Caenorhabditis elegans avoids staphylococcal superantigenic toxins via 5-hydroxytryptamine-dependent pathway

Avoidance behavior of Caenorhabditis elegans, a nematode, towards Staphylococcus aureus, a pathogenic bacterium, was studied. Caenorhabditis elegans avoided S. aureus cultures and also their culture supernatants, suggesting that secretory molecules are involved in the repellent activity. We demonstrated that toxic shock syndrome toxin 1 (TSST-1) and staphylococcal enterotoxin C (SEC), the superantigenic toxins produced by S. aureus, are responsible for the nematode avoidance. By using TSST-1 and SEC mutants, the results indicated that the repellent activity of these toxins is independent of their superantigenic activity. The TSST-1 and SEC were found to locate at chemosensory neurons that are responsible for the recognition of repellents and avoidance of pathogenic bacteria. When mutants of C. elegans deficient in Toll/interleukin-1 receptor (TIR-1) and 5-hydroxytryptamine (5-HT) biosynthesis were used, avoidance behavior was attenuated. In the 5-HT biosynthesis deficient mutant nematodes, the avoidance activity was recovered when exogenous 5-HT was added. tph-1 expression and 5-HT production were upregulated when the nematodes were treated with TSST-1 or SEC. These results suggest that C. elegans avoids S. aureus by recognizing secretory molecules including TSST-1 and SEC and this avoidance is dependent on TIR and production of 5-HT.