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Summary  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.

Molecular mechanism of the smart attack of pathogenic bacteria on nematodes