Long-term organic and mineral fertilization strategies shape the rhizosphere microbiota and performance of lettuce

Belowground plant-microbe interactions are crucial for plant development and health. Although previous studies have shown that soil microbial communities are influenced by fertilization strategies, less is known about the aboveground plant response to the rhizosphere microbiota assemblage shaped by agricultural management strategies. In our study, we aimed to investigate the effects of long-term fertilization strategies across field sites on the rhizosphere prokaryotic (Bacteria and Archaea) community composition and plant performance. We conducted growth chamber experiments with lettuce (Lactuca sativa L.) cultivated in soils from two long-term field experiments situated in Therwil, Switzerland and Thyrow, Germany, each of which compared organic vs. mineral fertilization strategies. High-throughput sequencing of bacterial 16S rRNA genes amplified from total community DNA showed a rhizosphere core microbiota shared in all lettuce plants across soils, going beyond differences in community composition depending on field site and fertilization strategies. Firmicutes were enriched irrespective of the field site in the rhizosphere of lettuce grown in organically fertilized soils. When cultivated in organically fertilized soils, a higher expression of several stress-related genes was observed by RT-qPCR analysis in lettuce leaves although plants were visibly free of disease symptoms. Another experiment showed that in presence of the soil-borne model pathogen Rhizoctonia solani AG1-IB, the plant productivity (dry biomass) decreased in soils from Thyrow with both long-term organic and mineral fertilization strategies. Moreover, we observed that the expression of genes like BGlu42 (β Glucosidase), OPT3 (Iron transporter) and MYB15 (Transcription factor) were significantly higher in the plants grown in organically fertilized soils in presence of R. solani. This could indicate an ISR response via iron-mobilizing phenolics, simulating root iron-deficiency response and changes in iron-homeostasis mechanisms in the rhizosphere, which can be expressed systemically throughout the plant. The ongoing analysis of the rhizosphere microbiome would reveal more information about the suggested mechanism. Taken together, besides effects of fertilization strategy and field site, results of our study under controlled conditions demonstrate the crucial role of the lettuce plant in driving the rhizosphere microbiota assemblage.