|Ramsey, John - John|
|JOHNSON, RICHARD - University Of Washington|
|HOKI, JASON - Cornell University|
|KRUSE, ANGELA - Cornell University|
|MAHONEY, JACLYN - Boyce Thompson Institute|
|SHROEDER, FRANK - Boyce Thompson Institute|
|MACCOSS, MICHAEL - University Of Washington|
Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/22/2015
Publication Date: 11/18/2015
Citation: Ramsey, J.S., Johnson, R., Hoki, J., Kruse, A., Mahoney, J., Hilf, M.E., Hunter, W.B., Hall, D.G., Shroeder, F., Maccoss, M., Cilia, M. 2015. Metabolic interplay between the Asian citrus psyllid and its Profftella symbiont: An Achilles’ heel of the citrus greening insect vector. PLoS One. DOI: 10.1371/journal.pone.0140826.
Interpretive Summary: Citrus greening disease (also known as Huanglongbing) is associated with ‘Candidatus Liberibacter asiaticus’ (CLas), a non-culturable bacterial pathogen transmitted by the Asian citrus psyllid (Diaphorina citri). The worldwide distribution of this citrus disease has caused extreme economic damage. The pathogen has spread throughout the state of Florida in the last decade, and has recently emerged in California and Texas. CLas must circulate throughout the body of insect to be transmitted as a component of saliva during feeding, invading cells in multiple insect organs in the process. We measured protein changes in the insect vector associated with feeding on infected citrus plants and acquiring the citrus greening pathogen. Proteins associated with defense, immunity, and metabolism varied in abundance between CLas(+) and CLas(-) insects, as did membrane and cytoskeleton proteins associated with microbial invasion into animal tissues. The endosymbiotic bacterium ‘Candidatus Profftella armatura’ resides within specialized insect cells and produces large amounts of a polyketide toxin. Proteins involved in the biosynthesis of this toxin were found to be up-regulated in CLas(+) insects, and mass spectrometry was used to reveal differences in polyketide abundance between CLas(+) and CLas(-) D. citri. Specific interactions between Profftella and D. citri represent promising control targets to stop the spread of citrus greening disease by the insect vector.
Technical Abstract: ‘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. Insect proteins differentially expressed between CLas(+) and CLas(-) D. citri include 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.