Control of Pyrethroid-Resistant Chagas Disease Vectors with Entomopathogenic Fungi

Abstract

Background Triatoma infestans-mediated transmission of Tripanosoma cruzi, the causative agent of Chagas disease, remains as a major health issue in southern South America. Key factors of T. infestans prevalence in specific areas of the geographic Gran Chaco region—which extends through northern Argentina, Bolivia, and Paraguay—are both recurrent reinfestations after insecticide spraying and emerging pyrethroid-resistance over the past ten years. Among alternative control tools, the pathogenicity of entomopathogenic fungi against triatomines is already known; furthermore, these fungi have the ability to fully degrade hydrocarbons from T. infestans cuticle and to utilize them as fuel and for incorporation into cellular components.Methodology and FindingsHere we provide evidence of resistance-related cuticle differences; capillary gas chromatography coupled to mass spectrometry analyses revealed that pyrethroid-resistant bugs have significantly larger amounts of surface hydrocarbons, peaking 56.2±6.4% higher than susceptible specimens. Also, a thicker cuticle was detected by scanning electron microscopy (32.1±5.9 µm and 17.8±5.4 µm for pyrethroid-resistant and pyrethroid-susceptible, respectively). In laboratory bioassays, we showed that the virulence of the entomopathogenic fungi Beauveria bassiana against T. infestans was significantly enhanced after fungal adaptation to grow on a medium containing insect-like hydrocarbons as the carbon source, regardless of bug susceptibility to pyrethroids. We designed an attraction-infection trap based on manipulating T. infestans behavior in order to facilitate close contact with B. bassiana. Field assays performed in rural village houses infested with pyrethroid-resistant insects showed 52.4% bug mortality. Using available mathematical models, we predicted that further fungal applications could eventually halt infection transmission.ConclusionsThis low cost, low tech, ecologically friendly methodology could help in controlling the spread of pyrethroid-resistant bugs.

CYP52X1, Representing New Cytochrome P450 Subfamily, Displays Fatty Acid Hydroxylase Activity and Contributes to Virulence and Growth on Insect Cuticular Substrates in Entomopathogenic Fungus Beauveria bassiana

“…CYP52X1 displayed robust activity (Ͼ40 pmol/min/mg of protein) against lauric (C12:0), myristic, and 10-epoxysteric acids, 2-10 pmol/min/mg of protein of activity against C(9:0), C(16:0), C(18:1), and C(18:2), and ϳ 0.5 pmol/min/mg protein of activity against C18:0. These data indicate that the enzyme prefers the mid-range (possibly C 10 -11 , C [12][13][14] , and possibly C 15 ) saturated fatty acids. Intriguingly, the enzyme displayed better activity toward unsaturated and epoxy-C 18 fatty acids than toward the saturated C 18 fatty acid.…”

“…Hydrocarbon assimilation plays a critical role in the ability of B. bassiana to infect certain insects, and alkane growth has been linked to increased virulence. Fungal cells grown on alkane-containing media displayed a 2-4-fold increase in mortality against the bean weevil Acanthoscelides obtectus when compared with cells grown on glucose (11), and derepression of the alkane pathway increased fungal virulence against insects that had developed resistance to chemical pesticides (12).…”

Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen

“…Several isolates of the Ascomycetes Beauveria bassiana and Metarhizium anisopliae have been successfully used worldwide to control insects of both agricultural and medical importance (16)(17)(18)(19). B. bassiana is known as a broad host range arthropod pathogen capable of infecting a wide range of target hosts.…”

History of insecticide resistance of Triatominae vectors

“…The authors found that recently hatched fi rst instar nymphs (1-3h old) were more vulnerable than older ones (24-36h old). Pedrini et al (65) used scanning electronic microscopy to show that Argentinean populations of T. infestans resistant to deltamethrin have thicker exoskeletons (32.1 ± 5.9μm) than susceptible populations (17.8 ± 5.4μm). Thicker cuticles enriched in hydrocarbons probably restrict deltamethrin penetration in resistant insects.…”