Interspecies bacterial infomolecules facilitate nutrient exchange in biological soil crusts

Nitrogen fixation is crucial for the ecology of N-limited drylands. An important, though only recently recognized, plant-independent avenue for N₂-fixation takes place in desert topsoils through “C-for-N” mutualisms between specific heterotrophic diazotrophs and the cyanobacterium Microcoleus vaginatus, where partners need to come together into spatially close and partner-specific associations within the background of a diverse soil microbiome. We hypothesized that chemical signaling within the partner microbe’s exometabolome influences the motility behavior of mutualists, enabling them to collocate and stay together. Although well-characterized in the context of trans-kingdom symbiosis, the use of infomolecules to shape microbiomes in exclusively bacterial mutualisms has not yet been described. Using a combination of culture and field research, exometabolomic analyses, and chemotaxis assays, we showed that the M. vaginatus exometabolome can elicit the enrichment of heterodiazotrophs from the soil microbiome. This effect, when the cyanobacterium is N-starved, could be traced to three specific compounds: N-acetylglutamic acid, N-acetyl-L-methionine, and indole-3-acetic acid, which are only significantly produced under this condition. Together with prior reports that M. vaginatus similarly responds to molecular prompts through GABA and glutamate from carbon-starved heterotrophs, our findings unravel a bidirectional chemical dialogue between partners that can sustain symbiotic proximity in space and time. Interestingly, some, though not all of these infomolecules act as such in plant and animal systems. Together with its unique mode of N-transfer through urea, this keystone symbiosis in drylands can maintain its specificity even in an “open system” through the use of infomolecules and specific chemotactic responses, which also allow M. vaginatus to architect a microbiome that is tailored to its nutritional needs.