous examples of obligate, mutualistic bacteria, fungi, and protozoans exist, viruses are thought to usually form parasitic associations. An exception is the family Polydnaviridae, which consists of large DNA viruses that have evolved into mutualists of insects called parasitoid wasps. Each wasp species relies on its associated polydnavirus to parasitize hosts while each polydnavirus relies on its wasp for transmission. Polydnaviruses in the genus Bracovirus evolved approximately 100 million years ago from a group of viruses called nudiviruses, which are closely related to another large family of viruses called baculoviruses that are virulent pathogens of insects. Bracoviruses are of interest, therefore, because they provide a study system for examining how evolution into mutualists affects the structure and function of viral genomes. In this study, we sequenced the genome of the wasp Microplitis demolitor to characterize the proviral genome of M. demolitor bracovirus (MdBV). While the viral ancestor of bracoviruses possessed an independent circular genome, the proviral genome of MdBV is widely dispersed in the genome of M. demolitor. Our results also provide new insights into how the MdBV genome functions to produce virus particles that wasps rely upon to parasitize host insects.
Zdroje
1. MoranNA (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci U S A 104 Suppl 1: 8627–8633.
2. VillarrealLP (2007) Virus-host symbiosis mediated by persistence. Symbiosis 43: 1–9.
3. WernegreenJJ (2012) Endosymbiosis. Curr Biol 22: R555–561.
4. OchmanH, MoranNA (2001) Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292: 1096–1099.
5. RaffaeleS, KamounS (2012) Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol 10: 417–430.
6. OldroydGE (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11: 252–263.
7. KuoCH, OchmanH (2009) Deletional bias across the three domains of life. Genome Biol Evol 1: 145–152.
8. MiraA, OchmanH, MoranNA (2001) Deletional bias and the evolution of bacterial genomes. Trends Genet 17: 589–596.
9. McCutcheonJP, MoranNA (2012) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10: 13–26.
10. KelkarYD, OchmanH (2012) Causes and consequences of genome expansion in fungi. Genome Biol Evol 4: 13–23.
11. LynchM, ConeryJS (2003) The origins of genome complexity. Science 302: 1401–1404.
12. VogelKJ, MoranNA (2013) Functional and evolutionary analysis of the genome of an obligate fungal symbiont. Genome Biol Evol 5: 891–904.
13. MartinF, KohlerA, MuratC, BalestriniR, CoutinhoPM, et al. (2010) Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464: 1033–1038.
14. DuffyS, ShackeltonLA, HolmesEC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9: 267–276.
15. FeschotteC, GilbertC (2012) Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 13: 283–296.
16. KatzourakisA, GiffordRJ (2010) Endogenous viral elements in animal genomes. PLOS Genet 6: e1001191.
17. KijimaTE, InnanH (2010) On the estimation of the insertion time of LTR retrotransposable elements. Mol Biol Evol 27: 896–904.
18. HolmesEC (2011) What does virus evolution tell us about virus origins? J Virol 85: 5247–5251.
19. MalletF, BoutonO, PrudhommeS, CheynetV, OriolG, et al. (2004) The endogenous retroviral locus ERVWE1 is a bona fide gene involved in hominoid placental physiology. Proc Natl Acad Sci U S A 101: 1731–1736.
20. StrandMR, BurkeGR (2013) Polydnavirus-wasp associations: evolution, genome organization, and function. Curr Opin Virol 3: 587–594.
21. Gundersen-RindalD, DupuyC, HuguetE, Drezen, JM (2013) Parasitoid polydnaviruses: evolution, pathology and applications. Biocontrol Sci Techn 23: 1–61.
22. HerniouEA, HuguetE, ThézéJ, BézierA, PeriquetG, et al. (2013) When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses. Philos Trans R Soc Lond B Biol Sci 368: 20130051 doi:1 0.1098/rstb.2013.0051
23. Godfray HJC (1994) Parasitoids: behavioural and evolutionary ecology. Princeton: Princeton University Press.
24. MurphyN, BanksJC, WhitfieldJB, AustinAD (2008) Phylogeny of the parasitic microgastroid subfamilies (Hymenoptera: Braconidae) based on sequence data from seven genes, with an improved time estimate of the origin of the lineage. Mol Phylogenet Evol 47: 378–395.
25. RodriguezJJ, Fernández-TrianaJL, SmithMA, JanzenDH, HallwachsW, et al. (2013) Extrapolations from field studies and known faunas converge on dramatically increased estimates of global microgastrine parasitoid wasp species richness (Hymenoptera: Braconidae). Insect Conserv and Diver 6: 530–536.
