Defective or effective? Mutualistic interactions between virus genotypes

López‐Ferber, M.; Simón, Oihane; Williams, Trevor; Caballero, Primitivo

doi:10.1098/rspb.2003.2498

Cited by 107 publications

(110 citation statements)

References 36 publications

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“…Even defective viruses, which often reduce the virulence of the virus population (e.g. Muñoz et al, 1998;Zwart et al, 2008), in some particular instances increase the virulence of the population when co-infecting with a helper virus (Lopez-Ferber et al, 2003;Lauzon et al, 2005). Here, however, we have identified a case were genetic heterogeneity is inversely correlated with disease outbreaks.…”

contrasting

confidence: 45%

Mixed-genotype white spot syndrome virus infections of shrimp are inversely correlated with disease outbreaks in ponds

Hoa

Zwart

Phượng

et al. 2010

Journal of General Virology

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Outbreaks of white spot syndrome virus (WSSV) in shrimp culture and the relationship between the virus and virulence are not well understood. Here, we provide evidence showing that WSSV mixed-genotype infections correlate with lower outbreak incidence and that disease outbreaks correlate with single-genotype infections. We tested 573 shrimp samples from 81 shrimp ponds in the Mekong delta with outbreak or non-outbreak status. The variable number tandem repeat (VNTR) loci of WSSV were used as molecular markers for the characterization of single-and mixed-genotype infections. The overall prevalence of mixed-genotype WSSV infections was 25.7 %. Non-outbreak ponds had a significantly higher frequency of mixed-genotype infections than outbreak ponds for all VNTR loci, both at the individual shrimp as well as at the pond level. The genetic composition of WSSV populations appears to correlate with the health status of shrimp culture in ponds. The causal relationship between genotypic diversity and disease outbreaks can now be experimentally approached.

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contrasting

confidence: 45%

Mixed-genotype white spot syndrome virus infections of shrimp are inversely correlated with disease outbreaks in ponds

Hoa

Zwart

Phượng

et al. 2010

Journal of General Virology

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“…One proposal is that genome segmentation evolved in response to high mutation rates to provide multicomponent reproduction as a form of sex to attenuate the effect of deleterious mutations (5,31). In this respect, it has been recently reported that genomes of nucleopolyhedrovirus with deletions can work with full-length partners to mutual benefit, possibly through complementation (19). Another proposal is that segmentation could result from selection of shorter RNA molecules that replicate faster than the corresponding parental genome, favored at high MOIs to ensure efficient complementation (25,40).…”

Section: Discussionmentioning

confidence: 99%

Evolutionary Transition toward Defective RNAs That Are Infectious by Complementation

García-Arriaza

Manrubia

Toja

et al. 2004

J Virol

155

201

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Passage of foot-and-mouth disease virus (FMDV) in cell culture resulted in the generation of defective RNAs that were infectious by complementation. Deletions (of nucleotides 417, 999, and 1017) mapped in the L proteinase and capsid protein-coding regions. Cell killing followed two-hit kinetics, defective genomes were encapsidated into separate viral particles, and individual viral plaques contained defective genomes with no detectable standard FMDV RNA. Infection in the absence of standard FMDV RNA was achieved by cotransfection of susceptible cells with transcripts produced in vitro from plasmids encoding the defective genomes. These results document the first step of an evolutionary transition toward genome segmentation of an unsegmented RNA virus and provide an experimental system to compare rates of RNA progeny production and resistance to enhanced mutagenesis of a segmented genome versus its unsegmented counterpart.Mutation, recombination, and ensuing phenotypic modifications in response to selective pressures can be readily observed and quantitated with RNA viruses both in cell culture and in vivo within modest time periods. This has rendered viruses suitable experimental systems for studies of basic Darwinian processes of genetic modification, competition, and selection or random drift as agents of genome diversification and biological adaptation (reviewed in references 1, 8, and 12). However, some major evolutionary transitions such as RNA genome segmentation have never been observed in the laboratory, yet they have probably occurred, given the hundreds of animal, plant, bacterial, and fungal viruses with segmented RNA genomes that have been described, including picornavirus-like plant RNA viruses (43). We have carried out extensive studies on the population dynamics of the important animal picornavirus foot-and-mouth disease virus (FMDV), including that of phenotypic evolution upon long-term serial cytopathic infections of BHK-21 cells (2). Unexpectedly, after more than 200 serial infections of viral population C-S8c1 of FMDV (a clone of serotype C [reviewed in reference 33]), defective genomes became dominant in the population. Defective interfering (DI) particles are frequently produced upon passage of RNA viruses at a high multiplicity of infection (MOI). DI particles are deletion mutants that require the presence of helper virus for replication and can interfere with the replication of the standard infectious virus (14-16, 29, 32, 35). The results described here show that defective genomes which individually could not cause cytopathology could nevertheless complement each other to produce progeny and kill cells in the absence of standard virus. The results provide, to our knowledge, the first description of defective RNA genomes occurring during viral replication that can be stably maintained by complementation upon passage at a high MOI in the absence of standard infectious virus. Therefore, the results provide experimental evidence of the initial step of an evolutionary transition towards genome ...

