Abstract
BackgroundSoil microorganisms are key determinants of soil fertility and plant health. Soil phytopathogenic fungi are one of the most important causes of crop losses worldwide. Microbial biocontrol agents have been extensively studied as alternatives for controlling phytopathogenic soil microorganisms, but molecular interactions between them have mainly been characterised in dual cultures, without taking into account the soil microbial community. We used an RNA sequencing approach to elucidate the molecular interplay of a soil microbial community in response to a plant pathogen and its biocontrol agent, in order to examine the molecular patterns activated by the microorganisms.ResultsA simplified soil microcosm containing 11 soil microorganisms was incubated with a plant root pathogen (Armillaria mellea) and its biocontrol agent (Trichoderma atroviride) for 24 h under controlled conditions. More than 46 million paired-end reads were obtained for each replicate and 28,309 differentially expressed genes were identified in total. Pathway analysis revealed complex adaptations of soil microorganisms to the harsh conditions of the soil matrix and to reciprocal microbial competition/cooperation relationships. Both the phytopathogen and its biocontrol agent were specifically recognised by the simplified soil microcosm: defence reaction mechanisms and neutral adaptation processes were activated in response to competitive (T. atroviride) or non-competitive (A. mellea) microorganisms, respectively. Moreover, activation of resistance mechanisms dominated in the simplified soil microcosm in the presence of both A. mellea and T. atroviride. Biocontrol processes of T. atroviride were already activated during incubation in the simplified soil microcosm, possibly to occupy niches in a competitive ecosystem, and they were not further enhanced by the introduction of A. mellea.ConclusionsThis work represents an additional step towards understanding molecular interactions between plant pathogens and biocontrol agents within a soil ecosystem. Global transcriptional analysis of the simplified soil microcosm revealed complex metabolic adaptation in the soil environment and specific responses to antagonistic or neutral intruders.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3174-4) contains supplementary material, which is available to authorized users.
Highlights
Soil microorganisms are key determinants of soil fertility and plant health
Five conditions were analysed in triplicate: the simplified soil microcosm incubated for 24 h either without exogenous fungi (SSM), with the biocontrol agent T. atroviride (SSM+T), with the plant pathogen A. mellea (SSM+A) or with both (SSM+T+A), and the simplified soil microcosm collected at the beginning of the experiment just after inoculation of the 11 soil microorganisms (SSM0)
Experimental design and RNA-Seq analysis of the simplified soil microcosm The simplified soil microcosm was based on a soil matrix simultaneously inoculated with 11 soil microorganisms whose genomes were already sequenced and available that were selected to mimic a community of bacteria (Gram-positive and negative), yeasts and filamentous fungi commonly found in soil [44, 54,55,56,57,58,59,60,61,62,63,64,65,66], having beneficial, pathogenic, saprophytic or neutral properties for crops (Table 1)
Summary
Soil microorganisms are key determinants of soil fertility and plant health. Soil phytopathogenic fungi are one of the most important causes of crop losses worldwide. Microbe-microbe interactions have an important impact on microbial fitness in the soil [3] and they can positively or negatively affect other participants, including organisms of higher taxa [4]. These interactions can be synergistic, neutral or antagonistic, and can affect the growth, metabolism and differentiation of members of the microbial community [5]. Plant pathogens have to compete with members of the rhizosphere microbiota for available nutrients and microsites in order to infect root tissue, and they are significantly restricted in growth by the antagonistic activities of biocontrol microorganisms in suppressive soils [6]. Despite the widespread occurrence of interspecific microbial interactions in nature and their crucial relevance, there is a lack of understanding about how each species perceives and responds to interactions with other microbes within a complex community [7]
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