TY - JOUR

T1 - Involvement of bacteria in the development of fungal infections in the Colorado potato beetle

AU - Kryukov, Vadim Yu

AU - Kosman, Elena

AU - Slepneva, Irina

AU - Vorontsova, Yana L.

AU - Polenogova, Olga

AU - Kazymov, Gleb

AU - Alikina, Tatyana

AU - Akhanaev, Yuriy

AU - Sidorenko, Darya

AU - Noskov, Yury A.

AU - Krivopalov, Anton

AU - Kabilov, Marsel R.

AU - Yaroslavtseva, Olga

N1 - The study was initiated within the framework of support from the Russian Science Foundation (No. 20-74-10043) and continued with the same funding (No. 22-14-00309).

PY - 2024/7/10

Y1 - 2024/7/10

N2 - Entomopathogenic fungi may interact with insects’ symbiotic bacteria during infection. We hypothesized that topical infection with Beauveria bassiana may alter the microbiota of the Colorado potato beetle (CPB) and that these modifications may alter the course of mycoses. We used a model with two concentrations of conidia: (1) high concentration that causes rapid (acute) pathogenesis with fast mortality followed by bacterial decomposition of insects; (2) lower concentration that leads to prolonged pathogenesis ending in conidiation on cadavers. The fungal infections increased loads of enterobacteria and bacilli on the cuticle surface and in hemolymph and midgut, and the greatest increase was detected during the acute mycosis. By contrast, stronger activation of IMD and JAK–STAT signaling pathways in integuments and fat body was observed during the prolonged mycosis. Relatively stable (nonpathogenic) conditions remained in the midgut during both scenarios of mycosis with slight changes in bacterial communities, the absence of mesh and stat expression, a decrease in reactive oxygen species production, and slight induction of Toll and IMD pathways. Oral administration of antibiotic and predominant CPB bacteria (Enterobacteriaceae, Lactococcus, Pseudomonas) led to minor and mainly antagonistic effects in survival of larvae infected with B. bassiana. We believe that prolonged mycosis is necessary for successful development of the fungus because such pathogenesis allows the host to activate antibacterial reactions. Conversely, after infection with high concentrations of the fungus, the host's resources are insufficient to fully activate antibacterial defenses, and this situation makes successful development of the fungus impossible.

AB - Entomopathogenic fungi may interact with insects’ symbiotic bacteria during infection. We hypothesized that topical infection with Beauveria bassiana may alter the microbiota of the Colorado potato beetle (CPB) and that these modifications may alter the course of mycoses. We used a model with two concentrations of conidia: (1) high concentration that causes rapid (acute) pathogenesis with fast mortality followed by bacterial decomposition of insects; (2) lower concentration that leads to prolonged pathogenesis ending in conidiation on cadavers. The fungal infections increased loads of enterobacteria and bacilli on the cuticle surface and in hemolymph and midgut, and the greatest increase was detected during the acute mycosis. By contrast, stronger activation of IMD and JAK–STAT signaling pathways in integuments and fat body was observed during the prolonged mycosis. Relatively stable (nonpathogenic) conditions remained in the midgut during both scenarios of mycosis with slight changes in bacterial communities, the absence of mesh and stat expression, a decrease in reactive oxygen species production, and slight induction of Toll and IMD pathways. Oral administration of antibiotic and predominant CPB bacteria (Enterobacteriaceae, Lactococcus, Pseudomonas) led to minor and mainly antagonistic effects in survival of larvae infected with B. bassiana. We believe that prolonged mycosis is necessary for successful development of the fungus because such pathogenesis allows the host to activate antibacterial reactions. Conversely, after infection with high concentrations of the fungus, the host's resources are insufficient to fully activate antibacterial defenses, and this situation makes successful development of the fungus impossible.

KW - Beauveria bassiana

KW - IMD

KW - JAK-STAT

KW - gut

KW - integument

KW - microbiota

UR - https://www.scopus.com/record/display.uri?eid=2-s2.0-85197235582&origin=inward&txGid=22b96ee8b8d52121f7d196c975faac72

UR - https://www.webofscience.com/wos/woscc/full-record/WOS:001261131000001

UR - https://www.mendeley.com/catalogue/c9f48b1e-0a09-343f-af75-2602e8862019/

U2 - 10.1111/1744-7917.13414

DO - 10.1111/1744-7917.13414

M3 - Article

C2 - 38956988

JO - Insect Science

JF - Insect Science

SN - 1672-9609

ER -