Species of the core leaf microbiome correlate with phyllodulcin and hydrangenol contents in Hydrangea macrophylla subsp. serrata

Hydrangenol and phyllodulcin, economically significant dihydroisocoumarins from Hydrangea macrophylla subsp. serrata, accumulate differentially in young leaves and decline as foliage ages in the cultivars ‘Oamacha’, ‘Odoriko Amacha’, and ‘Amagi Amacha’. To gain more insights into this phenomenon, we investigated the age- and genotype-dependent α- and β-diversity of leaf microbiome species, emphasizing endophytic microorganisms and the core microbiota. While the dynamics of the entire fungal and bacterial communities during leaf aging are cultivar-dependent, the predominance of the core species Cladosporium spp. and Lactobacillus spp. is not. Spearman correlations indicate an influence of phyllodulcin and hydrangenol on these dynamics. Endophytes with the highest positive correlation to both compounds are Cladosporium spp. and Streptococcus lutetiensis, while Clavispora lusitaniae, and Escherichia sp. show the opposite correlation. Molecular docking analysis suggests that phyllodulcin and hydrangenol can shape the leaf microbiota by suppressing biofilm formation, the divisome, and quorum sensing proteins of low-abundant species. Also, binding to fungal deacetylases may lead to altered metabolic activities. The results classify these dihydroisocoumarins as growth-suppressors of different endophytic genera, such as Pseudomonas, Bacillus and Candida species. We assume that aging of the host and potentially of microbiome members, changes in the production of bioactive compounds, shifting sensitivity to them combined with the cumulative impact of environmental factors, are responsible for the observed microbiome alterations in older leaves.