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Suppression of the insect cuticular microbiomes by a fungal defensin to facilitate parasite infection

Abstract

Insects can assemble defensive microbiomes on their body surfaces to defend against fungal parasitic infections. The strategies employed by fungal pathogens to combat host cuticular microbiotas remains unclear. Here, we report the identification and functional characterization of the defensin-like antimicrobial gene BbAMP1 encoded by the entomopathogenic fungus Beauveria bassiana. The mature peptide of BbAMP1 can coat fungal spores and can be secreted by the fungus to target and damage Gram-positive bacterial cells. Significant differences in insect survival were observed between the wild-type and BbAMP1 mutant strains during topical infection but not during injection assays that bypassed insect cuticles. Thus, BbAMP1 deletion considerably reduced fungal virulence while gene overexpression accelerated the fungal colonization of insects compared with the wild-type strain in natural infections. Topical infection of axenic Drosophila adults evidenced no difference in fly survivals between strains. However, the gnotobiotic infections with the addition of Gram-positive but not Gram-negative bacterial cells in fungal spore suspensions substantially increased the survival of the flies treated with ∆BbAMP1 compared to those infected by the wild-type and gene-overexpression strains. Bacterial colony counts and microbiome analysis confirmed that BbAMP1 could assist the fungus to manipulate insect surface bacterial loads. This study reveals that fungal defensin can suppress the host surface defensive microbiomes, which underscores the importance to extend the research scope of fungus-host interactions.

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Fig. 1: BbAMP1 protein characteristics and inductive expression.
Fig. 2: BbAMP1 expression and antimicrobial activity assays.
Fig. 3: Insect survivals after being treated with different fungal strains.
Fig. 4: Inhibition of fungal growth and membrane penetration by different bacteria.
Fig. 5: Differential manipulation of the fly surface microbiomes by different fungal strains.

Data availability

Bacterial 16S rRNA sequencing fastq data have been deposited in the SRA (Sequencing Read Achieve) database with the BioProject accessions PRJNA751686 (SRX11638323-SRX11638354).

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Funding

This work was supported by the National Natural Science Foundation of China (No. 32021001) and the Chinese Academy of Sciences (Nos. XDPB16 and QYZDJ-SSW-SMC028).

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Conceptualization, supervision and funding acquisition: CW; performed the experiments: SH, YS, HC; analyzed the data: SH, HC; wrote the paper: SH, CW. All the authors read and approved the final manuscript.

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Correspondence to Chengshu Wang.

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Hong, S., Sun, Y., Chen, H. et al. Suppression of the insect cuticular microbiomes by a fungal defensin to facilitate parasite infection. ISME J (2022). https://doi.org/10.1038/s41396-022-01323-7

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