Transcriptomic responses of a simplified soil microcosm to a plant pathogen and its biocontrol agent reveal a complex reaction to harsh habitat

BACKGROUND:Soil microorganisms are key determinants of soil fertility and plant health. Soil phytopathogenic fungiare one of the most important causes of crop losses worldwide. Microbial biocontrol agents have been extensivelystudied as alternatives for controlling phytopathogenic soil microorganisms, but molecular interactions betweenthem 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 inresponse to a plant pathogen and its biocontrol agent, in order to examine the molecular patterns activated by themicroorganisms. RESULTS:A 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 than46 million paired-end reads were obtained for each replicate and 28,309 differentially expressed genes wereidentified in total. Pathway analysis revealed complex adaptations of soil microorganisms to the harsh conditions ofthe soil matrix and to reciprocal microbial competition/cooperation relationships. Both the phytopathogen and itsbiocontrol agent were specifically recognised by the simplified soil microcosm: defence reaction mechanisms andneutral 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 soilmicrocosm in the presence of bothA. melleaandT. atroviride. Biocontrol processes ofT. atroviridewere alreadyactivated during incubation in the simplified soil microcosm, possibly to occupy niches in a competitive ecosystem,and they were not further enhanced by the introduction ofA. mellea. CONCLUSIONS:This work represents an additional step towards understanding molecular interactions between plantpathogens and biocontrol agents within a soil ecosystem. Global transcriptional analysis of the simplified soilmicrocosm revealed complex metabolic adaptation in the soil environment and specific responses to antagonisticor neutral intruders