26. WhitfieldJB (2002) Estimating the age of the polydnavirus/braconid wasp symbiosis. Proc Natl Acad Sci U S A 99: 7508–7513.
27. BézierA, AnnaheimM, HerbinièreJ, WetterwaldC, GyapayG, et al. (2009) Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323: 926–930.
28. BurkeGR, StrandMR (2012) Deep sequencing identifies viral and wasp genes with potential roles in replication of Microplitis demolitor Bracovirus. J Virol 86: 3293–3306.
29. MartiD, Grossniklaus-BurginC, WyderS, WylerT, LanzreinB (2003) Ovary development and polydnavirus morphogenesis in the parasitic wasp Chelonus inanitus. I. Ovary morphogenesis, amplification of viral DNA and ecdysteroid titres. J Gen Virol 84: 1141–1150.
30. GruberA, StettlerP, HeinigerP, SchumperliD, LanzreinB (1996) Polydnavirus DNA of the braconid wasp Chelonus inanitus is integrated in the wasp's genome and excised only in later pupal and adult stages of the female. J Gen Virol 77 (Pt 11) 2873–2879.
31. StoltzDB, VinsonSB (1977) Baculovirus-like particles in the reproductive tracts of female parasitoid wasps. II. The genus Apanteles. Can J Microbiol 23: 28–37.
32. StoltzDB, VinsonSB (1979) Viruses and parasitism in insects. Adv Virus Res 24: 125–171.
33. Strand MR (2010) Polydnaviruses. In: Asgari S, Johnson KN, editors. Insect Virology. Norwich, UK: Caister Academic Press. pp. 171–197.
34. StrandMR, BurkeGR (2012) Polydnaviruses as symbionts and gene delivery systems. PLOS Pathog 8: e1002757.
35. BeckMH, ZhangS, BitraK, BurkeGR, StrandMR (2011) The encapsidated genome of Microplitis demolitor bracovirus integrates into the host Pseudoplusia includens. J Virol 85: 11685–11696.
36. WetterwaldC, RothT, KaeslinM, AnnaheimM, WespiG, et al. (2010) Identification of bracovirus particle proteins and analysis of their transcript levels at the stage of virion formation. J Gen Virol 91: 2610–2619.
37. Jehle JA (2010) Nudiviruses. In: Asgari S, Johnson KN, editors. Insect Virology. Norwich, UK: Caister Academic Press. pp. 153–170.
38. Rohrmann GF (2013) Baculovirus molecular biology. Bethesda: National Library of Medicine, National Center for Biotechnology information.
39. WangY, JehleJA (2009) Nudiviruses and other large, double-stranded circular DNA viruses of invertebrates: new insights on an old topic. J Invertebr Pathol 101: 187–193.
40. ChenYF, GaoF, YeXQ, WeiSJ, ShiM, et al. (2011) Deep sequencing of Cotesia vestalis bracovirus reveals the complexity of a polydnavirus genome. Virology 414: 42–50.
41. DesjardinsCA, Gundersen-RindalDE, HostetlerJB, TallonLJ, FadroshDW, et al. (2008) Comparative genomics of mutualistic viruses of Glyptapanteles parasitic wasps. Genome Biol 9: R183.
42. EspagneE, DupuyC, HuguetE, CattolicoL, ProvostB, et al. (2004) Genome sequence of a polydnavirus: insights into symbiotic virus evolution. Science 306: 286–289.
43. WebbBA, StrandMR, DickeySE, BeckMH, HilgarthRS, et al. (2006) Polydnavirus genomes reflect their dual roles as mutualists and pathogens. Virology 347: 160–174.
44. WeberB, AnnaheimM, LanzreinB (2007) Transcriptional analysis of polydnaviral genes in the course of parasitization reveals segment-specific patterns. Arch Insect Biochem Physiol 66: 9–22.
45. BitraK, ZhangS, StrandMR (2011) Transcriptomic profiling of Microplitis demolitor bracovirus reveals host, tissue and stage-specific patterns of activity. J Gen Virol 92: 2060–2071.
46. Webb BA, Strand MR (2005) The biology and genomics of polydnaviruses. In: Gilbert L, Iatrou I, Gill SS, editors. Comprehensive molecular insect science. Boston: Elsevier. pp. 323–360.
