Gustatory-mediated avoidance of bacterial lipopolysaccharides via TRPA1 activation in Drosophila

Abstract

Detecting pathogens and mounting immune responses upon infection is crucial for animal health. However, these responses come at a high metabolic price (McKean and Lazzaro, 2011, Kominsky et al., 2010), and avoiding pathogens before infection may be advantageous. The bacterial endotoxins lipopolysaccharides (LPS) are important immune system infection cues (Abbas et al., 2014), but it remains unknown whether animals possess sensory mechanisms to detect them prior to infection. Here we show that Drosophila melanogaster display strong aversive responses to LPS and that gustatory neurons expressing Gr66a bitter receptors mediate avoidance of LPS in feeding and egg laying assays. We found the expression of the chemosensory cation channel dTRPA1 in these cells to be necessary and sufficient for LPS avoidance. Furthermore, LPS stimulates Drosophila neurons in a TRPA1-dependent manner and activates exogenous dTRPA1 channels in human cells. Our findings demonstrate that flies detect bacterial endotoxins via a gustatory pathway through TRPA1 activation as conserved molecular mechanism.DOI: http://dx.doi.org/10.7554/eLife.13133.001

Molecular and Cellular Organization of Taste Neurons in Adult Drosophila Pharynx

“…For example, L7-7 is involved in sensing sucrose but limiting sugar ingestion, representing an Ir neuron that operates in a negative circuit module for sugar intake (Joseph et al, 2017). In addition, another recent study suggests that TRPA1 expression in L8 and L9 of the LSO is involved in feeding avoidance to bacterial endotoxins lipopolysaccharides (LPS) (Soldano et al, 2016). Alternatively, some pharyngeal GRNs may evaluate characteristics other than palatability, such as temperature or viscosity.…”

Bacterial Signaling to the Nervous System through Toxins and Metabolites

“…Following LPS activation, trigeminal and DRG neurons produce pain and nodose ganglia neurons modulate appetite, nausea and fever. In the fruitfly Drosophila melanogaster , bitter-sensing gustatory neurons have been reported to detect LPS via TRPA1, allowing the organism to avoid food contaminated with bacteria [84]. We speculate that LPS-mediated defense mechanisms may also exist in mammals, such as inducing sickness behavior that promotes social isolation and limits the spread of pathogens.…”

Pathogen induced food evasion behavior in Drosophila larvae

“…As it is known that bitter receptors also play a role in bacterial detection (Tizzano et al, 2010;Maurer et al, 2015;Soldano et al, 2016), we tested whether the HuginPC neurons -bitter taste interneurons in the larval brain (Hückesfeld et al, 2016) -play an (C) Quantitative analysis of the red to green fluorescence ratio displayed by HuginPC neurons of larvae incubated in PBS (n=116 cells of 15 larvae), with live Pe (n=120 cells of 15 larvae) or with dead Pe (n=112 cells of 15 larvae) (both OD 600 =60). Significant differences could be detected between PBS and dead Pe compared with live Pe.…”