C. elegans avoidance of Pseudomonas: thioredoxin shapes the sensory response to bacterially produced nitric oxide

Abstract

We show that C. elegans avoids a bacterial pathogen Pseudomonas aeruginosa (PA14) by detecting PA14-produced nitric oxide (NO). PA14 mutants deficient for NO production fail to elicit avoidance and NO donors repel worms. PA14 and NO avoidance are mediated by the ASJ chemosensory neurons, which respond to NO with intracellular calcium rises. PA14 avoidance and NO-evoked calcium responses require receptor guanylate cyclases (DAF-11 and GCY-27), and cyclic nucleotide gated ion channels (TAX-2 and -4). ASJ exhibits calcium increases at both the onset and removal of NO. These NO-evoked ON and OFF calcium transients are affected by a redox sensing protein, TRX-1/thioredoxin. TRX-1s trans-nitrosylation activity inhibits the ON transient whereas TRX-1s de-nitrosylation activity promotes the OFF transient. Thus, C. elegans exploits bacterially produced NO as a cue to mediate avoidance and TRX-1 functions as an NO-sensor that endows ASJ with a bi-phasic response to NO exposure.