47. BézierA, LouisF, JancekS, PeriquetG, ThézéJ, et al. (2013) Functional endogenous viral elements in the genome of the parasitoid wasp Cotesia congregata: insights into the evolutionary dynamics of bracoviruses. Philos Trans R Soc Lond B Biol Sci 368: 20130047.
48. DesjardinsCA, Gundersen-RindalDE, HostetlerJB, TallonLJ, FuesterRW, et al. (2007) Structure and evolution of a proviral locus of Glyptapanteles indiensis bracovirus. BMC Microbiol 7: 61.
49. BurkeGR, ThomasSA, EumJH, StrandMR (2013) Mutualistic polydnaviruses share essential replication gene functions with pathogenic ancestors. PLoS Pathog 9: e1003348.
50. BeckMH, InmanRB, StrandMR (2007) Microplitis demolitor bracovirus genome segments vary in abundance and are individually packaged in virions. Virology 359: 179–189.
51. AlbrechtU, WylerT, Pfister-WilhelmR, GruberA, StettlerP, et al. (1994) Polydnavirus of the parasitic wasp Chelonus inanitus (Braconidae): characterization, genome organization and time point of replication. J Gen Virol 75: 3353–3363.
52. SavaryS, BeckageN, TanF, PeriquetG, DrezenJM (1997) Excision of the polydnavirus chromosomal integrated EP1 sequence of the parasitoid wasp Cotesia congregata (Braconidae, Microgastinae) at potential recombinase binding sites. J Gen V: 3125–3134.
53. SavaryS, DrezenJM, TanF, BeckageNE, PeriquetG (1999) The excision of polydnavirus sequences from the genome of the wasp Cotesia congregata (Braconidae, microgastrinae) is developmentally regulated but not strictly restricted to the ovaries in the adult. Insect Mol Biol 8: 319–327.
54. SerbielleC, DupasS, PerdereauE, HéricourtF, DupuyC, et al. (2012) Evolutionary mechanisms driving the evolution of a large polydnavirus gene family coding for protein tyrosine phosphatases. BMC Evol Biol 12: 253.
55. BurkeGR, StrandMR (2012) Polydnaviruses of parasitic wasps: domestication of viruses to act as gene delivery vectors. Insects 3: 91–119.
56. HrcekJMS, WhitfieldJB, ShimaH, NovotnyV (2013) Parasitism rate, parasitoid community composition and host specificity on exposed and semi-concealed caterpillars from a tropical rainforest. Oecologia 173: 521–532.
57. SmithMA, RodriguezJJ, WhitfieldJB, DeansAR, JanzenDH, et al. (2008) Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proc Natl Acad Sci U S A 105: 12359–12364.
58. BurkeGR, StrandMR (2014) Systematic analysis of a wasp parasitism arsenal. Mol Ecol 23: 890–901.
59. HerniouEA, OlszewskiJA, CoryJS, O'ReillyDR (2003) The genome sequence and evolution of baculoviruses. Annu Rev Entomol 48: 211–234.
60. ThézéJ, BézierA, PeriquetG, DrezenJM, HerniouEA (2011) Paleozoic origin of insect large dsDNA viruses. Proc Natl Acad Sci U S A 108: 15931–15935.
61. ChenYR, ZhongS, FeiZ, HashimotoY, XiangJZ, et al. (2013) The transcriptome of the baculovirus Autographa californica multiple nucleopolyhedrovirus in Trichoplusia ni cells. J Virol 87: 6391–6405.
62. MansRM, Knebel-MörsdorfD (1998) In vitro transcription of pe38/polyhedrin hybrid promoters reveals sequences essential for recognition by the baculovirus-induced RNA polymerase and for the strength of very late viral promoters. J Virol 72: 2991–2998.
63. WerrenJH, RichardsS, DesjardinsCA, NiehuisO, GadauJ, et al. (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327: 343–348.
64. LouisF, BézierA, PeriquetG, FerrasC, DrezenJM, et al. (2013) The bracovirus genome of the parasitoid wasp Cotesia congregata is amplified within 13 replication units, including sequences not packaged in the particles. J Virol 87: 9649–9660.
65. BurandJP, KimW, AfonsoCL, TulmanER, KutishGF, et al. (2012) Analysis of the genome of the sexually transmitted insect virus Helicoverpa zea nudivirus 2. Viruses 4: 28–61.
66. WuYL, WuCP, LeeST, TangH, ChangCH, et al. (2010) The early gene hhi1 reactivates Heliothis zea nudivirus 1 in latently infected cells. J Virol 84: 1057–1065.
