Differential Impact of Plant Secondary Metabolites on the Soil Microbiota

Abstract

Plant metabolites can shape the microbial community composition in the soil. Two indole metabolites, benzoxazolinone (BOA) and gramine, produced by different Gramineae species, and quercetin, a flavonoid synthesized by many dicot species, were studied for their impacts on the community structure of field soil bacteria. The three plant metabolites were directly added to agricultural soil over a period of 28 days. Alterations in bacterial composition were monitored by next generation sequencing of 16S rRNA gene PCR products and phospholipid fatty acid analysis. Treatment of the soil with the plant metabolites altered the community composition from phylum to amplicon sequence variant (ASV) level. Alpha diversity was significantly reduced by BOA or quercetin, but not by gramine. BOA treatment caused a decrease of the relative abundance of 11 ASVs, while only 10 ASVs were increased. Gramine or quercetin treatment resulted in the increase in relative abundance of many more ASVs (33 or 38, respectively), most of them belonging to the Proteobacteria. Isolation and characterization of cultivable bacteria indicated an enrichment in Pseudarthrobacter or Pseudomonas strains under BOA/quercetin or BOA/gramine treatments, respectively. Therefore, the effects of the treatments on soil bacteria were characteristic for each metabolite, with BOA exerting a predominantly inhibitory effect, with only few genera being able to proliferate, while gramine and quercetin caused the proliferation of many potentially beneficial strains. As a consequence, BOA or gramine biosynthesis, which have evolved in different barley species, is accompanied with the association of distinct bacterial communities in the soil, presumably after mutual adaptation during evolution.

Applications of the indole-alkaloid gramine modulate the assembly of individual members of the barley rhizosphere microbiota

“…2). Of note, the impact of gramine applications on individual bacterial enrichments displayed an experimental effect: in our investigation this was manifested with an apparent suppression of bacterial proliferation in unplanted soil controls more pronounced than previously reported (Schütz et al, 2021). In addition to differences in applications per se, it is important to consider that those experiments were conducted using different soil types.…”

Triterpenoid and Steroidal Saponins Differentially Influence Soil Bacterial Genera

“…Treating soil with pure compounds has revealed the strong influences PSMs have in shaping the microbiota [ 19 , 20 , 21 , 22 , 35 , 37 , 47 ]. In this study, we treated soil with saponins that had either steroid- or oleanane-type aglycones.…”

“…PSM-deficient mutants of certain plant species, such as thale cress ( Arabidopsis thaliana ) and maize ( Zea mays ), show that di-, sester-, tri-terpenoids, coumarins, and benzoxazinoids modulate the root-associated microbiome [ 12 , 13 , 14 , 15 , 16 , 17 , 18 ]. The treatment of soils with authentic compounds has also helped to reveal the roles of PSMs such as flavonoids (daidzein and quercetin), alkaloids (nicotine and gramine), benzoxazinoid, and opine (santhopine) in modulating the soil microbiome [ 19 , 20 , 21 , 22 ].…”

Recent Developments in the Study of Plant Microbiomes

“…Although conceptually quite different from assembling synthetic microbiomes from known and well-studied bacteria, it is possible to add specific chemicals to the soil and thereby increase the numbers of certain bacterial strains while decreasing the numbers of other strains [ 53 , 58 , 62 , 68 , 69 , 138 , 139 ]. This reflects the fact that plant metabolites often have a large impact on the bacterial community in the soil.…”

“…This reflects the fact that plant metabolites often have a large impact on the bacterial community in the soil. For example, in one recent set of experiments, three different plant metabolites: benzoxazolinone, gramine and quercetin were added to agricultural soil over a period of 28 days [ 139 ]. During this period of time, bacterial diversity was significantly reduced by both benzoxazolinone and quercetin, but not by gramine.…”