Defensive repertoire of Drosophila larvae in response to toxic fungi

Abstract

Chemical warfare including insecticidal secondary metabolites is a well-known strategy for environmental microbes to monopolize a food source. Insects in turn have evolved behavioural and physiological defences to eradicate or neutralize the harmful microorganisms. We studied the defensive repertoire of insects in this interference competition by combining behavioural and developmental assays with whole-transcriptome time-series analysis. Confrontation with the toxic filamentous fungus Aspergillus nidulans severely reduced the survival of Drosophila melanogaster larvae. Nonetheless, the larvae did not behaviourally avoid the fungus, but aggregated at it. Confrontation with fungi strongly affected larval gene expression, including many genes involved in detoxification (e.g., CYP, GST and UGT genes) and the formation of the insect cuticle (e.g., Tweedle genes). The most strongly upregulated genes were several members of the insect-specific gene family Osiris, and CHK-kinase-like domains were over-represented. Immune responses were not activated, reflecting the competitive rather than pathogenic nature of the antagonistic interaction. While internal microbes are widely acknowledged as important, our study emphasizes the underappreciated role of environmental microbes as fierce competitors.

Identifying candidate detoxification genes in the ecdysteroid kinase-like (EcKL) and cytochrome P450 gene families inDrosophila melanogasterby integrating evolutionary and transcriptomic data

“…Genes are identified by both their Drosophila ancestral clade nomenclature, and their name or annotation symbol, as appropriate. PB1, phenobarbital dataset 1 (W. W. Sun et al, 2006); PB2, phenobarbital dataset 2 (King-Jones et al, 2006); PB3, phenobarbital dataset 3 (Misra et al, 2011); PiB, piperonyl butoxide (Willoughby et al, 2007); MA, methamphetamine (L. Sun et al, 2011); Tun, tunicamycin (Chow et al, 2013); Fun, Aspergillus nidulans toxins (Trienens et al, 2017); Mg, midgut; MT, Malpighian tubules; FB, fat body; L, 3 rd instar larvae; F, adult females; M, adult males; DS, detoxification score.…”

“…Seven xenobiotic differential gene expression datasets were mined for EcKL and P450 genes: phenobarbital in 3 rd instar larvae (W. W. Sun et al, 2006); phenobarbital in adult flies (King-Jones et al, 2006; Misra et al, 2011); piperonyl butoxide in adult flies (Willoughby et al, 2007); methamphetamine in adult flies (L. Sun et al, 2011); tunicamycin (8-hour timepoint) in adult flies (Chow et al, 2013); and fungal toxins (6-hour timepoint, wild-type vs. ΔlaeA Aspergillus nidulans ) in 1 st -instar larvae (Trienens et al, 2017). Genes were considered induced in a dataset if they were up-regulated ≥ 1.5-fold with a reported p-value < 0.05, except in the case of Chow et al (2013), where their average up-regulation across all 20 lines needed to be ≥ 1.5-fold.…”

The microbiome of pest insects: it is not just bacteria

“…Some evidence on a functional role of yeasts in nutrient provisioning comes from research on the non-pest insect Drosophila melanogaster Meigen, in which the mechanisms for this interaction have also been studied. Specifically, D. melanogaster larvae cannot develop on sterile fruit substrates, and strongly prefer fruits containing filamentous fungi or yeast over food without microbial growth, even when the fungi produce insecticidal mycotoxins (Trienens et al, 2017). By actively feeding on fungi, the larvae of D. melanogaster acquire sterol, which is required to support their growth and development (Starmer & Fogleman, 1986;Carvalho et al, 2010).…”

“…By actively feeding on fungi, the larvae of D. melanogaster acquire sterol, which is required to support their growth and development (Starmer & Fogleman, 1986;Carvalho et al, 2010). This intricate dependency is also shown by the extensive repertoire of defensive chemicals that the larvae possess to cope with the mycotoxins produced by some of the fungi (Trienens et al, 2017). A close relative of D. melanogaster and emerging pest in several countries worldwide, Drosophila suzukii (Matsumura), lays eggs on fresh rather than fermenting fruits, where the density of molds and yeasts is initially very low.…”

The Aspergilli and Their Mycotoxins: Metabolic Interactions With Plants and the Soil Biota

“…For example, Drosophila larvae have been shown to aggregate around aflatoxigenic A. nidulans colonies suppressing fungal growth, improving the chance of larval survival to the adult stage in natural habitats (Rohlfs, 2005;Trienens et al, 2017).…”