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Expression of a peroral infection factor determines pathogenicity and population structure in an insect virus.

Simón O, Williams T, Cerutti M, Caballero P, López-Ferber M - PLoS ONE (2013)

Bottom Line: A Nicaraguan isolate of Spodoptera frugiperda multiple nucleopolyhedrovirus is being studied as a possible biological insecticide.Group success (transmission) depended on expression of pif1, but overexpression was prejudicial to group-specific transmissibility, both in terms of reduced pathogenicity and reduced production of virus progeny from each infected insect.These results offer a new and unexpected perspective on cooperative behavior between viral genomes in response to the abundance of an essential public good that is detrimental in excess.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Agrobiotecnología, Consejo Superior de Investigaciones Científicas-Gobierno de Navarra, Mutilva Baja, Navarra, Spain.

ABSTRACT
A Nicaraguan isolate of Spodoptera frugiperda multiple nucleopolyhedrovirus is being studied as a possible biological insecticide. This virus exists as a mixture of complete and deletion genotypes; the latter depend on the former for the production of an essential per os transmission factor (pif1) in coinfected cells. We hypothesized that the virus population was structured to account for the prevalence of pif1 defector genotypes, so that increasing the abundance of pif1 produced by a cooperator genotype in infected cells would favor an increased prevalence of the defector genotype. We tested this hypothesis using recombinant viruses with pif1 expression reprogrammed at its native locus using two exogenous promoters (egt, p10) in the pif2/pif1 intergenic region. Reprogrammed viruses killed their hosts markedly faster than the wild-type and rescue viruses, possibly due to an earlier onset of systemic infection. Group success (transmission) depended on expression of pif1, but overexpression was prejudicial to group-specific transmissibility, both in terms of reduced pathogenicity and reduced production of virus progeny from each infected insect. The presence of pif1-overproducing genotypes in the population was predicted to favor a shift in the prevalence of defector genotypes lacking pif1-expressing capabilities, to compensate for the modification in pif1 availability at the population level. As a result, defectors increased the overall pathogenicity of the virus population by diluting pif1 produced by overexpressing genotypes. These results offer a new and unexpected perspective on cooperative behavior between viral genomes in response to the abundance of an essential public good that is detrimental in excess.

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DNA and genome content of Occlusion Bodies.A) Mean amounts of DNA (ng/µl) extracted from samples of 5×108 OBs of SfNIC-B, SfNIC-Bpif1, SfNIC-Begt and SfNIC-Bp10 viruses and determined by qPCR. Mean amounts of DNA from OB samples did not differ significantly between viruses (ANOVA, P = 0.401). B) ODV banding patterns of SfNIC-B, SfNIC-Bpif1, SfNIC-Begt and SfNIC-Bp10 viruses after sucrose-gradient separation of ODVs from similar quantities of occlusion bodies (5×108 OBs). Stars indicate the positions of the observed ODV bands. C) ODV content in 5×108 OBs of SfNIC-B, SfNIC-Bpif1, SfNIC-Begt and SfNIC-Bp10 viruses. Sf9 cells were infected with serial dilutions (1∶10, 1∶50, 1∶250, 1∶1250, 1∶6250) of ODVs released from OBs. ODV titers (ODV/ml) were calculated by end-point dilution. No significant differences were observed in the ODV content of OBs of the different viruses (ANOVA, P = 0.440).
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pone-0078834-g003: DNA and genome content of Occlusion Bodies.A) Mean amounts of DNA (ng/µl) extracted from samples of 5×108 OBs of SfNIC-B, SfNIC-Bpif1, SfNIC-Begt and SfNIC-Bp10 viruses and determined by qPCR. Mean amounts of DNA from OB samples did not differ significantly between viruses (ANOVA, P = 0.401). B) ODV banding patterns of SfNIC-B, SfNIC-Bpif1, SfNIC-Begt and SfNIC-Bp10 viruses after sucrose-gradient separation of ODVs from similar quantities of occlusion bodies (5×108 OBs). Stars indicate the positions of the observed ODV bands. C) ODV content in 5×108 OBs of SfNIC-B, SfNIC-Bpif1, SfNIC-Begt and SfNIC-Bp10 viruses. Sf9 cells were infected with serial dilutions (1∶10, 1∶50, 1∶250, 1∶1250, 1∶6250) of ODVs released from OBs. ODV titers (ODV/ml) were calculated by end-point dilution. No significant differences were observed in the ODV content of OBs of the different viruses (ANOVA, P = 0.440).

Mentions: Selected characteristics of OBs were determined in order to exclude them as a potential explanation for the observed differences in biological potencies of OBs among the pif1 reprogrammed and parental viruses. No significant differences were detected by qPCR in the mean amounts of DNA in samples of 5×108 OBs (F3,104 = 0.989, p = 0.401), suggesting similar numbers of genome copies in OBs of each of the different viruses (Fig. 3A). The efficiency of the qPCR technique was 99% (r2 = 0.9914). No gross differences were observed in the number of ODV bands or their intensity in samples originating from equal numbers of OBs of each of the viruses (Fig. 3B), indicating that these viruses did not differ appreciably in the distribution of numbers of nucleocapsids among ODVs. Finally, ODV titers from samples of 5×108 OBs were estimated by end-point dilution (Fig. 3C), and did not differ significantly between any of the viruses tested (F3,44 = 0.919, p = 0.440).


