Synchronous loss of quasispecies memory in parallel viral lineages: a deterministic feature of viral quasispecies.

Viral quasispecies are endowed with a memory of their past evolutionary history in the form of minority genomes of their mutant spectra. To determine the fate of memory genomes in evolving viral quasispecies, we have measured memory levels of antigenic variant of foot-and-mouth disease virus (FMDV) RED, which includes an Arg-Glu-Asp (RED) at a surface antigenic loop of the viral capsid. The RED reverted to the standard Arg-Gly-Asp (RGD), and the RED remained as memory in the evolving quasispecies. In four parallel evolutionary lineages, memory reduction followed a strikingly similar pattern, and at passage 60 memory levels were indistinguishable from those of control populations (devoid of memory). Nucleotide sequence analyses indicated that memory loss occurred synchronously despite its ultimate molecular basis being the stochastic occurrence of mutations in the evolving quasispecies. These results on the kinetics of memory levels have unveiled a deterministic feature of viral quasispecies. Molecular mechanisms that may underlie synchronous memory loss are the averaging of noise signals derived from mutational input, and constraints to genome diversification imposed by a nucleotide sequence context in the viral genome. Possible implications of the behaviour of complex, adaptive viral systems as experimental models to address primary mechanisms of neurological memory are discussed.

[1]  L. Tsimring,et al.  Reproducible nonlinear population dynamics and critical points during replicative competitions of RNA virus quasispecies. , 1996, Journal of molecular biology.

[2]  M. Eigen On the nature of virus quasispecies. , 1996, Trends in microbiology.

[3]  A. Moya,et al.  Fitness alteration of foot-and-mouth disease virus mutants: measurement of adaptability of viral quasispecies , 1991, Journal of virology.

[4]  E. Domingo,et al.  Nucleotide sequence heterogeneity of the RNA from a natural population of foot-and-mouth-disease virus. , 1980, Gene.

[5]  D. Crothers,et al.  Nucleic Acids: Structures, Properties, and Functions , 2000 .

[6]  A. Moya,et al.  Genetic lesions associated with Muller's ratchet in an RNA virus. , 1996, Journal of molecular biology.

[7]  M. Eigen,et al.  Kinetics of RNA replication: competition and selection among self-replicating RNA species. , 1985, Biochemistry.

[8]  S. Elena,et al.  Exponential increases of RNA virus fitness during large population transmissions. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[9]  E. Domingo,et al.  Virus mutation frequencies can be greatly underestimated by monoclonal antibody neutralization of virions , 1989, Journal of virology.

[10]  G. Cowan,et al.  Complexity Metaphors, Models, and Reality , 1994 .

[11]  Claus O. Wilke,et al.  Dynamic fitness landscapes in molecular evolution , 1999, physics/9912012.

[12]  M. Eigen,et al.  Molecular quasi-species. , 1988 .

[13]  John Maynard Smith,et al.  Natural Selection and the Concept of a Protein Space , 1970, Nature.

[14]  E. Domingo,et al.  Systematic Replacement of Amino Acid Residues within an Arg-Gly-Asp-containing Loop of Foot-and-Mouth Disease Virus and Effect on Cell Recognition* , 1996, The Journal of Biological Chemistry.

[15]  E. Domingo,et al.  Evolution of Cell Recognition by Viruses , 2001, Science.

[16]  Miguel Ángel Martínez,et al.  A single amino acid substitution affects multiple overlapping epitopes in the major antigenic site of foot-and-mouth disease virus of serotype C. , 1990, The Journal of general virology.

[17]  E. Domingo,et al.  Multiple molecular pathways for fitness recovery of an RNA virus debilitated by operation of Muller's ratchet. , 1999, Journal of molecular biology.

[18]  E. Domingo,et al.  Multiple genetic variants arise in the course of replication of foot-and-mouth disease virus in cell culture. , 1983, Virology.

[19]  E. Domingo,et al.  Duration and fitness dependence of quasispecies memory. , 2002, Journal of molecular biology.

[20]  E. Domingo,et al.  Evolution of Cell Recognition by Viruses: A Source of Biological Novelty with Medical Implications , 2003, Advances in Virus Research.

[21]  E. Domingo,et al.  Detection and Biological Implications of Genetic Memory in Viral Quasispecies , 2003 .

[22]  J. Valcárcel,et al.  Phenotypic hiding: the carryover of mutations in RNA viruses as shown by detection of mar mutants in influenza virus , 1989, Journal of virology.

[23]  J. Wixted,et al.  Genuine power curves in forgetting: A quantitative analysis of individual subject forgetting functions , 1997, Memory & cognition.

[24]  C. Wilke,et al.  Phenotypic mixing and hiding may contribute to memory in viral quasispecies. , 2003, BMC microbiology.

[25]  E. Domingo,et al.  Resistance to extinction of low fitness virus subjected to plaque-to-plaque transfers: diversification by mutation clustering. , 2002, Journal of molecular biology.

[26]  A. King,et al.  Structure and receptor binding. , 2003, Virus research.

[27]  J. Drake,et al.  Mutation rates among RNA viruses. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[28]  E. Domingo,et al.  Modeling Viral Genome Fitness Evolution Associated with Serial Bottleneck Events: Evidence of Stationary States of Fitness , 2002, Journal of Virology.