67. CasewellNR, WusterW, VonkFJ, HarrisonRA, FryBG (2013) Complex cocktails: the evolutionary novelty of venoms. Trends Ecol Evol 28: 219–229.
68. Huguet E, Serbielle C, Moreau SJM. (2012) Evolution and origin of polydnavirus virulence genes. In Beckage NE, Drezen J-M editors. Parasitoid Viruses Symbionts and Pathogens. Academic Press. pp. 63–78.
69. FriedmanR, HughesAL (2006) Pattern of gene duplication in the Cotesia congregata bracovirus. Infect Genet Evol 6: 315–322.
70. DrezenJM, BézierA, LesobreJ, HuguetE, CattolicoL, et al. (2006) The few virus-like genes of Cotesia congregata bracovirus. Arch Insect Biochem Physiol 61: 110–122.
71. HackerJ, KaperJB (2000) Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54: 641–679.
72. VolkoffAN, JouanV, UrbachS, SamainS, BergoinM, et al. (2010) Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. PLOS Pathog 6: e1000923.
73. AswadA, KatzourakisA (2012) Paleovirology and virally derived immunity. Trends Ecol Evol 27: 627–636.
74. NovákováE, HypsaV, KleinJ, FoottitRG, von DohlenCD, MoranNA (2013) Reconstructing the phylogeny of aphids (Hemiptera: Aphididae) using DNA of the obligate symbiont Buchnera aphidicola. Mol Phylogenet Evol 68: 42–54.
75. AnderssonJO (2000) Evolutionary genomics: is Buchnera a bacterium or an organelle? Curr Biology 10: R866–R868.
76. KelleyDR, SchatzMC, SalzbergSL (2010) Quake: quality-aware detection and correction of sequencing errors. Genome Biol 11: R116.
77. LiY, HuY, BolundL, WangJ (2010) State of the art de novo assembly of human genomes from massively parallel sequencing data. Hum Genomics 4: 271–277.
78. BurkeGR, MoranNA (2011) Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol Evol 3: 195–208.
79. LiH, DurbinR (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760.
80. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079.
81. MilneI, BayerM, CardleL, ShawP, StephenG, et al. (2010) Tablet–next generation sequence assembly visualization. Bioinformatics 26: 401–402.
82. GrabherrMG, HaasBJ, YassourM, LevinJZ, ThompsonDA, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29: 644–652.
83. MortazaviA, WilliamsBA, McCueK, SchaefferL, WoldB (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621–628.
84. HoltC, YandellM (2011) MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinformatics 12: 491.
85. TrapnellC, RobertsA, GoffL, PerteaG, KimD, et al. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562–578.
86. Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443: 931–949.
87. Ter-HovhannisyanV, LomsadzeA, ChernoffYO, BorodovskyM (2008) Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res 18: 1979–1990.
88. KellerO, KollmarM, StankeM, WaackS (2011) A novel hybrid gene prediction method employing protein multiple sequence alignments. Bioinformatics 27: 757–763.
89. KorfI (2004) Gene finding in novel genomes. BMC Bioinformatics 5: 59.
90. LeeE, HarrisN, GibsonM, ChettyR, LewisS (2009) Apollo: a community resource for genome annotation editing. Bioinformatics 25: 1836–1837.
91. FinnRD, MistryJ, TateJ, CoggillP, HegerA, et al. (2008) The Pfam protein families database. Nucleic Acids Res 38: D211–222.
92. HaftDH, SelengutJD, WhiteO (2003) The TIGRFAMs database of protein families. Nucleic Acids Res 31: 371–373.
93. LaslettD, CanbackB (2004) ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32: 11–16.
94. EdgarRC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
95. LiL, StoeckertCJJr, RoosDS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178–2189.
96. Zeng X, Pei, J., Vergara, I.A., Nesbitt, M., Wang, K., and Chen, N. OrthoCluster: A new tool for mining synteny blocks and applications in comparative genomics.; 2008 March 25–30; Nantes, France. Association for Computer Machinery, New York.
97. McKaySJ, VergaraIA, StajichJE (2010) Using the Generic Synteny Browser (GBrowse_syn). Curr Protoc Bioinformatics Chapter 9: Unit 9 12.
98. SteinLD, MungallC, ShuS, CaudyM, MangoneM, et al. (2002) The generic genome browser: a building block for a model organism system database. Genome Res 12: 1599–1610.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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