Ammonia leakage can underpin nitrogen-sharing among soil microorganisms

Soil microbial communities host a large number of microbial species that support important ecological functions such as biogeochemical cycling and plant nutrition. The extent and stability of these functions are affected by inter-species interactions among soil microorganisms, yet the different mechanisms underpinning microbial interactions in the soil are not fully understood. Here, we study the extent of nutrient-based interactions among two model, plant-supporting soil microorganisms, the fungi Serendipita indica, and the bacteria Bacillus subtilis. We found that S. indica is unable to grow with nitrate - a common nitrogen source in the soil - but this inability could be rescued, and growth restored in the presence of B. subtilis. We demonstrate that this effect is due to B. subtilis utilising nitrate and releasing ammonia, which can be used by S. indica. We refer to this type of mechanism as ammonia mediated nitrogen sharing (N-sharing). Using a mathematical model, we demonstrated that the pH dependent equilibrium between ammonia (NH3) and ammonium (NH+4) results in an inherent cellular leakiness, and that reduced amonnium uptake or assimilation rates could result in higher levels of leaked ammonia. In line with this model, a mutant B. subtilis - devoid of ammonia uptake - showed higher S. indica growth support in nitrate media. These findings highlight that ammonia based N-sharing can be a previously under-appreciated mechanism underpinning interaction among soil microorganisms and could be influenced by microbial or abiotic alteration of pH in microenvironments.