Ammonia leakage can underpin nitrogen-sharing among soil microbes

Abstract

AbstractSoil 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 microbes, 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 microbes, the fungiSerendipita indicaand the bacteriaBacillus subtilis. We find thatS. indicais unable to grow with nitrate - a common nitrogen source in the soil - but this inability can be rescued, and growth restored in the presence ofB. subtilis. We demonstrate that this effect is due toB. subtilisutilising nitrate and releasing ammonia, which can be used byS. indica. We refer to this type of mechanism as ammonia mediated nitrogen sharing (N-sharing). Using a mathematical model, we demonstrate that the pH dependent equilibrium between ammonia (NH3) and ammonium (NH4+) results in an inherent cellular leakiness, and that reduced amonnium uptake or assimilation rates can result in higher levels of leaked ammonia. In line with this model, a mutantB. subtilis- devoid of ammonia uptake - shows higherS. indicagrowth support in nitrate media. These findings highlight that ammonia based N-sharing can be a previously under-appreciated mechanism underpinning interaction among soil microbes and could be influenced by microbial or abiotic alteration of pH in microenvironments.Significance statementSoil microbial communities are an important factor in environmental nutrient cycling and sub-sequently plant health.S. indicais a well-studied plant growth promoting soil fungus but its inability to use nitrate, a major component of both agricultural/natural soils and crop fertilisers, may have important implications for agriculture and microbial ecology. We have demonstrated thatS. indicais dependant on external sources of nitrogen in nitrate-only environments and these can be produced byB. subtilis, another common soil microbe. We then demonstrate that this nitrogen sharing interaction is likely mediated by leaked ammonia and that ammonia leakage is influenced by environmental pH. Ammonia leakage and sharing represent currently unexplored and potentially vital components of nutrient interactions between microbes in soil communities, with profound implications for microbiome community structure and subsequent consequences for soil biogeochemical cycling and crop health.