Bacteria are known to communicate primarily via secreted extracellular factors. Here we identify a previously uncharacterized type of bacterial communication mediated by nanotubes that bridge neighboring cells. Using Bacillus subtilis as a model organism, we visualized transfer of cytoplasmic fluorescent molecules between adjacent cells. Additionally, by coculturing strains harboring different antibiotic resistance genes, we demonstrated that molecular exchange enables cells to transiently acquire nonhereditary resistance. Furthermore, nonconjugative plasmids could be transferred from one cell to another, thereby conferring hereditary features to recipient cells. Electron microscopy revealed the existence of variously sized tubular extensions bridging neighboring cells, serving as a route for exchange of intracellular molecules. These nanotubes also formed in an interspecies manner, between B. subtilis and Staphylococcus aureus, and even between B. subtilis and the evolutionary distant bacterium Escherichia coli. We propose that nanotubes represent a major form of bacterial communication in nature, providing a network for exchange of cellular molecules within and between species.
Bibliographical noteFunding Information:
We thank I. Popov, E. Blayvas, N. Feinstein, and E. Rahamim (Hebrew University, IL) for technical support during EM studies. We are grateful to A. Rouvinski (Hebrew University, IL) for experimental advice and insightful discussions. We thank R. Losick (Harvard University, USA), M. Kassel (National Institutes of Health, USA), G. Bachrach (Hebrew University, IL), D. Kearns (Indiana University, USA), A. Taraboulos (Hebrew University, IL), and members of the Ben-Yehuda laboratory for valuable discussions and comments. We thank the National BioResource Project National Institute of Genetics, Japan (NIG, Japan) for providing B. subtilis mutant strains. This work was supported by the European Research Council Starting Grant (209130), and by the Israel Science Foundation (696/07) awarded to S. B-Y.