Unraveling the shifts in the belowground microbiota and metabolome of Pinus pinaster trees affected by forest decline

Pinus pinaster Aiton (maritime pine) stands are suffering a generalized deterioration due to different decline episodes throughout all its distribution area. It is well known that external disturbances can alter the plant associated microbiota and metabolome, which ultimately can entail the disruption of the normal growth of the hosts. Notwithstanding, very little is known about the shifts in the microbiota and the metabolome in pine trees affected by decline. The aim of our work was to unravel whether bacterial and fungal communities inhabiting the rhizosphere and root endosphere of P. pinaster trees with symptoms of decline and affected by Matsucoccus feytaudi in the National Park of Sierra Nevada (Granada, Spain) showed alterations in the structure, taxonomical profiles and associative patterns. We also aimed at deciphering potential changes in the rhizosphere and root metabolome. Trees infected by M. feytaudi and healthy individual harbored distinct microbial communities at both compositional and associative patterns. Unhealthy trees were enriched selectively in certain plant growth promoting microorganisms such as several ectomycorrhizal fungi (Clavulina) and Streptomyces, while other beneficial microorganisms (Micromonospora) were more abundant in unaffected pines. The rhizosphere of unhealthy trees was richer in secondary metabolites involved in plant defense than healthy pines, while the opposite trend was detected in root samples. The abundance of certain microorganisms was significantly correlated with several antimicrobial metabolites, thus, being all of them worthy of further isolation and study of their role in forest decline.