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Enhanced UV resistance and improved killing of malaria mosquitoes by photolyase transgenic entomopathogenic fungi.

ABSTRACT: The low survival of microbial pest control agents exposed to UV is the major environmental factor limiting their effectiveness. Using gene disruption we demonstrated that the insect pathogenic fungus Metarhizium robertsii uses photolyases to remove UV-induced cyclobutane pyrimidine dimers (CPD) and pyrimidine (6-4) photoproducts [(6-4)PPs] from its DNA. However, this photorepair is insufficient to fix CPD lesions and prevent the loss of viability caused by seven hours of solar radiation. Expression of a highly efficient archaeal (Halobacterium salinarum) CPD photolyase increased photorepair >30-fold in both M. robertsii and Beauveria bassiana. Consequently, transgenic strains were much more resistant to sunlight and retained virulence against the malaria vector Anopheles gambiae. In the field this will translate into much more efficient pest control over a longer time period. Conversely, our data shows that deleting native photolyase genes will strictly contain M. robertsii to areas protected from sunlight, alleviating safety concerns that transgenic hypervirulent Metarhizium spp will spread from mosquito traps or houses. The precision and malleability of the native and transgenic photolyases allows design of multiple pathogens with different strategies based on the environments in which they will be used.

SUBMITTER: Fang W

PROVIDER: S-EPMC3422317 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Enhanced UV resistance and improved killing of malaria mosquitoes by photolyase transgenic entomopathogenic fungi.

Fang Weiguo W St Leger Raymond J RJ

PloS one 20120817 8

The low survival of microbial pest control agents exposed to UV is the major environmental factor limiting their effectiveness. Using gene disruption we demonstrated that the insect pathogenic fungus Metarhizium robertsii uses photolyases to remove UV-induced cyclobutane pyrimidine dimers (CPD) and pyrimidine (6-4) photoproducts [(6-4)PPs] from its DNA. However, this photorepair is insufficient to fix CPD lesions and prevent the loss of viability caused by seven hours of solar radiation. Express ...[more]

PMID: 22912789

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Project description:Although entomopathogenic fungi (EPF) are best known for their ability to protect crops against insect pests, they may have other beneficial effects on their host plants. These effects, which include promoting plant growth and conferring resistance against abiotic stresses, have been examined in recent years to acquire a better understanding of them. The primary purposes of the present study were (i) to ascertain in vitro whether three different strains of EPF (viz., Metarhizium, Beauveria and Isaria) would increase the Fe bioavailability in calcareous or non-calcareous media containing various Fe sources (ferrihydrite, hematite and goethite) and (ii) to assess the influence of the EPF inoculation method (seed dressing, soil treatment or leaf spraying) on the extent of the endophytic colonization of sorghum and the improvement in the Fe nutrition of pot-grown sorghum plants on an artificial calcareous substrate. All the EPFs studied were found to increase the Fe availability during the in vitro assay. The most efficient EPF was M. brunneum EAMa 01/58-Su, which lowered the pH of the calcareous medium, suggesting that it used a different strategy (organic acid release) than the other two fungi that raised the pH of the non-calcareous medium. The three methods used to inoculate sorghum plants with B. bassiana and M. brunneum in the pot experiment led to differences in re-isolation from plant tissues and in the plant height. These three inoculation methods increased the leaf chlorophyll content of young leaves when the Fe deficiency symptoms were most apparent in the control plants (without fungal inoculation) as well as the Fe content of the above-ground biomass in the plants at the end of the experiment. The total root lengths and fine roots were also increased in response to fungal applications with the three inoculation methods. However, the soil treatment was the most efficient method; thus, its effect on the leaf chlorophyll content was the most persistent, and the effects on the total root length and fine roots were the most apparent. In conclusion, EPF improved the Fe nutrition of the sorghum plants, but their effects depended on the inoculation method.

Project description:BackgroundChemical insecticides against adult mosquitoes are a key element in most malaria management programmes, but their efficacy is threatened by the evolution of insecticide-resistant mosquitoes. By killing only older mosquitoes, entomopathogenic fungi can in principle significantly impact parasite transmission while imposing much less selection for resistance. Here an assessment is made as to which of the wide range of possible virulence characteristics for fungal biopesticides best realise this potential.MethodsWith mathematical models that capture relevant timings and survival probabilities within successive feeding cycles, transmission and resistance-management metrics are used to compare susceptible and resistant mosquitoes exposed to no intervention, to conventional instant-kill interventions, and to delayed-action biopesticides with a wide range of virulence characteristics.ResultsFungal biopesticides that generate high rates of mortality at around the time mosquitoes first become able to transmit the malaria parasite offer potential for large reductions in transmission while imposing low fitness costs. The best combinations of control and resistance management are generally accessed at high levels of coverage. Strains which have high virulence in malaria-infected mosquitoes but lower virulence in malaria-free mosquitoes offer the ultimate benefit in terms of minimizing selection pressure whilst maximizing impact on transmission. Exploiting this phenotype should be a target for product development. For indoor residual spray programmes, biopesticides may offer substantial advantages over the widely used pyrethroid-based insecticides. Not only do fungal biopesticides provide substantial resistance management gains in the long term, they may also provide greater reductions in transmission before resistance has evolved. This is because fungal spores do not have contact irritancy, reducing the chances that a blood-fed mosquito can survive an encounter and thus live long enough to transmit malaria.ConclusionsDelayed-action products, such as fungal biopesticides, have the potential to achieve reductions in transmission comparable with those achieved with existing instant-kill insecticides, and to sustain this control for substantially longer once resistant alleles arise. Given the current insecticide resistance crisis, efforts should continue to fully explore the operational feasibility of this alternative approach.

Dataset Information

Enhanced UV resistance and improved killing of malaria mosquitoes by photolyase transgenic entomopathogenic fungi.

Publications

Enhanced UV resistance and improved killing of malaria mosquitoes by photolyase transgenic entomopathogenic fungi.

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