Metabolic Interplay between the Asian Citrus Psyllid and Its <i>Profftella</i> Symbiont: An Achilles’ Heel of the Citrus Greening Insect Vector

‘Candidatus Liberibacter asiaticus’ (CLas), the bacterial pathogen associated with citrus greening disease, is transmitted by Diaphorina citri, the Asian citrus psyllid. Interactions among D. citri and its microbial endosymbionts, including ‘Candidatus Profftella armatura’, are likely to impact transmission of CLas. We used quantitative mass spectrometry to compare the proteomes of CLas(+) and CLas(-) populations of D. citri, and found that proteins involved in polyketide biosynthesis by the endosymbiont Profftella were up-regulated in CLas(+) insects. Mass spectrometry analysis of the Profftella polyketide diaphorin in D. citri metabolite extracts revealed the presence of a novel diaphorin-related polyketide and the ratio of these two polyketides was changed in CLas(+) insects. Insect proteins differentially expressed between CLas(+) and CLas(-) D. citri included defense and immunity proteins, proteins involved in energy storage and utilization, and proteins involved in endocytosis, cellular adhesion, and cytoskeletal remodeling which are associated with microbial invasion of host cells. Insight into the metabolic interdependence between the insect vector, its endosymbionts, and the citrus greening pathogen reveals novel opportunities for control of this disease, which is currently having a devastating impact on citrus production worldwide.亚洲韧皮部杆菌（Candidatus Liberibacter asiaticus，CLas）是与柑橘黄龙病相关的细菌性病原菌，其传播媒介为亚洲柑橘木虱（Diaphorina citri）。亚洲柑橘木虱与其包括Candidatus Profftella armatura在内的微生物内共生体之间的互作，可能会影响CLas的传播。本研究采用定量质谱法（quantitative mass spectrometry）比较了携带CLas（CLas(+)）与不携带CLas（CLas(-)）的亚洲柑橘木虱种群的蛋白质组，发现内共生体普罗夫特氏菌参与聚酮化合物生物合成的相关蛋白在带菌木虱体内显著上调。通过对亚洲柑橘木虱代谢提取物中的普罗夫特氏菌聚酮化合物双菌素（diaphorin）开展质谱分析，本研究鉴定出一种新型双菌素相关聚酮化合物，且两类聚酮化合物的相对比例在携带CLas的木虱体内发生显著改变。携带CLas与不携带CLas的亚洲柑橘木虱之间差异表达的昆虫蛋白涵盖防御与免疫相关蛋白、能量储存与利用相关蛋白，以及与宿主细胞微生物入侵过程相关的内吞作用、细胞黏附及细胞骨架重塑相关蛋白。本研究对媒介昆虫、其体内内共生体与柑橘黄龙病病原菌之间的代谢依存关系的解析，为当前正对全球柑橘产业造成毁灭性冲击的该病害防控提供了全新思路。