Differential effects of pine wilt disease on root endosphere, rhizosphere, and soil microbiome of Korean white pine

ABSTRACT Pine wilt disease (PWD), caused by pinewood nematodes, is highly destructive to pine forests in Asia and Europe, including Korean white pine ( Pinus koraiensis ). The microbiome in the needles and trunk of Pinus spp. are recognized to play key roles in resistance against PWD. However, the role of root and soil microbiomes in the resistance remains unclear. This study compares bacterial and fungal communities in the root endosphere, rhizosphere soil, and bulk soil of diseased versus healthy P. koraiensis . Results showed that PWD increased the α-diversity of fungi in rhizosphere soil but did not affect the microbial diversity in the root endosphere or bulk soil. The composition of bacterial and fungal communities in rhizosphere and bulk soils was significantly altered by PWD. Specifically, the relative abundance of Planctomycetes decreased, and the relative abundance of Tremellomycetes increased, while Agaricomycetes decreased in both rhizosphere and bulk soils after infestation with PWD, respectively. Relative abundances of Chloroflexi and Verrucomicrobia increased, while Proteobacteria decreased in bulk soil following PWD. Relative abundances of Leotiomycetes and Eurotiomycetes increased in the rhizosphere soil and bulk soil following PWD, respectively. Furthermore, with the host plant infestation by PWD, the relative abundance of ectomycorrhizal fungi decreases, while that of saprotrophic fungi increases in both rhizosphere and bulk soils. Our results revealed that PWD significantly affects the soil microbiomes of P. koraiensis , with varying impacts across different plant–soil compartments. This study provides insights into how root and soil microbiomes respond to PWD, enhancing our understanding of the disease’s ecological consequences. IMPORTANCE The belowground microbiome is often sensitive to infection of forest diseases and is also recognized as a potential reservoir for selection of microbial agents against PWD. Our study demonstrates that the dynamics of belowground microbiome following natural infection of PWD are compartment and taxa specific, with varying degrees of responses in both diversity and composition of bacterial or fungal communities across the root endosphere, rhizosphere soil, and bulk soil. The results highlight the importance of utilizing appropriate plant–soil compartments and microbial taxa to understand the ecological consequences of the destructive PWD.