Biological nitrification inhibition in the rhizosphere: determining interactions and impact on microbially mediated processes and potential applications

ABSTRACT Nitrification is the microbial conversion of reduced forms of nitrogen (N) to nitrate (NO3−), and in fertilized soils it can lead to substantial N losses via NO3− leaching or nitrous oxide (N2O) production. To limit such problems, synthetic nitrification inhibitors have been applied but their performance differs between soils. In recent years, there has been an increasing interest in the occurrence of biological nitrification inhibition (BNI), a natural phenomenon according to which certain plants can inhibit nitrification through the release of active compounds in root exudates. Here, we synthesize the current state of research but also unravel knowledge gaps in the field. The nitrification process is discussed considering recent discoveries in genomics, biochemistry and ecology of nitrifiers. Secondly, we focus on the ‘where’ and ‘how’ of BNI. The N transformations and their interconnections as they occur in, and are affected by, the rhizosphere, are also discussed. The NH4+ and NO3− retention pathways alternative to BNI are reviewed as well. We also provide hypotheses on how plant compounds with putative BNI ability can reach their targets inside the cell and inhibit ammonia oxidation. Finally, we discuss a set of techniques that can be successfully applied to solve unresearched questions in BNI studies. The BNI phenomenon is critically reviewed and hypotheses concerning the mode of action of BNI compounds on ammonia-oxidizing microrganisms are proposed together with a polyphasic approach useful to test BNI in soil systems.