Plant-derived benzoxazinoids act as antibiotics and shape bacterial communities

Abstract

Plants synthesize and release specialized metabolites into their environment that can serve as chemical cues for other organisms. Metabolites that are released from the roots are important factors in determining which microorganisms will colonize the root and become part of the plant rhizosphere microbiota. Root exudates are often further converted by soil microorganisms, which can result in the formation of toxic compounds. How individual members of the plant rhizosphere respond to individual compounds and how the differential response of individual microorganisms contributes to the response of a microbial community remains unclear. Here, we investigated the impact of derivatives of one class of plant root exudates, benzoxazinoids, which are released by important crops such as wheat and maize, on a collection of 180 root-associated bacteria. We show that phenoxazine, derived from benzoxazinoids, inhibits the growth of root-associated bacteria in vitro in a strain-specific manner, with sensitive and resistant isolates in most of the studied clades. Synthetic bacterial communities that were assembled from only resistant isolates were more resilient to chemical perturbations than communities comprised of only sensitive members. Isolates that were shared between different communities revealed stable interactions, independent of the overall community composition. On the other hand, we could attribute differential community development to differences in interactions formed by closely related representatives of the same bacterial genus. Our findings highlight the fact that profiling isolate collections can aid the rational design of synthetic communities. Moreover, our data show that simplified in vitro community systems are able to recapitulate observations on the influence of metabolite exudation on the structure of root-associated communities, thus providing an avenue for reductionist explorations of the rhizosphere biology in defined, host-free settings.

An optimized hydroponic pipeline for large‐scale identification of wheat genotypes with resilient biological nitrification inhibition activity

“…However, some organic compounds limiting nitrification can have broad antimicrobial activity (Lodhi & Killingbeck, 1980; Tahir et al ., 2021). Several well‐characterized BNIs have also been shown to inhibit bacteria species besides the AOB in the soil (Bending & Lincoln, 2000; Sarr et al ., 2020; Schandry et al ., 2021; Wang et al ., 2021). The deployment and optimal use of the BNI trait in crop plants will undoubtedly require in‐depth analysis of their BNI activities on bacterial communities.…”

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

“…To complement previous studies 20 , we specifically investigated the genetic basis of benzoxazinoid metabolisation in the native context of root bacteria isolated from benzoxazinoid-exuding maize plants. We focused on MBOA, the most abundant 11 and most selective 19 benzoxazinoid in the maize rhizosphere.…”

“…Poaceae, including crops such as wheat, maize, and rye 17 . These compounds accumulate in leaves as chemical defences against insect pests and pathogens 17 and are exuded from the roots as phytosiderophores 18 and antimicrobials [19][20][21] . Benzoxazinoids directly shape the root and rhizosphere microbiomes [9][10][11]22 , and when metabolised to aminophenoxazinones by soil microbes, they also become allelopathic, inhibiting the germination and growth of neighbouring plants 17 .…”

Functions and biosynthesis of plant signaling metabolites mediating plant–microbe interactions

“…14 Similar to MBOA (58), another specic benzoxazinoid, phenoxazine (61), also displayed ecological functions in plant-microbe interactions. 99 Overall, our understanding on the roles of alkaloids and cyanogenic molecules in plant-microbe interactions are so far predominated by their antimicrobial properties as manifested by camalexin ( 52) and 4-OH-ICN (56), whilst the knowledge obtained from BXs might be applied to direct the outcome of plant-microbe interactions.…”

“…14 Similar to MBOA ( 58 ), another specific benzoxazinoid, phenoxazine ( 61 ), also displayed ecological functions in plant–microbe interactions. 99…”