Algae-fungi symbioses and bacteria-fungi co-exclusion drive tree species-specific differences in canopy bark microbiomes

Abstract

With over 3 trillion trees, forest ecosystems comprise nearly one-third of the terrestrial surface of the Earth. Very little attention has been given to the exploration of the above-ground plant microbiome of trees, its complex trophic interactions, and variations among tree species. To address this knowledge gap, we applied a primer-independent shotgun metatranscriptomic approach to assess the entire living canopy bark microbiome comprising prokaryotic and eukaryotic primary producers, decomposers, and various groups of consumers. With almost 1500 genera, we found a high microbial diversity on three tree species with distinct bark textures: oak (Quercus robur), linden (Tilia cordata), both with rough bark, and maple (Acer pseudoplatanus) with smooth bark. Core co-occurrence network analysis revealed a rich food web dominated by algal primary producers, and bacterial and fungal decomposers, sustaining a diverse community of consumers, including protists, microscopic metazoans, and predatory bacteria. Whereas maple accommodated a depauperate microbiome, oak and linden accommodated a richer microbiome mainly differing in their relative community composition: Bacteria exhibited an increased dominance on linden, whereas co-occurring algae and fungi dominated on oak, highlighting the importance of algal-fungal lichen symbioses even at the microscopic scale. Further, due to bacteria-fungi co-exclusion, bacteria on bark are not the main beneficiaries of algae-derived carbon compounds as it is known from aquatic systems.