title: A Plant Bacterial Pathogen Manipulates Its Insect Vector's Energy Metabolism.
abstract: Insect-transmitted plant-pathogenic bacteria may alter their vectors' fitness, survival, behavior, and metabolism. Because these pathogens interact with their vectors on the cellular and organismal levels, potential changes at the biochemical level might occur. "CandidatusLiberibacter asiaticus" (CLas) is transmitted in a persistent, circulative, and propagative manner. The genome ofCLas revealed the presence of an ATP translocase that mediates the uptake of ATP and other nucleotides from medium to achieve its biological processes, such as growth and multiplication. Here, we showed that the levels of ATP and many other nucleotides were significantly higher inCLas-infected than healthy psyllids. Gene expression analysis showed upregulation for ATP synthase subunits, while ATPase enzyme activity showed a decrease in ATPase activity. These results indicated thatCLas stimulatedDiaphorina citrito produce more ATP and many other energetic nucleotides, while it may inhibit their consumption by the insect. As a result of ATP accumulation, the adenylated energy charge (AEC) increased and the AMP/ATP and ADP/ATP ratios decreased inCLas-infectedD. citripsyllids. Survival analysis confirmed a shorter life span forCLas-infectedD. citripsyllids. In addition, electropenetrography showed a significant reduction in total nonprobing time, salivation time, and time from the last E2 (phloem ingestion) to the end of recording, indicating thatCLas-infected psyllids were at a higher hunger level and they tended to forage more often. This increased feeding activity reflects theCLas-induced energetic stress. In conclusion,CLas alters the energy metabolism of its psyllid vector,D. citri, in order to secure its need for energetic nucleotides.IMPORTANCEInsect transmission of plant-pathogenic bacteria involves propagation and circulation of the bacteria within their vectors. The transmission process is complex and requires specific interactions at the molecular and biochemical levels. The growth of the plant-pathogenic bacteria in the hemolymph of their vectors indicated that the hemolymph contains all the necessary nutrients for their growth. In addition to nutrients, "CandidatusLiberibacter asiaticus" (CLas) can take up energetic nucleotides, such as ATP, from its vector,Diaphorina citri, using ATP translocase. In this study, we found that theCLas pathogen manipulates the energy metabolism of its insect vector. The accumulation of ATP inCLas-infectedD. citripsyllids indicated thatCLas induces ATP production to fulfill its need for this energetic compound. As a result of ATP accumulation, a shorter life span and altered feeding behavior were observed. These findings increase our knowledge of insect transmission of the persistent-circulative-propagative type of plant pathogens vectored by insects.
authors.affiliation: Plant Pathology Department, Citrus Research and Education Center, University of Florida, Lake Alfred, Florida, USA nabilkilliny@ufl.edu.
authors.forename: Nabil
authors.identifier: http://orcid.org/0000-0002-3895-6943
authors.initials: N
authors.lastname: Killiny
authors.affiliation: Plant Pathology Department, Citrus Research and Education Center, University of Florida, Lake Alfred, Florida, USA.
authors.forename: Faraj
authors.initials: F
authors.lastname: Hijaz
authors.affiliation: Entomology and Nematology Department, Citrus Research and Education Center, University of Florida, Lake Alfred, Florida, USA.
authors.forename: Timothy A
authors.initials: TA
authors.lastname: Ebert
authors.affiliation: Entomology and Nematology Department, Citrus Research and Education Center, University of Florida, Lake Alfred, Florida, USA.
authors.forename: Michael E
authors.initials: ME
authors.lastname: Rogers
mesh_terms: D000251:Adenosine Triphosphatases / Q000378:metabolism; D000255:Adenosine Triphosphate / Q000378:metabolism; D000818:Animals; D002957:Citrus / Q000382:microbiology; D004734:Energy Metabolism; D057075:Enzyme Assays; D020558:GTP Phosphohydrolases / Q000378:metabolism; D005786:Gene Expression Regulation; D006430:Hemiptera / Q000235:genetics / Q000378:metabolism* / Q000382:microbiology*; D006458:Hemolymph / Q000378:metabolism / Q000382:microbiology; D054884:Host-Pathogen Interactions / Q000502:physiology*; D007303:Insect Vectors / Q000382:microbiology* / Q000502:physiology*; D009711:Nucleotides / Q000378:metabolism; D010935:Plant Diseases / Q000382:microbiology; D012230:Rhizobiaceae / Q000254:growth & development / Q000378:metabolism* / Q000472:pathogenicity; D013534:Survival
chemical_list: D009711:Nucleotides; D000255:Adenosine Triphosphate; D000251:Adenosine Triphosphatases; D020558:GTP Phosphohydrolases
keywords: ATP; Diaphorina citri; HPLC; adenylated energy charge; electric penetration graph; electropenetrography; huanglongbing; “Candidatus Liberibacter asiaticus,” energy metabolism