A Neurotoxic Insecticide Promotes Fungal Infection in Aedes aegypti Larvae by Altering the Bacterial Community

Abstract

Symbiotic bacteria have a significant impact on the formation of defensive mechanisms against fungal pathogens and insecticides. The microbiome of the mosquito Aedes aegypti has been well studied; however, there are no data on the influence of insecticides and pathogenic fungi on its structure. The fungus Metarhizium robertsii and a neurotoxic insecticide (avermectin complex) interact synergistically, and the colonization of larvae with hyphal bodies is observed after fungal and combined (conidia + avermectins) treatments. The changes in the bacterial communities (16S rRNA) of Ae. aegypti larvae under the influence of fungal infection, avermectin toxicosis, and their combination were studied. In addition, we studied the interactions between the fungus and the predominant cultivable bacteria in vitro and in vivo after the coinfection of the larvae. Avermectins increased the total bacterial load and diversity. The fungus decreased the diversity and insignificantly increased the bacterial load. Importantly, avermectins reduced the relative abundance of Microbacterium (Actinobacteria), which exhibited a strong antagonistic effect towards the fungus in in vitro and in vivo assays. The avermectin treatment led to an increased abundance of Chryseobacterium (Flavobacteria), which exerted a neutral effect on mycosis development. In addition, avermectin treatment led to an elevation of some subdominant bacteria (Pseudomonas) that interacted synergistically with the fungus. We suggest that avermectins change the bacterial community to favor the development of fungal infection.

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Data Availability

The MiSeq data were deposited in GenBank under the study accession number PRJNA625381. The sequences of the 16S rDNA genes were deposited in the GenBank database under accession numbers MT040033–MT040053. Experimental data are presented in Appendix A.

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Acknowledgments

We are grateful to Dr. Vladimir A. Shilo (Karasuk biological station of ISEA SB RAS) for assisting in the experiments organization and Elena Balzovskaya for technical assistance. We also acknowledge Dr. Andrey A. Miller for preparation of ultrathin sections of mosquito larvae, Dr. Aleksandr A. Alekseev for determining the exact ratio of avermectins’ isomers in an industrial product Phytoverm using HPLC, and Daria Noskova for help in performing the experiments.

Funding

This work was supported by the Russian Science Foundation (project No. 18-74-00090). The maintenance of the mosquito line and microorganism collections at Institute of Systematics and Ecology of Animals SB RAS were supported by Federal Fundamental Scientific Research Programs (No. АААА-А16-116121410124-8 and No. АААА-А16-116121410123-1). A collection of extremophilic microorganisms and type cultures at Institute of Chemical Biology and Fundamental Medicine SB RAS was supported by the project АААА-А17-117020210027-9.

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Experimental design (VYK, VVG, YAN), performing the experiments (MRK, OVP, YAY, OEB, ONY, TYA, AMB, UNR, VVM), data analysis (VYK, YAN, MRK, UNR, VVM, AMB), writing the manuscript (YAN, VYK, MRK, OVP), and obtain funding (YAN, VVG, VVM).

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Correspondence to Y. A. Noskov.

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Noskov, Y.A., Kabilov, M.R., Polenogova, O.V. et al. A Neurotoxic Insecticide Promotes Fungal Infection in Aedes aegypti Larvae by Altering the Bacterial Community. Microb Ecol (2020). https://doi.org/10.1007/s00248-020-01567-w

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Keywords

  • Avermectins
  • Mosquito
  • Microbiome
  • Entomopathogens
  • Metarhizium