[29]  E. Domingo,et al.  Molecular intermediates of fitness gain of an RNA virus: characterization of a mutant spectrum by biological and molecular cloning. , 2001, The Journal of general virology.

[30]  M. Eigen,et al.  Natural selection: a phase transition? , 2000, Biophysical chemistry.

[31]  A. Rodrigo,et al.  Transition between Stochastic Evolution and Deterministic Evolution in the Presence of Selection: General Theory and Application to Virology , 2001, Microbiology and Molecular Biology Reviews.

[32]  Miguel Ángel Martínez,et al.  Implications of a quasispecies genome structure: effect of frequent, naturally occurring amino acid substitutions on the antigenicity of foot-and-mouth disease virus. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Richard W. Hamming,et al.  Coding and Information Theory , 2018, Feynman Lectures on Computation.

[34]  D. Stuart,et al.  The structure and antigenicity of a type C foot-and-mouth disease virus. , 1994, Structure.

[35]  M. Eigen,et al.  The Hypercycle: A principle of natural self-organization , 2009 .

[36]  Ingo Rechenberg,et al.  Evolutionsstrategie : Optimierung technischer Systeme nach Prinzipien der biologischen Evolution , 1973 .

[37]  E. Domingo,et al.  Memory in Viral Quasispecies , 2000, Journal of Virology.

[38]  Carmen Molina-París,et al.  Memory in Retroviral Quasispecies: Experimental Evidence and Theoretical Model for Human Immunodeficiency Virus , 2003, Journal of Molecular Biology.

[39]  M. G. Mateu,et al.  Antibody recognition of picornaviruses and escape from neutralization: a structural view. , 1995, Virus research.

[40]  D. Sheppard,et al.  The Epithelial Integrin αvβ6 Is a Receptor for Foot-and-Mouth Disease Virus , 2000, Journal of Virology.

[41]  E. Domingo,et al.  Evolution subverting essentiality: dispensability of the cell attachment Arg-Gly-Asp motif in multiply passaged foot-and-mouth disease virus. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[42]  E. Domingo,et al.  Resistance of virus to extinction on bottleneck passages: Study of a decaying and fluctuating pattern of fitness loss , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[43]  E. Domingo,et al.  Origin and Evolution of Viruses , 2010, Virus Genes.

[44]  E. Domingo,et al.  Multiple Virulence Determinants of Foot-and-Mouth Disease Virus in Cell Culture , 1998, Journal of Virology.

[45]  E. Domingo,et al.  Cell Recognition by Foot-and-Mouth Disease Virus That Lacks the RGD Integrin-Binding Motif: Flexibility in Aphthovirus Receptor Usage , 2000, Journal of Virology.

[46]  David Gray,et al.  Immunological Memory and Protective Immunity: Understanding Their Relation , 1996, Science.

[47]  E. Domingo,et al.  A Similar Pattern of Interaction for Different Antibodies with a Major Antigenic Site of Foot-and-Mouth Disease Virus: Implications for Intratypic Antigenic Variation , 1998, Journal of Virology.

[48]  E. Domingo,et al.  Structure of the major antigenic loop of foot‐and‐mouth disease virus complexed with a neutralizing antibody: direct involvement of the Arg‐Gly‐Asp motif in the interaction. , 1995, The EMBO journal.

[49]  E. Domingo,et al.  Fitness distributions in exponentially growing asexual populations. , 2003, Physical review letters.

[50]  R. Shepard,et al.  Toward a universal law of generalization for psychological science. , 1987, Science.

[51]  John E. R. Staddon Adaptive Dynamics: The Theoretical Analysis of Behavior , 2001 .

[52]  E. Batschelet,et al.  The proportion of revertant and mutant phage in a growing population, as a function of mutation and growth rate. , 1976, Gene.

[53]  D. Stuart,et al.  Efficient infection of cells in culture by type O foot-and-mouth disease virus requires binding to cell surface heparan sulfate , 1996, Journal of virology.

[54]  C. Ofria,et al.  Evolution of digital organisms at high mutation rates leads to survival of the flattest , 2001, Nature.

[55]  Murray Gell-Mann,et al.  Complex adaptive systems , 1999 .

[56]  E. Domingo,et al.  Contingent Neutrality in Competing Viral Populations , 2001, Journal of Virology.

[57]  P. Mason,et al.  Antibodies to the vitronectin receptor (integrin alpha V beta 3) inhibit binding and infection of foot-and-mouth disease virus to cultured cells , 1995, Journal of virology.

[58]  P. Mason,et al.  Foot-and-Mouth Disease Virus Virulent for Cattle Utilizes the Integrin αvβ3 as Its Receptor , 1998, Journal of Virology.

[59]  M. Eigen Selforganization of matter and the evolution of biological macromolecules , 1971, Naturwissenschaften.

[60]  S. Grossberg,et al.  The Adaptive Brain , 1990 .

[61]  E. Domingo,et al.  Long-term, large-population passage of aphthovirus can generate and amplify defective noninterfering particles deleted in the leader protease gene. , 1996, Virology.