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.
Nitrogen (N) is considered as a main limiting factor in plant growth, and nitrogen losses through denitrification can be responsible for severe decreases in plant productivity. Recently, it was demonstrated that Fallopia spp. is responsible for biological denitrification inhibition (BDI) through the release of unknown secondary metabolites. Here, we investigate the secondary metabolites involved in the BDI of Fallopia spp. The antioxidant, protein precipitation capability of Fallopia spp. extracts was measured in relation to the aerobic respiration and denitrification of two bacteria (Gram positive and Gram negative). Proanthocyanidin concentrations were estimated. Proanthocyanidins in extracts were characterized by chromatographic analysis, purified and tested on the bacterial denitrification and aerobic respiration of two bacterial strains. The effect of commercial procyanidins on denitrification was tested on two different soil types. Denitrification and aerobic respiration inhibition were correlated with protein precipitation capacity and concentration of proanthocyanidins but not to antioxidant capacity. These proanthocyanidins were B-type procyanidins that inhibited denitrification more than the aerobic respiration of bacteria. In addition, procyanidins also inhibited soil microbial denitrification. We demonstrate that procyanidins are involved in the BDI of Fallopia spp. Our results pave the way to a better understanding of plant-microbe interactions and highlight future applications for a more sustainable agriculture.
Hymenopterous parasitoids are key species involved in the regulation of insect populations. Kairomone perception is an important step leading to host parasitization. The massive use of insecticides induces environmental pollution that can interact with the reproduction of parasitoids. In this work, we have determined the sublethal effects of two insecticides, an organophosphorus (chlorpyrifos) and a pyrethroid (deltamethrin), on the arrestment, by host kairomones, of female parasitoids surviving an LD 20 for 24 h. The behavior of the parasitoids has been recorded with a video-computerized system. The analysis of the behaviors in control conditions versus exposed to an LD 20 have shown that both insecticides significantly increased the arrestment of parasitoids by kairomones. This increase was not followed up by a modification of the kinetics of the behavior. In both control and exposed conditions, parasitoids regularly increased their residence time on the kairomone patch indicating that no saturation to kairomones had occurred. In a field situation where hosts could be scarce, this increase in arrestment could be advantageous for parasitoids by increasing their host finding.
Recently, it has been shown that procyanidins from Fallopia spp. inhibit bacterial denitrification, a phenomenon called biological denitrification inhibition (BDI). However, the mechanisms involved in such a process remain unknown. Here, we investigate the mechanisms of BDI involving procyanidins, using the model strain Pseudomonas brassicacearum NFM 421. The aerobic and anaerobic (denitrification) respiration, cell permeability and cell viability of P. brassicacearum were determined as a function of procyanidin concentration. The effect of procyanidins on the bacterial membrane was observed using transmission electronic microscopy. Bacterial growth, denitrification, NO3- and NO2-reductase activity, and the expression of subunits of NO3- (encoded by the gene narG) and NO2-reductase (encoded by the gene nirS) under NO3 or NO2 were measured with and without procyanidins. Procyanidins inhibited the denitrification process without affecting aerobic respiration at low concentrations. Procyanidins also disturbed cell membranes without affecting cell viability. They specifically inhibited NO3- but not NO2-reductase.Pseudomonas brassicacearum responded to procyanidins by over-expression of the membrane-bound NO3-reductase subunit (encoded by the gene narG). Our results suggest that procyanidins can specifically inhibit membrane-bound NO3-reductase inducing enzymatic conformational changes through membrane disturbance and that P. brassicacearum responds by over-expressing membrane-bound NO3-reductase. Our results lead the way to a better understanding of BDI.
Nitrate is a limiting resource in heathland acid soils. Nitrate levels increase in heathland soils after Pteridium aquilinum invasions, and this species is assumed to biologically control nitrogen cycle processes, thus increasing nitrate availability. We compared how P. aquilinum (bracken) and Erica cinerea (bell heather) modify processes driving nitrate availability along a soil pH gradient in a Natura 2000 reserve facing bracken invasion. Soil nitrate and ammonium concentrations, substrate‐induced respiration (SIR), denitrification and nitrification enzyme activities (DEA and NEA, respectively), root procyanidin concentrations, and denitrification inhibition by procyanidins were measured on five sites under P. aquilinum and E. cinerea stands. NEA and nitrate levels were higher, and ammonium levels and SIR lower, for P. aquilinum in the most acid soils. Procyanidins from both species induced the same level of denitrification inhibition, soil nitrate being correlated with root procyanidin concentration for both species. Soil nitrate correlated with NEA only for P. aquilinum. Our results show that both species increased procyanidin production in the most acid soils, thereby reducing denitrification and decreasing nitrate loss, this process being more efficient for E. cinerea. However, P. aquilinum additionally increased nitrification, and this double control on nitrification and denitrification was very efficient to increase soil nitrate availability in the most acid soils. This may participate to the success of P. aquilinum invasions in heathlands. This shows that approaches for bracken control in heathlands should better account for belowground processes and, more generally, that biological denitrification inhibition by plants may be a widespread phenomenon influencing soil N dynamics in N‐poor environments.
Aim
The success of invasive species in their introduced range is often assumed to result from evolutionary changes in defence and growth traits, or as a response to more favourable conditions. The latter is assumed particularly for species exhibiting low, or even no, sexual reproduction in the introduced range.
Location and Methods
Here, we compared Japanese (native range) and French (introduced range) populations of Fallopia japonica under common growth conditions in a glasshouse. We measured height, aboveground and belowground mass, stem stiffness, leaf toughness and secondary metabolites found in hydroalcoholic extracts of rhizomes of F. japonica, as well as the competitive response of Rubus caesius (a co‐occurring native species in the invaded range) in the presence of F. japonica from both ranges.
Results
Aboveground biomass, height, stem stiffness and composition of secondary metabolites were not significantly different between the two ranges, showing that increased aboveground vigour observed in situ in France is probably the result of a plastic response following the release of abiotic or biotic constraints from the native range. On the other hand, belowground mass, effect on R. caesius, and leaf toughness were all higher in French populations, suggesting increases in competitive ability and defence mechanisms. These differences between France and Japan may be explained either by post‐introduction evolution or by the introduction in Europe, in nineteenth century, of an exceptionally vigorous clone (pre‐adaptation).
Main conclusions
Our results provide evidence that the high vigour of this major invasive species in its introduced range is probably due to both a response to more favourable conditions and rapid evolution.
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