Biology subjects

Thoenen, L.

Publications and source records attributed to Thoenen, L..

3 recordsLinked to original sources

bioRxiv2023

The lactonase BxdA mediates metabolic adaptation of maize root bacteria to benzoxazinoids

Root exudates contain secondary metabolites that affect the plants root microbiome. How microbes cope with these bioactive compounds, and how this ability shapes root microbiomes remain largely unknown. We investigated how maize root bacteria metabolise benzoxazinoids, the main specialised metabolites of maize. Diverse and abundant bacteria metabolised the major compound (6-methoxy-benzoxazolin-2-one, MBOA) in the maize rhizosphere to 2-amino-7-methoxyphenoxazin-3-one (AMPO). By contrast, bacteria isolated from Arabidopsis, which does not produce benzoxazinoids, were unable to metabolise MBOA. Among Microbacteria strains, this differential metabolisation allowed to identify a conserved gene cluster containing the lactonase bxdA. BxdA converts MBOA to AMPO in vitro and we show that this capacity provided bacteria a growth benefit under carbon-limiting conditions. Together these results reveal that maize root bacteria - through BxdA - are metabolically adapted to the benzoxazinoids of their host. We propose that metabolic adaptation to plant-specialised compounds shapes root bacterial communities across the plant kingdom.

microbiology↗

bioRxiv2023

Bacterial tolerance to host-exuded specialized metabolites structures the maize root microbiome

Plants exude specialized metabolites from their roots and these compounds are known to structure the root microbiome. However, the underlying mechanisms are poorly understood. We established a representative collection of maize root bacteria and tested their tolerance against benzoxazinoids, the dominant specialized and bioactive metabolites in the root exudates of maize plants. In vitro experiments revealed that benzoxazinoids inhibited bacterial growth in a strain- and compound-dependent manner. Tolerance against these selective antimicrobial compounds depended on bacterial cell wall structure. Further, we found that native root bacteria isolated from maize tolerated the benzoxazinoids better compared to non-host Arabidopsis bacteria. This finding suggests the adaptation of the root bacteria to the specialized metabolites of their host plant. Bacterial tolerance to 6-methoxy-benzoxazolin-2-one (MBOA), the most abundant and selective antimicrobial metabolite in the maize rhizosphere, correlated significantly with the abundance of these bacteria on benzoxazinoid-exuding maize roots. Thus, strain-dependent tolerance to benzoxazinoids largely explained the abundance pattern of bacteria on maize roots. Abundant bacteria generally tolerated MBOA, while low abundant root microbiome members were sensitive to this compound. Our findings reveal that tolerance to plant specialized metabolites is an important competence determinant for root colonization. We propose that bacterial tolerance to plant-secreted antimicrobial compounds is an underlying mechanism determining the structure of host-specific microbial communities. Significance StatementDiverse microbial communities colonize plant roots. They feed on carbon rich root exudates which contain a diverse mix of chemicals including primary and specialized metabolites. Here we show that specialized metabolites act as selective antibiotics to shape the root bacterial communities. By growing single isolates of maize root bacteria in the presence of benzoxazinoids in vitro, we find that the strains differ greatly in their tolerance to benzoxazinoids. Their different levels of tolerance largely explained their abundance on benzoxazinoid-exuding roots. Our work shows how plant specialized metabolites act to shape the maize root microbial community and thus deepened our mechanistic understanding of how plants shape their microbiome.

microbiology↗

bioRxiv2023

Soil chemical and microbial gradients determine accumulation of root exuded secondary metabolites and plant-soil feedbacks in the field

IntroductionHarnessing positive plant-soil feedbacks via crop rotations is a promising strategy for sustainable agriculture. Plants can influence soil properties including microbes by exuding specialized metabolites. However, the effects are often context dependent and variable. If and how local soil heterogeneity may explain this variation is unknown. Benzoxazinoids are specialized metabolites that are released in high quantities by cereals such as wheat and maize. Benzoxazinoids can alter rhizosphere microbiota and the performance of plants subsequently growing in the exposed soils and are thus an excellent model to study agriculturally relevant plant-soil feedbacks in the field, and to assess how soil factors affect their outcome. Materials & methodsTo understand the importance of local variation in soil properties on benzoxazinoid-mediated plant-soil feedbacks, we conditioned plots with wild-type maize and benzoxazinoid-deficient bx1 mutant plants in a grid pattern across an arable field. We then grew winter wheat across the entire field in the following season. We determined accumulation of benzoxazinoids, root-associated microbial communities, abiotic soil properties and wheat performance in each plot. We also determined benzoxazinoid conversion dynamics in a labelling experiment under controlled conditions, and then assessed associations between soil chemical variation and benzoxazinoid-mediated plant-soil feedbacks. ResultsAcross the field, we detected a marked gradient in soil chemical and microbial community composition. This gradient resulted in significant differences in benzoxazinoid accumulation. These differences were explained by differential benzoxazinoid degradation rather than exudation. Benzoxazinoid exudation modulated alpha diversity of root and rhizosphere bacteria and fungi during maize growth, but not during subsequent wheat growth, while the chemical fingerprint of benzoxazinoid accumulation persisted. Averaged across the field, we detected no significant feedback effects of benzoxazinoid conditioning on wheat performance and defence, apart from a transient decrease in biomass during vegetative growth. Closer analysis however, revealed pronounced feedback effects along the chemical and microbial gradient of the field, with effects gradually changing from negative to positive along the gradient. ConclusionOverall, this study revealed that plant-soil feedbacks differ in strength and direction within a field, and that this variation can be explained by standing chemical and microbial gradients, which strongly affect benzoxazinoid accumulation in the soil. Understanding within-field soil heterogeneity is crucial for the future exploitation of plant-soil feedbacks in sustainable precision agriculture.

plant biology↗