The Strange Lifestyle of Multipartite Viruses

Sicard, Anne; Michalakis, Yannis; Gutiérrez, Serafín; Blanc, Stéphane

doi:10.1371/journal.ppat.1005819

Cited by 101 publications

(137 citation statements)

References 103 publications

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“…Variation in gene expression potential at the population level may also facilitate selective regulation of viral gene expression through gene dosing effects, as has been demonstrated for multipartite plant viruses (104,105). Changes in the percentage of particles that carry a functional copy of a given IAV genome segment will alter the stoichiometry of gene segments delivered to multiply infected cells.…”

Section: Effects Of Sips On Population-level Phenotypesmentioning

confidence: 99%

Population Diversity and Collective Interactions during Influenza Virus Infection

Brooke

2017

J Virol

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Influenza A virus (IAV) continues to pose an enormous and unpredictable global public health threat, largely due to the continual evolution of escape from preexisting immunity and the potential for zoonotic emergence. Understanding how the unique genetic makeup and structure of IAV populations influences their transmission and evolution is essential for developing more-effective vaccines, therapeutics, and surveillance capabilities. Owing to their mutation-prone replicase and unique genome organization, IAV populations exhibit enormous amounts of diversity both in terms of sequence and functional gene content. Here, I review what is currently known about the genetic and genomic diversity present within IAV populations and how this diversity may shape the replicative and evolutionary dynamics of these viruses.

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Section: Effects Of Sips On Population-level Phenotypesmentioning

confidence: 99%

Population Diversity and Collective Interactions during Influenza Virus Infection

Brooke

2017

J Virol

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“…A recent study showed that these different genomic segments consistently accumulate at different relative frequencies in the host plant, defining the genome formula (28). It has been hypothesized that the genome formula could correspond to a gene expression regulation system through the modification of the gene copy number (29). The multipartite structure of the FBNSV genome, the fact that its segments are of similar sizes and share common sequences, and the obvious importance of the genome formula make FBNSV a great model to investigate potential quantitative NGS biases at the intraspecific level.…”

Section: Importancementioning

confidence: 99%

The Number of Target Molecules of the Amplification Step Limits Accuracy and Sensitivity in Ultradeep-Sequencing Viral Population Studies

Gallet

Fabre

Michalakis

et al. 2017

J Virol

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The invention of next-generation sequencing (NGS) techniques marked the coming of a new era in the detection of the genetic diversity of intrahost viral populations. A good understanding of the genetic structure of these populations requires, first, the ability to identify the different isolates or variants and, second, the ability to accurately quantify them. However, the initial amplification step of NGS studies can impose potential quantitative biases, modifying the variant relative frequencies. In particular, the number of target molecules (NTM) used during the amplification step is vastly overlooked although of primary importance, as it sets the limit of the accuracy and sensitivity of the sequencing procedure. In the present article, we investigated quantitative biases in an NGS study of populations of a multipartite single-stranded DNA (ssDNA) virus at different steps of the procedure. We studied 20 independent populations of the ssDNA virus faba bean necrotic stunt virus (FBNSV) in two host plants, Vicia faba and Medicago truncatula. FBNSV is a multipartite virus composed of eight genomic segments, whose specific and hostdependent relative frequencies are defined as the "genome formula." Our results show a significant distortion of the FBNSV genome formula after the amplification and sequencing steps. We also quantified the genetic bottleneck occurring at the amplification step by documenting the NTM of two genomic segments of FBNSV. We argue that the NTM must be documented and carefully considered when determining the sensitivity and accuracy of data from NGS studies.IMPORTANCE The advent of next-generation sequencing (NGS) techniques now enables study of the genetic diversity of viral populations. A good understanding of the genetic structure of these populations first requires the ability to identify the different isolates or variants and second requires the ability to accurately quantify them. Prior to sequencing, viral genomes need to be amplified, a step that potentially imposes quantitative biases and modifies the viral population structure. In particular, the number of target molecules (NTM) used during the amplification step is of primary importance, as it sets the limit of the accuracy and sensitivity of the sequencing procedure. In this work, we used 20 replicated populations of the multipartite faba bean necrotic stunt virus (FBNSV) to estimate the various limitations of ultradeep-sequencing studies performed on intrahost viral populations. We report quantitative biases during rolling-circle amplification and the NTM of two genomic segments of FBNSV.KEYWORDS DNA sequencing, FBNSV, faba bean, Medicago truncatula, nextgeneration sequencing, number of target molecules, rolling-circle amplification, sequencing accuracy, sequencing sensitivity

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“…These viruses, first described in the 1960s [1], have a genome segmented in two or more parts. According to current evidence, the segments are encapsidated separately and, apparently, propagate independently [2,3]. As of today, there is no mainstream theory able to explain the adaptive advantage of such a strange lifestyle [4].…”

Section: Introductionmentioning

confidence: 99%

Endemicity and prevalence of multipartite viruses under heterogeneous between-host transmission

Valdano

Manrubia²,

Gómez

et al. 2019

PLoS Comput Biol

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Multipartite viruses replicate through a puzzling evolutionary strategy. Their genome is segmented into two or more parts, and encapsidated in separate particles that appear to propagate independently. Completing the replication cycle, however, requires the full genome, so that a systemic infection of a host requires the concurrent presence of several particles. This represents an apparent evolutionary drawback of multipartitism, while its advantages remain unclear. A transition from monopartite to multipartite viral forms has been described in vitro under conditions of high multiplicity of infection, suggesting that cooperation between defective mutants is a plausible evolutionary pathway towards multipartitism. However, it is unknown how the putative advantages that multipartitism might enjoy at the microscopic level affect its epidemiology, or if an explicit advantange is needed to explain its ecological persistence. In order to disentangle which mechanisms might contribute to the rise and fixation of multipartitism, we here investigate the interaction between viral spreading dynamics and host population structure. We set up a compartmental model of the spread of a virus in its different forms and explore its epidemiology using both analytical and numerical techniques. We uncover that the impact of host contact structure on spreading dynamics entails a rich phenomenology of ecological relationships that includes cooperation, competition, and commensality. Furthermore, we find out that multipartitism might rise to fixation even in the absence of explicit microscopic advantages. Multipartitism allows the virus to colonize environments that could not be invaded by the monopartite form, while homogeneous contacts between hosts facilitate its spread. We conjecture that these features might have led to an increase in the diversity and prevalence of multipartite viral forms concomitantly with the expansion of agricultural practices.

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The Strange Lifestyle of Multipartite Viruses

Cited by 101 publications

References 103 publications

Population Diversity and Collective Interactions during Influenza Virus Infection

Population Diversity and Collective Interactions during Influenza Virus Infection

The Number of Target Molecules of the Amplification Step Limits Accuracy and Sensitivity in Ultradeep-Sequencing Viral Population Studies

Endemicity and prevalence of multipartite viruses under heterogeneous between-host transmission

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