Biological denitrification inhibition (BDI) on nine contrasting soils: An unexpected link with the initial soil denitrifying community

Denitrification is considered the major pathway leading to soil gaseous (N) losses, affecting N availability for plants and consequently plant productivity. Biological denitrification inhibition (BDI) in Fallopia spp., a plant species complex with a high level of growth and competitiveness for mineral N, acts through procyanidin production. However, the soil factors governing BDI development are still unknown. Through a mesocosm experiment using two treatments – soil planted with Fallopia japonica and unplanted–, nine biologically and physically contrasting soils were studied with the aim to ascertain how each can affect BDI development. Microbial enzyme activities (respiration - SIR, denitrification - DEA), denitrifying functional gene abundance (nirK, nirS), total bacterial community abundance (rRNA 16S) and soil physicochemical parameters (N mineral forms, soil texture, moisture, pH) were measured before and after plant growth, and the DEA:SIR ratio was used as a BDI proxy. The DEA:SIR ratio decreased for six soils. BDI development is related to a small number of soil factors, mainly initial soil moisture and ammonium concentration, and unexpectedly, with the initial abundance of nirK(in), nirS(in) and rRNA 16S(in). The intensity of this decrease is positively correlated to the level of DEA in unplanted soil: the higher the DEA in unplanted soil, the more intense the BDI under F. japonica. The procyanidin concentration of the F. japonica belowground system was positively correlated to BDI intensity. These results suggest that a procyanidin assay from the plant belowground system could be a new proxy for measuring BDI intensity. Interestingly, this research shows that BDI is not systematic, and that few (a)biotic soil parameters influence its development. More importantly, this research is the first to highlight that biotic factors are relevant in explaining BDI. This paper also presents new perspectives on plant-microorganism interactions in terms of plant awareness of the soil microbial community. •This study investigated the soil factors governing biological denitrification inhibition.•The microbial denitrification/respiration ratio was used to identify BDI strategy.•BDI strategy is correlated with soil initial biotic factors (initial gene abundances).•Procyanidin levels in plant belowground systems are a new proxy for BDI development.