Tree decline and mortality following pathogen invasion alters the diversity, composition and network structure of the soil microbiome

Abstract

The loss of tree health is a global concern with many unknown cascading impacts on the diversity and function of forest ecosystems. Specifically, it is uncertain how the process of tree decline and mortality driven by exotic pathogens might alter the soil microbiome. Here we combined high-throughput sequencing, neighborhood models, and network analysis to explore the impacts of the decline of a Mediterranean tree species, Quercus suber, on the diversity, composition and network structure of soil fungal and bacterial communities in forests invaded by the exotic pathogen Phytophthora cinnamomi. The belowground footprint of pathogen-driven tree decline implied an increase in the taxonomic and phylogenetic diversity of both bacteria and fungi, but also a severe reduction of tree-symbiotic fungi and Proteobacteria known to have positive effects on plant growth and disease suppression. Moreover, we detected alterations of the topology of soil microbial networks in declining tree neighborhoods (lower connectivity, higher modularity), with implications for ecosystem function. Our findings reveal the large impacts that moderate levels of tree decline can have on the soil microbiome of invaded forests, and highlight the recovery of a functionally diverse and highly connected soil microbiome as a key target in the restoration of these disturbed systems.