Viral Genome Segmentation Can Result from a Trade-Off between Genetic Content and Particle Stability

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The evolutionary benefit of viral genome segmentation is a classical, yet unsolved question in evolutionary biology and RNA genetics. Theoretical studies anticipated that replication of shorter RNA segments could provide a replicative advantage over standard size genomes. However, this question has remained elusive to experimentalists because of the lack of a proper viral model system. Here we present a study with a stable segmented bipartite RNA virus and its ancestor non-segmented counterpart, in an identical genomic nucleotide sequence context. Results of RNA replication, protein expression, competition experiments, and inactivation of infectious particles point to a non-replicative trait, the particle stability, as the main driver of fitness gain of segmented genomes. Accordingly, measurements of the volume occupation of the genome inside viral capsids indicate that packaging shorter genomes involves a relaxation of the packaging density that is energetically favourable. The empirical observations are used to design a computational model that predicts the existence of a critical multiplicity of infection for domination of segmented over standard types. Our experiments suggest that viral segmented genomes may have arisen as a molecular solution for the trade-off between genome length and particle stability. Genome segmentation allows maximizing the genetic content without the detrimental effect in stability derived from incresing genome length.

Vyšlo v časopise: Viral Genome Segmentation Can Result from a Trade-Off between Genetic Content and Particle Stability. PLoS Genet 7(3): e32767. doi:10.1371/journal.pgen.1001344
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001344

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Zdroje

1. Garcia-ArriazaJ

ManrubiaSC

TojaM

DomingoE

EscarmisC

2004 Evolutionary transition toward defective RNAs that are infectious by complementation. J Virol 78 11678 11685

2. Garcia-ArriazaJ

OjosnegrosS

DavilaM

DomingoE

EscarmisC

2006 Dynamics of mutation and recombination in a replicating population of complementing, defective viral genomes. J Mol Biol 360 558 572

3. NeeS

1987 The evolution of multicompartmental genomes in viruses. J Mol Evol 25 277 281

4. SzathmaryE

1992 Natural selection and dynamical coexistence of defective and complementing virus segments. J Theor Biol 157 383 406

5. ChaoL

1988 Evolution of sex in RNA viruses. J Theor Biol 133 99 112

6. HolmesEC

2009 The Evolution and Emergence of RNA Viruses;

HarveyPM

MayRM

Oxford Oxford University Press

7. EscarmisC

CarrilloEC

FerrerM

ArriazaJF

LopezN

1998 Rapid selection in modified BHK-21 cells of a foot-and-mouth disease virus variant showing alterations in cell tropism. J Virol 72 10171 10179

8. BarclayW

LiQ

HutchinsonG

MoonD

RichardsonA

1998 Encapsidation studies of poliovirus subgenomic replicons. J Gen Virol 79 Pt 7 1725 1734

9. MateoR

LunaE

RinconV

MateuMG

2008 Engineering viable foot-and-mouth disease viruses with increased thermostability as a step in the development of improved vaccines. J Virol 82 12232 12240

10. SzathmaryE

1992 Viral sex, levels of selection, and the origin of life. J Theor Biol 159 99 109

11. MillsDR

PetersonRL

SpiegelmanS

1967 An extracellular Darwinian experiment with a self-duplicating nucleic acid molecule. Proc Natl Acad Sci USA 58 217 224

12. SaboDL

DomingoE

BandleEF

FlavellRA

WeissmannC

1977 A guanosine to adenosine transition in the 3′ terminal extracistronic region of bacteriophage Qβ RNA leading to loss of infectivity. J Mol Biol 112 235 252

13. ColeCN

BaltimoreD

1973 Defective interfering particles of poliovirus. IV. Mechanisms of enrichment. J Virol 12 1414 1426

14. LundquistRE

SullivanM

MaizelJVJr

1979 Characterization of a new isolate of poliovirus defective interfering particles. Cell 18 759 769

15. NowakMA

MayRM

2000 Virus Dynamics. Mathematical Principles of Immunology and Virology New York Oxford University Press Inc

16. MatthewsBW

1968 Solvent content of protein crystals. J Mol Biol 33 491 497

17. JohnsonJE

RueckertRR

1997 Packaging and release of the viral genome.

ChiuW

BurnettRM

GarceaRL

Structural Biology of Viruses New York Oxford University Press 269 287

18. EscarmisC

DavilaM

CharpentierN

BrachoA

MoyaA

1996 Genetic lesions associated with Muller's ratchet in an RNA virus. J Mol Biol 264 255 267

19. DiezJ

DavilaM

EscarmisC

MateuMG

DominguezJ

1990 Unique amino acid substitutions in the capsid proteins of foot-and-mouth disease virus from a persistent infection in cell culture. J Virol 64 5519 5528

20. BettAJ

PrevecL

GrahamFL

1993 Packaging capacity and stability of human adenovirus type 5 vectors. J Virol 67 5911 5921

21. GelbartWM

KnoblerCM

2009 Virology. Pressurized viruses. Science 323 1682 1683

22. 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 doi:10.1371/journal.pbio.0040193

23. ChiricoN

VianelliA

Belshaw R Why genes overlap in viruses. Proc Biol Sci 277 3809 3817

24. SobrinoF

DavilaM

OrtinJ

DomingoE

1983 Multiple genetic variants arise in the course of replication of foot-and-mouth disease virus in cell culture. Virology 128 310 318

25. EscarmisC

DavilaM

DomingoE

1999 Multiple molecular pathways for fitness recovery of an RNA virus debilitated by operation of Muller's ratchet. J Mol Biol 285 495 505

26. ManrubiaSC

Garcia-ArriazaJ

EscarmísC

DomingoE

2006 Long-range transport and universality classes in in vitro viral infection spread. Europhysics Letters 74 547 553

27. PeralesC

AgudoR

TejeroH

ManrubiaSC

DomingoE

2009 Potential benefits of sequential inhibitor-mutagen treatments of RNA virus infections. PLoS Pathog 5 e1000658 doi:10.1371/journal.ppat.1000658

28. PeralesC

MateoR

MateuMG

DomingoE

2007 Insights into RNA virus mutant spectrum and lethal mutagenesis events: replicative interference and complementation by multiple point mutants. J Mol Biol 369 985 1000

29. MateuMG

MartinezMA

CapucciL

AndreuD

GiraltE

1990 A single amino acid substitution affects multiple overlapping epitopes in the major antigenic site of foot-and-mouth disease virus of serotype C. J Gen Virol 71 Pt 3 629 637

30. EscarmisC

PeralesC

DomingoE

2009 Biological effect of Muller's Ratchet: distant capsid site can affect picornavirus protein processing. J Virol 83 6748 6756

31. MareeAF

KeulenW

BoucherCA

De BoerRJ

2000 Estimating relative fitness in viral competition experiments. J Virol 74 11067 11072

32. HollandJJ

de la TorreJC

ClarkeDK