JDoonan_table S1_ESM.xlsx from Host–microbiota–insect interactions drive emergent virulence in a complex tree disease

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 incoluations 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 <i>Agrilus biguttatus</i>. We identified expression of key pathogenicity genes in <i>Brenneria goodwinii</i>, 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 <i>Agrilus</i> larvae. This study highlights the emergent properties of complex host–pathobiota–insect interactions that underlie the pathology of diseases that threaten global forest biomes.

由气候扰动、虫害与病原微生物引发的森林衰退正威胁着全球生态景观，而树木病害愈发被归因于宿主、微生物群与昆虫之间复杂生态互作的涌现特性（emergent properties）。为验证这一假说，本研究将还原论方法（reductionist approaches，即单物种与多物种细菌培养）与涌现论方法（emergentist approaches，即在添加昆虫幼虫的橡树感染模型中开展细菌接种）相结合，以阐明急性橡树衰退（Acute Oak Decline, AOD）病害系统（pathosystem）中宿主-微生物群-昆虫互作的基因表达图谱与症状严重程度。急性橡树衰退（AOD）是一类复杂的衰退病害，其特征为存在易感非生物因子、由细菌病原生物组（bacterial pathobiome）驱动的内皮损伤，以及蛀皮甲虫双斑吉丁虫（*Agrilus biguttatus*）的幼虫坑道。本研究在AOD病原生物组的优势成员——古德温氏布伦纳菌（*Brenneria goodwinii*）中，鉴定出关键致病基因的表达情况，获得了组织特异性基因表达谱，明确了其与其他细菌病原生物组成员在糖代谢过程中的协同作用，并证实当存在双斑吉丁虫（*Agrilus*）幼虫时，致病基因的表达会出现上调。本研究揭示了复杂宿主-病原生物组-昆虫互作的涌现特性，而这些特性正是威胁全球森林生物群落的病害病理的核心基础。