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“…However, pif1-and pif2-defective genotypes can replicate autonomously in cell culture or in larvae, if injected. Remarkably, the progeny viruses from insects that had been simultaneously inoculated with a mixture of complete and deletion genotypes, in a ratio similar to that found in nature (ϳ3:1), were ϳ2.5 times more pathogenic, as indicated by concentration-mortality metrics, than the complete genotype alone (28,38,39). Whether the increased pathogenicity of mixed genotype inocula was specifically due to the deletion has remained unclear and identifying the gene(s) involved represents a key to our understanding of baculovirus infection strategies.…”

mentioning

confidence: 95%

“…Primers were designed to differentiate between genotype SfNIC-B (amplicon of ϳ750 bp) and the recombinant genotypes SfNIC-B⌬16K (amplicon of 1,076 bp) and SfNIC-B⌬pifs (amplicon of 868 bp) (B-pif2fw, Sfpif.4, and Sf100a; Table 1). Reactions were stopped at the mid-logarithmic phase of amplification (19 cycles), since a series of amplifications involving different numbers of cycles indicated that this was the mid-logarithmic phase for the amplification of this product, as described in previous studies (28,40,41). The intensities of PCR products were determined relative to the SfNIC-B internal standard by using the ChemiDoC densitometric analysis software (Bio-Rad, Hercules, CA).…”

Section: Methodsmentioning

confidence: 99%

“…Pathogenicity of single and mixed genotype OBs. Purified OB suspensions containing 5 ϫ 10 8 OBs/ml of the SfNIC-B isolate and the SfNIC-B⌬16K and SfNIC-B⌬pifs recombinant viruses were mixed in the desired proportions, comprising 10, 25, 50, 75, or 90% SfNIC-B and the corresponding percentage of recombinant OBs, as previously described (28). OB mixtures were solubilized and 8-l volumes of the released ODVs were injected into S. frugiperda fourth instars that were incubated individually on semisynthetic diet until death.…”

Section: Methodsmentioning

confidence: 99%

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Mixtures of Complete andpif1- andpif2-Deficient Genotypes Are Required for Increased Potency of an Insect Nucleopolyhedrovirus

Clavijo

Williams

Simón

et al. 2009

J Virol

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The insecticidal potency of a nucleopolyhedrovirus population (SfNIC) that infects Spodoptera frugiperda (Lepidoptera) is greater than the potency of any of the component genotypes alone. Occlusion bodies (OBs) produced in mixed infections comprising the complete genotype and a deletion genotype are as pathogenic as the natural population of genotypes from the field. To test whether this increased potency was due to the deletion or to some other characteristic of the deletion variant genome, we used the SfNIC-B genome to construct a recombinant virus (SfNIC-B⌬16K) with the same 16.4-kb deletion as that observed in SfNIC-C and another recombinant (SfNIC-B⌬pifs) with a deletion encompassing two adjacent genes (pif1 and pif2) that are essential for transmission per os. Mixtures comprising SfNIC-B and SfNIC-B⌬16K in OB ratios that varied between 10:90 and 90:10 were injected into insects, and the progeny OBs were fed to larvae in an insecticidal potency assay. A densitometric analysis of PCR products indicated that SfNIC-B was generally more abundant than expected in mixtures based on the proportions of OBs used to produce the inocula. Mixtures derived from OB ratios of 10, 25, or 50% of SfNIC-B⌬16K and the corresponding SfNIC-B proportions showed a significant increase in potency compared to SfNIC-B alone. The results of potency assays with mixtures comprising various proportions of SfNIC-B plus SfNIC-B⌬pifs were almost identical to the results observed with SfNIC-B⌬16K, indicating that deletion of the pif gene region was responsible for the increased potency observed in mixtures of SfNIC-B and each deletion recombinant virus. Subsequently, mixtures produced from OB ratios involving 10 or 90% of SfNIC-B⌬16K with the corresponding proportions of SfNIC-B were subjected to four rounds of per os transmission in larvae. The composition of each experimental mixture rapidly converged to a common equilibrium with a genotypic composition of ϳ85% SfNIC-B plus ϳ15% SfNIC-B⌬16K. Nearly identical results were observed in peroral-passage experiments involving mixtures of SfNIC-B plus SfNICB⌬pifs. We conclude that (i) the deletion of the pif1 and pif2 region is necessary and sufficient to explain the increased potency observed in mixtures of complete and deletion genotypes and (ii) viral populations with decreased ratios of pif1-and pif2-deficient genotypes in the virus population increase the potency of genotypic mixtures and are likely to positively influence the transmission of this pathogen.

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Defective or effective? Mutualistic interactions between virus genotypes

Cited by 107 publications

References 36 publications

Mixed-genotype white spot syndrome virus infections of shrimp are inversely correlated with disease outbreaks in ponds

Mixed-genotype white spot syndrome virus infections of shrimp are inversely correlated with disease outbreaks in ponds

Evolutionary Transition toward Defective RNAs That Are Infectious by Complementation

Mixtures of Complete andpif1- andpif2-Deficient Genotypes Are Required for Increased Potency of an Insect Nucleopolyhedrovirus

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