Molecular mechanism of the smart attack of pathogenic bacteria on nematodes

Abstract

Nematode–bacterial associations are far-reaching subjects in view of their impact on ecosystems, economies, agriculture and human health. There is still no conclusion regarding which pathogenic bacteria sense nematodes. Here, we found that the pathogenic bacterium Bacillus nematocida B16 was sensitive to C. elegans and could launch smart attacks to kill the nematodes. Further analysis revealed that the spores of B. nematocida B16 are essential virulence factors. Once gaseous molecules (morpholine) produced from C. elegans were sensed, the sporulation of B16 was greatly accelerated. Then, B16 showed maximum attraction to C. elegans during the spore-forming process but had no attraction until all the spores were formed. The disruption of either the spore formation gene spo0A or the germination gene gerD impaired colonization and attenuated infection in B16. In contrast, complementation with the intact genes restored most of the above-mentioned deficient phenotypes, which indicated that the spo0A gene was a key factor in the smart attack of B16 on C. elegans. Further, transcriptome, molecular simulations and quantitative PCR analysis showed that morpholine from C. elegans could promote sporulation and initiate infection by increasing the transcription of the spo0A gene by decreasing the transcription of the rapA and spo0E genes. The overexpression of rapA or spo0E decreased the induced sporulation effect, and morpholine directly reduced the level of phosphorylation of purified recombinant RapA and Spo0E compared to that of Spo0A. Collectively, these findings further support a ‘Trojan horse-like’ infection model. The significance of our paper is that we showed that the soil-dwelling bacterium B. nematocida B16 has the ability to actively detect, attract and attack their host C. elegans. These studies are the first report on the behaviours, signalling molecules and mechanism of the smart attack of B16 on nematodes and also reveal new insights into microbe–host interactions.