Superoxide dismutase SOD-1 modulates C. elegans pathogen avoidance behavior

Abstract

The C. elegans nervous system mediates protective physiological and behavioral responses amid infection. However, it remains largely unknown how the nervous system responds to reactive oxygen species (ROS) activated by pathogenic microbes during infection. Here, we show superoxide dismutase-1 (SOD-1), an enzyme that converts superoxide into less toxic hydrogen peroxide and oxygen, functions in the gustatory neuron ASER to mediate C. elegans pathogen avoidance response. When C. elegans first encounters pathogenic bacteria P. aeruginosa, SOD-1 is induced in the ASER neuron. After prolonged P. aeruginosa exposure, ASER-specific SOD-1 expression is diminished. In turn, C. elegans starts to vacate the pathogenic bacteria lawn. Genetic knockdown experiments reveal that pathogen-induced ROS activate sod-1 dependent behavioral response non cell-autonomously. We postulate that the delayed aversive response to detrimental microbes may provide survival benefits by allowing C. elegans to temporarily utilize food that is tainted with pathogens as an additional energy source. Our data offer a mechanistic insight into how the nervous system mediates food-seeking behavior amid oxidative stress and suggest that the internal state of redox homeostasis could underlie the behavioral response to harmful microbial species.

Neuronal and non-neuronal signals regulate Caernorhabditis elegans avoidance of contaminated food

“…A number of sensory neurons required for pathogen avoidance have been identified [ 6 , 11 , 19 , 34 ]. In some cases, these neurons appear to regulate the avoidance of more than one pathogen; for example AWB is required for the avoidance of both S. marcescens and P. aeruginosa [ 6 , 11 ].…”

Superoxide dismutases: Dual roles in controlling ROS damage and regulating ROS signaling

“… Horspool and Chang (2017) show that sod-1 expression is specifically induced in the gustatory neuron ASER in response to pathogenic bacteria and that this up-regulation is required to mediate pathogen avoidance. Horspool and Chang (2017) interpret these findings to suggest that pathogen-induced ROS activate a sod-1 –dependent pathway to mediate the avoidance behavior. SODs have also been shown to be required in a developmental context: the development of the vulva, which is regulated by the RAS signaling pathway.…”

“…There is also a very interesting study on cell-specific up-regulation of sod-1 ( Horspool and Chang, 2017 ). Horspool and Chang (2017) show that sod-1 expression is specifically induced in the gustatory neuron ASER in response to pathogenic bacteria and that this up-regulation is required to mediate pathogen avoidance.…”

“…There is also a very interesting study on cell-specific up-regulation of sod-1 ( Horspool and Chang, 2017 ). Horspool and Chang (2017) show that sod-1 expression is specifically induced in the gustatory neuron ASER in response to pathogenic bacteria and that this up-regulation is required to mediate pathogen avoidance. Horspool and Chang (2017) interpret these findings to suggest that pathogen-induced ROS activate a sod-1 –dependent pathway to mediate the avoidance behavior.…”

Neuron-specific regulation of superoxide dismutase amid pathogen-induced gut dysbiosis

“…Recent studies reveal that pathogenic bacteria Pseudomonas aeruginosa , which are frequently found in the habitats of nematodes [15] , [16] , can colonize the intestine of C. elegans [17] , [18] , [19] , [20] . Switching C. elegans from a diet of E. coli to a diet of P. aeruginosa creates a condition that mimics gut dysbiosis [21] , [22] , [23] . The change in the microbial composition in the intestine activates host responses [22] , [24] , [25] , [26] .…”