Evidence for biological denitrification inhibition (BDI) by plant secondary metabolites

Abstract

SummaryPrevious studies on the effect of secondary metabolites on the functioning of rhizosphere microbial communities have often focused on aspects of the nitrogen (N) cycle but have overlooked biological denitrification inhibition (BDI), which can affect plant N-nutrition. Here, we investigated the BDI by the compounds of Fallopia spp., an invasive weed shown to be associated with a low potential denitrification of the soil.Fallopia spp. extracts were characterized by chromatographic analysis and were used to test the BDI effects on the metabolic and respiratory activities of denitrifying bacteria, under aerobic and anaerobic (denitrification) conditions. The BDI of Fallopia spp. extracts was tested on a complex soil community by measuring denitrification enzyme activity (DEA), substrate induced respiration (SIR), as well as abundances of denitrifiers and total bacteria.In 15 strains of denitrifying bacteria, extracts led to a greater BDI (92%) than respiration inhibition (50%). Anaerobic metabolic activity reduction was correlated with catechin concentrations and the BDI was dose dependent. In soil, extracts reduced the DEA/SIR ratio without affecting the denitrifiers: total bacteria ratio.We show that secondary metabolite(s) from Fallopia spp. inhibit denitrification. This provides new insight into plant-soil interactions and improves our understanding of a plant's ability to shape microbial soil functioning.

Differential influence of four invasive plant species on soil physicochemical properties in a pot experiment

“…Overall, total and available forms of N (N-NO 3 , N-NH 4 ) and P (Olsen), S-SO 4 , exchangeable K, and Mg contributed the most to the discrimination of soils under different plant species. The influence of invasive I. glandulifera, R. japonica, and S. gigantea on soil has been estimated earlier in numerous field studies Vanderhoeven et al 2006;Dassonville et al 2008;Scharfy et al 2009;Maurel et al 2010;Tharayil et al 2013;Quist et al 2014;Ruckli et al 2013Ruckli et al , 2014bStefanowicz et al 2017), but experiments concerning this problem are rare (Scharfy et al 2010(Scharfy et al , 2011Bardon et al 2014Bardon et al , 2016. Previous studies focused mainly on invasion-induced changes in different forms of N and P in soil and found that these properties responded variably to the presence of I. glandulifera, R. japonica, or S. gigantea, and so did some exchangeable cations, for example K and Mg (ChapuisLardy et al 2006;Hejda and Pyšek 2006;Vanderhoeven et al 2006;Dassonville et al 2007;Scharfy et al 2009Scharfy et al , 2010Scharfy et al , 2011Tharayil et al 2013;Ruckli et al 2014b;Stefanowicz et al 2017).…”

“…A few experimental and field works have consistently reported the ability of R. japonica to modify N turnover (Hirose and Tateno 1984;Tharayil et al 2013;Bardon et al 2014Bardon et al , 2016Stefanowicz et al 2016). This species increases, at least seasonally, the concentration of N-NO 3 in soil in comparison to native vegetation, presumably due to the modification of denitrification and N mineralization processes via secondary metabolites (Hirose and Tateno 1984;Tharayil et al 2013;Bardon et al 2016;Stefanowicz et al 2017).…”

“…While the tissues or litter of I. glandulifera, R. japonica, R. laciniata, and S. gigantea have been assessed in respect of element and/or secondary metabolite concentrations and some authors tried to link their tissue quality with the soil environment (Kalemba et al 2001;Dassonville et al 2008;Fan et al 2009;Aguilera et al 2010;Tharayil et al 2013;Bardon et al 2014;Ruckli et al 2014a;Stefanowicz et al 2017), much less is known on the quality of root exudates of these species or their effects on physicochemical and biological soil properties (Scharfy et al 2010;Ruckli et al 2014a). Ruckli et al (2014a) found that I. glandulifera is able to inhibit mycelium growth by naphthoquinones-phenolics released from roots or leached from leaves by rain.…”

“…In another experiment, six invasive forbs, including I. glandulifera, R. japonica, and S. gigantea, were compared with the groups of native forbs and graminoids in respect of their effects on soil properties, suggesting no significant differences in soluble phenolics, nitrate, ammonium, or phosphate concentrations between the species groups (Scharfy et al 2011). Other experiments proved that extracts from the roots and rhizomes of R. japonica inhibit denitrification (Bardon et al 2014(Bardon et al , 2016. Comparison of the effects of the above-mentioned invaders on the properties of standardized soil would contribute to our knowledge on the invasion impact on ecosystems.…”

“…To date, only few experimental studies have tested the impact of I. glandulifera, R. japonica, R. laciniata, or S. gigantea on soil (Scharfy et al 2010(Scharfy et al , 2011Bardon et al 2014Bardon et al , 2016. Scharfy et al (2010) performed a mesocosm experiment simulating the invasion of a single species-S. gigantea into three wetland plant communities and found no invasion effect on N and P availability in soil.…”