Abstract

There is increasing evidence that microbial volatiles (VOCs) play an important role in natural suppression of soil-borne diseases, but little is known on the factors that influence production of suppressing VOCs. In the current study we examined whether a stress-induced change in soil microbial community composition would affect the production by soils of VOCs suppressing the plant-pathogenic oomycete Pythium. Using pyrosequencing of 16S ribosomal gene fragments we compared the composition of bacterial communities in sandy soils that had been exposed to anaerobic disinfestation (AD), a treatment used to kill harmful soil organisms, with the composition in untreated soils. Three months after the AD treatment had been finished, there was still a clear legacy effect of the former anaerobic stress on bacterial community composition with a strong increase in relative abundance of the phylum Bacteroidetes and a significant decrease of the phyla Acidobacteria, Planctomycetes, Nitrospirae, Chloroflexi, and Chlorobi. This change in bacterial community composition coincided with loss of production of Pythium suppressing soil volatiles (VOCs) and of suppression of Pythium impacts on Hyacinth root development. One year later, the composition of the bacterial community in the AD soils was reflecting that of the untreated soils. In addition, both production of Pythium-suppressing VOCs and suppression of Pythium in Hyacinth bioassays had returned to the levels of the untreated soil. GC/MS analysis identified several VOCs, among which compounds known to be antifungal, that were produced in the untreated soils but not in the AD soils. These compounds were again produced 15 months after the AD treatment. Our data indicate that soils exposed to a drastic stress can temporarily lose pathogen suppressive characteristics and that both loss and return of these suppressive characteristics coincides with shifts in the soil bacterial community composition. Our data are supporting the suggested importance of microbial VOCs in the natural buffer of soils against diseases caused by soil-borne pathogens.

Highlights

  • In the light of sustainable agriculture and the call for reduction of pesticide use, insights in the mechanisms of natural suppression of soil-borne pathogens are essential

  • Addition of Pythium to the soils showed an overall effect of the pathogen: the root weight was significantly reduced in all soils in the consecutive years

  • Volatile organic compounds form an important part of the underground chemical communication network between plants, fungi and bacteria (Ryu et al, 2003; Vespermann et al, 2007; Insam and Seewald, 2010; Effmert et al, 2012; Bitas et al, 2013; Fiers et al, 2013)

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Summary

Introduction

In the light of sustainable agriculture and the call for reduction of pesticide use, insights in the mechanisms of natural suppression of soil-borne pathogens are essential. Depletion of carbon sources by indigenous microbes hampers the pre-infective growth of soil-borne pathogens resulting in lower infection rates (Hoitink and Boehm, 1999). This competition-related mechanism of pathogen control is known as “general disease suppression” (Hoitink and Boehm, 1999). Besides substrate competition, inhibitory compounds, released by microbes, have been indicated to contribute to fungistasis (Romine and Baker, 1972; De Boer et al, 2003) This implies that the carbon-withdrawing activity of the total soil microbial community is involved in fungistasis and the secondary metabolite production of certain groups within the soil microbial community. Based on this, Garbeva et al (2011) argued that the composition of soil microbial communities is more important in fungistasis than previously has been appreciated

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