Disruption of microbial community composition and identification of plant growth promoting microorganisms after exposure of soil to rapeseed-derived glucosinolates.

Meike Siebers,Thomas Rohr,Margot Schulz,Stephan Thies,Filip Kovacic,Peter Dörmann,Marina Ventura,Vadim Schütz,Martin Berg,Karl-Erich Jaeger,Ricardo Aroca

doi:10.1371/journal.pone.0200160

Abstract

Land plants are engaged in intricate communities with soil bacteria and fungi indispensable for plant survival and growth. The plant-microbial interactions are largely governed by specific metabolites. We employed a combination of lipid-fingerprinting, enzyme activity assays, high-throughput DNA sequencing and isolation of cultivable microorganisms to uncover the dynamics of the bacterial and fungal community structures in the soil after exposure to isothiocyanates (ITC) obtained from rapeseed glucosinolates. Rapeseed-derived ITCs, including the cyclic, stable goitrin, are secondary metabolites with strong allelopathic affects against other plants, fungi and nematodes, and in addition can represent a health risk for human and animals. However, the effects of ITC application on the different bacterial and fungal organisms in soil are not known in detail. ITCs diminished the diversity of bacteria and fungi. After exposure, only few bacterial taxa of the Gammaproteobacteria, Bacteriodetes and Acidobacteria proliferated while Trichosporon (Zygomycota) dominated the fungal soil community. Many surviving microorganisms in ITC-treated soil where previously shown to harbor plant growth promoting properties. Cultivable fungi and bacteria were isolated from treated soils. A large number of cultivable microbial strains was capable of mobilizing soluble phosphate from insoluble calcium phosphate, and their application to Arabidopsis plants resulted in increased biomass production, thus revealing growth promoting activities. Therefore, inclusion of rapeseed-derived glucosinolates during biofumigation causes losses of microbiota, but also results in enrichment with ITC-tolerant plant microorganisms, a number of which show growth promoting activities, suggesting that Brassicaceae plants can shape soil microbiota community structure favoring bacteria and fungi beneficial for Brassica plants.

Highlights

Glucosinolates (GSLs) are secondary metabolites of the Brassicales, a plant order including the family of Brassicaceae with numerous crop species, e.g. Brassica napus, Brassica oleracea and others
To study the impact of a standardized rapeseeds extract (RS-EX) containing predominantly the cylic ITC goitrin, on bacterial and fungal community structures, soil without a history of glucosinolates was treated with RS-EX followed by phospholipid fatty acid (PLFA) profiling as an indicator of microbial diversity. (S1 Table; Fig 1A and 1B)
The measurement of the phospholipid fatty acid (PLFA) composition was employed for the analysis of microbial diversity, because specific PLFAs are characteristic for bacterial and fungal taxa [41]

Summary

Introduction

Glucosinolates (GSLs) are secondary metabolites of the Brassicales, a plant order including the family of Brassicaceae with numerous crop species, e.g. Brassica napus (rapeseed, canola), Brassica oleracea (vegetables) and others. Rapeseed belongs to the most important oil crops, with Europe, Canada and China representing the leading production areas. Characterized by a short half-life (from hours to days), ITCs exert strong allelopathic effects against many plants, fungi and nematodes. Cyclized 2-hydroxy-3-butenyl ITC (goitrin) is a stable, water soluble ITC derived from progoitrin, the major GSL in rapeseed and other Brassica species. Garlic mustard (Alliaria petiolata), another Brassicaceae species and an aggressive invader in the USA, succeeded in the destruction of beneficial fungi living in a mutualistic lifestyle with native trees by ITC allelopathy [2,3]

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Conclusion