Microbiota modulation of allelopathy depends on litter chemistry: Mitigation or exacerbation?

Having a pivotal role in biogeochemical cycles, litter decomposition affects plant growth and regeneration by inducing the release of allelochemicals. The aim of this study was to assess the role of the microbiota in modulating the allelopathic effects of freshly fallen and decomposed leaf litter. To disentangle the chemical and microbial effects, bioassays were carried out on four target plants in sterile and non-sterile conditions. All litter types were characterized by carbon-13 cross polarization magic-angle spinning nuclear magnetic resonance (C-CPMAS NMR) spectroscopy, and the associated fungal and bacterial microbiota were described by next-generation sequencing. When the litter extract was sterilized, freshly fallen litter severely inhibited the plant root growth, but during decomposition, the allelopathic effect rapidly decreased. Root growth was negatively correlated with extractable carbon and positively correlated with parameters associated with tissue lignification. In non-sterile conditions, the living microbiota modulated the leaf litter allelopathic effects of mitigation (26.5% of cases) and exacerbation (26.6% of cases). The mitigation effect was more frequent and intense in stressful conditions, i.e., highly phytotoxic freshly fallen litter, than in benign environments, i.e., decomposed litter. Finally, we identified specific bacterial and fungal operational taxonomic units (OTUs) that could be involved in the mediation of the litter allelopathic effect. This study highlights the importance of studying allelopathy in both sterile conditions and in the presence of a living microbiota to assess the role of litter chemistry and the potential impact of plant detritus on the agro-ecosystem and natural plant communities.