Metabolic Interplay between the Asian Citrus Psyllid and Its Profftella 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.

[1]  A. Fereres,et al.  A Plant Virus Manipulates the Behavior of Its Whitefly Vector to Enhance Its Transmission Efficiency and Spread , 2013, PloS one.

[2]  Seth M. Barribeau,et al.  Immunity and other defenses in pea aphids, Acyrthosiphon pisum , 2010, Genome Biology.

[3]  R. Shatters,et al.  Localization of Candidatus Liberibacter asiaticus, Associated with Citrus Huanglongbing Disease, in its Psyllid Vector using Fluorescence in situ Hybridization , 2011 .

[4]  G. J. Blomquist,et al.  Comparative aspects of propionate metabolism. , 1989, Comparative biochemistry and physiology. B, Comparative biochemistry.

[5]  R. Aebersold,et al.  A statistical model for identifying proteins by tandem mass spectrometry. , 2003, Analytical chemistry.

[6]  P. Cossart,et al.  How bacterial pathogens colonize their hosts and invade deeper tissues. , 2015, Microbes and infection.

[7]  Alexey I Nesvizhskii,et al.  Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. , 2002, Analytical chemistry.

[8]  L. Stelinski,et al.  Glutathione Transferase and Cytochrome P450 (General Oxidase) Activity Levels in Candidatus Liberibacter Asiaticus-Infected and Uninfected Asian Citrus Psyllid (Hemiptera: Psyllidae) , 2011 .

[9]  Michael G Thomas,et al.  Biosynthesis of polyketide synthase extender units. , 2009, Natural product reports.

[10]  ScienceDirect Comparative biochemistry and physiology. B, Comparative biochemistry , 1993 .

[11]  S. Eigenbrode,et al.  Plant viruses alter insect behavior to enhance their spread , 2012, Scientific Reports.

[12]  A. Douglas Phloem-sap feeding by animals: problems and solutions. , 2006, Journal of experimental botany.

[13]  C. Slupsky,et al.  Metabolomic analysis of citrus infection by 'Candidatus Liberibacter' reveals insight into pathogenicity. , 2012, Journal of proteome research.

[14]  Jörn Piel,et al.  A polyketide synthase-peptide synthetase gene cluster from an uncultured bacterial symbiont of Paederus beetles , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Jörn Piel,et al.  Biosynthesis of polyketides by trans-AT polyketide synthases. , 2016, Natural product reports.

[16]  Yun-Ru Chen,et al.  Analysis of chitin-binding proteins from Manduca sexta provides new insights into evolution of peritrophin A-type chitin-binding domains in insects. , 2015, Insect biochemistry and molecular biology.

[17]  Wenbin Li,et al.  Quantitative real-time PCR for detection and identification of Candidatus Liberibacter species associated with citrus huanglongbing. , 2006, Journal of microbiological methods.

[18]  T. Ebert,et al.  Transmission Parameters for Candidatus Liberibacter asiaticus by Asian Citrus Psyllid (Hemiptera: Psyllidae) , 2010, Journal of economic entomology.

[19]  Cecilia Tamborindeguy,et al.  Transcriptome analyses of Bactericera cockerelli adults in response to “Candidatus Liberibacter solanacearum” infection , 2012, Molecular Genetics and Genomics.

[20]  H. Doddapaneni,et al.  Complete genome sequence of citrus huanglongbing bacterium, 'Candidatus Liberibacter asiaticus' obtained through metagenomics. , 2009, Molecular plant-microbe interactions : MPMI.

[21]  O. Steele‐Mortimer Exploitation of the Ubiquitin System by Invading Bacteria , 2011, Traffic.

[22]  Y. P. Jiang Purification of Mycoplasma-like Organisms from Lettuce with Aster Yellows Disease , 1987 .

[23]  Andrew R. Jones,et al.  ProteomeXchange provides globally co-ordinated proteomics data submission and dissemination , 2014, Nature Biotechnology.

[24]  M. Fawaz,et al.  The ATP-grasp enzymes. , 2011, Bioorganic chemistry.

[25]  Johannes Griss,et al.  The Proteomics Identifications (PRIDE) database and associated tools: status in 2013 , 2012, Nucleic Acids Res..

[26]  J. Bové,et al.  Huanglongbing: a destructive, newly-emerging, century-old disease of citrus [Asia; South Africa; Brazil; Florida] , 2006 .

[27]  Moriya Ohkuma,et al.  Defensive Bacteriome Symbiont with a Drastically Reduced Genome , 2013, Current Biology.

[28]  M. Mclaughlin,et al.  A comparison of protein extraction methods suitable for gel-based proteomic studies of aphid proteins. , 2009, Journal of biomolecular techniques : JBT.

[29]  F. L. Cônsoli,et al.  Population Dynamics and Growth Rates of Endosymbionts During Diaphorina citri (Hemiptera, Liviidae) Ontogeny , 2014, Microbial Ecology.

[30]  J. Piel Biosynthesis of polyketides by trans-AT polyketide synthases. , 2010, Natural product reports.

[31]  H. Alborn,et al.  Induced Release of a Plant-Defense Volatile ‘Deceptively’ Attracts Insect Vectors to Plants Infected with a Bacterial Pathogen , 2012, PLoS pathogens.

[32]  K. Reynolds,et al.  Polyketide synthase acyl carrier protein (ACP) as a substrate and a catalyst for malonyl ACP biosynthesis. , 1999, Chemistry & biology.