Expression of a peroral infection factor determines pathogenicity and population structure in an insect virus.

Simón O, Williams T, Cerutti M, Caballero P, López-Ferber M - PLoS ONE (2013)

DNA and genome content of Occlusion Bodies.A) Mean amounts of DNA (ng/µl) extracted from samples of 5×108 OBs of SfNIC-B, SfNIC-Bpif1, SfNIC-Begt and SfNIC-Bp10 viruses and determined by qPCR. Mean amounts of DNA from OB samples did not differ significantly between viruses (ANOVA, P = 0.401). B) ODV banding patterns of SfNIC-B, SfNIC-Bpif1, SfNIC-Begt and SfNIC-Bp10 viruses after sucrose-gradient separation of ODVs from similar quantities of occlusion bodies (5×108 OBs). Stars indicate the positions of the observed ODV bands. C) ODV content in 5×108 OBs of SfNIC-B, SfNIC-Bpif1, SfNIC-Begt and SfNIC-Bp10 viruses. Sf9 cells were infected with serial dilutions (1∶10, 1∶50, 1∶250, 1∶1250, 1∶6250) of ODVs released from OBs. ODV titers (ODV/ml) were calculated by end-point dilution. No significant differences were observed in the ODV content of OBs of the different viruses (ANOVA, P = 0.440).
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3818493&req=5

pone-0078834-g003: DNA and genome content of Occlusion Bodies.A) Mean amounts of DNA (ng/µl) extracted from samples of 5×108 OBs of SfNIC-B, SfNIC-Bpif1, SfNIC-Begt and SfNIC-Bp10 viruses and determined by qPCR. Mean amounts of DNA from OB samples did not differ significantly between viruses (ANOVA, P = 0.401). B) ODV banding patterns of SfNIC-B, SfNIC-Bpif1, SfNIC-Begt and SfNIC-Bp10 viruses after sucrose-gradient separation of ODVs from similar quantities of occlusion bodies (5×108 OBs). Stars indicate the positions of the observed ODV bands. C) ODV content in 5×108 OBs of SfNIC-B, SfNIC-Bpif1, SfNIC-Begt and SfNIC-Bp10 viruses. Sf9 cells were infected with serial dilutions (1∶10, 1∶50, 1∶250, 1∶1250, 1∶6250) of ODVs released from OBs. ODV titers (ODV/ml) were calculated by end-point dilution. No significant differences were observed in the ODV content of OBs of the different viruses (ANOVA, P = 0.440).
Mentions: Selected characteristics of OBs were determined in order to exclude them as a potential explanation for the observed differences in biological potencies of OBs among the pif1 reprogrammed and parental viruses. No significant differences were detected by qPCR in the mean amounts of DNA in samples of 5×108 OBs (F3,104 = 0.989, p = 0.401), suggesting similar numbers of genome copies in OBs of each of the different viruses (Fig. 3A). The efficiency of the qPCR technique was 99% (r2 = 0.9914). No gross differences were observed in the number of ODV bands or their intensity in samples originating from equal numbers of OBs of each of the viruses (Fig. 3B), indicating that these viruses did not differ appreciably in the distribution of numbers of nucleocapsids among ODVs. Finally, ODV titers from samples of 5×108 OBs were estimated by end-point dilution (Fig. 3C), and did not differ significantly between any of the viruses tested (F3,44 = 0.919, p = 0.440).

Bottom Line: A Nicaraguan isolate of Spodoptera frugiperda multiple nucleopolyhedrovirus is being studied as a possible biological insecticide.Group success (transmission) depended on expression of pif1, but overexpression was prejudicial to group-specific transmissibility, both in terms of reduced pathogenicity and reduced production of virus progeny from each infected insect.These results offer a new and unexpected perspective on cooperative behavior between viral genomes in response to the abundance of an essential public good that is detrimental in excess.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Agrobiotecnología, Consejo Superior de Investigaciones Científicas-Gobierno de Navarra, Mutilva Baja, Navarra, Spain.

ABSTRACT
A Nicaraguan isolate of Spodoptera frugiperda multiple nucleopolyhedrovirus is being studied as a possible biological insecticide. This virus exists as a mixture of complete and deletion genotypes; the latter depend on the former for the production of an essential per os transmission factor (pif1) in coinfected cells. We hypothesized that the virus population was structured to account for the prevalence of pif1 defector genotypes, so that increasing the abundance of pif1 produced by a cooperator genotype in infected cells would favor an increased prevalence of the defector genotype. We tested this hypothesis using recombinant viruses with pif1 expression reprogrammed at its native locus using two exogenous promoters (egt, p10) in the pif2/pif1 intergenic region. Reprogrammed viruses killed their hosts markedly faster than the wild-type and rescue viruses, possibly due to an earlier onset of systemic infection. Group success (transmission) depended on expression of pif1, but overexpression was prejudicial to group-specific transmissibility, both in terms of reduced pathogenicity and reduced production of virus progeny from each infected insect. The presence of pif1-overproducing genotypes in the population was predicted to favor a shift in the prevalence of defector genotypes lacking pif1-expressing capabilities, to compensate for the modification in pif1 availability at the population level. As a result, defectors increased the overall pathogenicity of the virus population by diluting pif1 produced by overexpressing genotypes. These results offer a new and unexpected perspective on cooperative behavior between viral genomes in response to the abundance of an essential public good that is detrimental in excess.

Show MeSH
Related in: MedlinePlus