TY - JOUR

T1 - Host–microbiota–insect interactions drive emergent virulence in a complex tree disease

AU - Doonan, James

AU - Broberg, Martin

AU - Denman, Sandra

AU - McDonald, James

PY - 2020/8/26

Y1 - 2020/8/26

N2 - Forest declines caused by climate disturbance, insect pests and microbial pathogens threaten the global landscape, and tree diseases are increasingly attributed to the emergent properties of complex ecological interactions between the host, microbiota and insects. To address this hypothesis, we combined reductionist approaches (single and polyspecies bacterial cultures) with emergentist approaches (bacterial inoculations in an oak infection model with the addition of insect larvae) to unravel the gene expression landscape and symptom severity of host–microbiota–insect interactions in the acute oak decline (AOD) pathosystem. AOD is a complex decline disease characterized by predisposing abiotic factors, inner bark lesions driven by a bacterial pathobiome, and larval galleries of the bark-boring beetle Agrilus biguttatus. We identified expression of key pathogenicity genes in Brenneria goodwinii, the dominant member of the AOD pathobiome, tissue-specific gene expression profiles, cooperation with other bacterial pathobiome members in sugar catabolism, and demonstrated amplification of pathogenic gene expression in the presence of Agrilus larvae. This study highlights the emergent properties of complex host–pathobiota–insect interactions that underlie the pathology of diseases that threaten global forest biomes.

AB - Forest declines caused by climate disturbance, insect pests and microbial pathogens threaten the global landscape, and tree diseases are increasingly attributed to the emergent properties of complex ecological interactions between the host, microbiota and insects. To address this hypothesis, we combined reductionist approaches (single and polyspecies bacterial cultures) with emergentist approaches (bacterial inoculations in an oak infection model with the addition of insect larvae) to unravel the gene expression landscape and symptom severity of host–microbiota–insect interactions in the acute oak decline (AOD) pathosystem. AOD is a complex decline disease characterized by predisposing abiotic factors, inner bark lesions driven by a bacterial pathobiome, and larval galleries of the bark-boring beetle Agrilus biguttatus. We identified expression of key pathogenicity genes in Brenneria goodwinii, the dominant member of the AOD pathobiome, tissue-specific gene expression profiles, cooperation with other bacterial pathobiome members in sugar catabolism, and demonstrated amplification of pathogenic gene expression in the presence of Agrilus larvae. This study highlights the emergent properties of complex host–pathobiota–insect interactions that underlie the pathology of diseases that threaten global forest biomes.

U2 - 10.1098/rspb.2020.0956

DO - 10.1098/rspb.2020.0956

M3 - Article

VL - 287

JO - Proceedings of the Royal Society B: Biological Sciences

JF - Proceedings of the Royal Society B: Biological Sciences

SN - 0962-8452

IS - 1933

M1 - 20200956

ER -