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

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INVERTEBRATE MICROBIOLOGY

A Neurotoxic Insecticide Promotes Fungal Infection in Aedes aegypti Larvae by Altering the Bacterial Community Y. A. Noskov 1,2 & M. R. Kabilov 3 & O. V. Polenogova 1 & Y. A. Yurchenko 1 & O. E. Belevich 1 & O. N. Yaroslavtseva 1 & T. Y. Alikina 3 & A. M. Byvaltsev 4 & U. N. Rotskaya 1 & V. V. Morozova 3 & V. V. Glupov 1 & V. Y. Kryukov 1 Received: 1 May 2020 / Accepted: 27 July 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020

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. Keywords Avermectins . Mosquito . Microbiome . Entomopathogens . Metarhizium

Introduction Interactions between bacteria and fungi in various habitats are important for the functioning of biological systems [1]. It is well known that in vertebrate animals, these interactions may be modulated by different factors, including infectious Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00248-020-01567-w) contains supplementary material, which is available to authorized users. * Y. A. Noskov [email protected] 1

Institute of Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences, Novosibirsk, Russia 630091

2

National Research Tomsk State University, Tomsk, Russia 634050

3

Institute of Chemical Biology and Fundamental Medicine, Siberian Branch, Russian Academy of Sciences, Novosibirsk, Russia 630090

4

Novosibirsk State University, Novosibirsk, Russia 630090

diseases and toxicant stresses [2]. Howe