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Infection of an Insect Vector with a Bacterial Plant Pathogen Increases Its Propensity for Dispersal.

ABSTRACT: The spread of vector-transmitted pathogens relies on complex interactions between host, vector and pathogen. In sessile plant pathosystems, the spread of a pathogen highly depends on the movement and mobility of the vector. However, questions remain as to whether and how pathogen-induced vector manipulations may affect the spread of a plant pathogen. Here we report for the first time that infection with a bacterial plant pathogen increases the probability of vector dispersal, and that such movement of vectors is likely manipulated by a bacterial plant pathogen. We investigated how Candidatus Liberibacter asiaticus (CLas) affects dispersal behavior, flight capacity, and the sexual attraction of its vector, the Asian citrus psyllid (Diaphorina citri Kuwayama). CLas is the putative causal agent of huanglongbing (HLB), which is a disease that threatens the viability of commercial citrus production worldwide. When D. citri developed on CLas-infected plants, short distance dispersal of male D. citri was greater compared to counterparts reared on uninfected plants. Flight by CLas-infected D. citri was initiated earlier and long flight events were more common than by uninfected psyllids, as measured by a flight mill apparatus. Additionally, CLas titers were higher among psyllids that performed long flights than psyllid that performed short flights. Finally, attractiveness of female D. citri that developed on infected plants to male conspecifics increased proportionally with increasing CLas bacterial titers measured within female psyllids. Our study indicates that the phytopathogen, CLas, may manipulate movement and mate selection behavior of their vectors, which is a possible evolved mechanism to promote their own spread. These results have global implications for both current HLB models of disease spread and control strategies.

SUBMITTER: Martini X

PROVIDER: S-EPMC4471203 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Infection of an Insect Vector with a Bacterial Plant Pathogen Increases Its Propensity for Dispersal.

Martini Xavier X Hoffmann Mark M Coy Monique R MR Stelinski Lukasz L LL Pelz-Stelinski Kirsten S KS

PloS one 20150617 6

The spread of vector-transmitted pathogens relies on complex interactions between host, vector and pathogen. In sessile plant pathosystems, the spread of a pathogen highly depends on the movement and mobility of the vector. However, questions remain as to whether and how pathogen-induced vector manipulations may affect the spread of a plant pathogen. Here we report for the first time that infection with a bacterial plant pathogen increases the probability of vector dispersal, and that such movem ...[more]

PMID: 26083763

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Project description: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. "Candidatus Liberibacter asiaticus" (CLas) is transmitted in a persistent, circulative, and propagative manner. The genome of CLas 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 in CLas-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 that CLas stimulated Diaphorina citri to 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 in CLas-infected D. citri psyllids. Survival analysis confirmed a shorter life span for CLas-infected D. citri psyllids. 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 that CLas-infected psyllids were at a higher hunger level and they tended to forage more often. This increased feeding activity reflects the CLas-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.IMPORTANCE Insect 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, "Candidatus Liberibacter asiaticus" (CLas) can take up energetic nucleotides, such as ATP, from its vector, Diaphorina citri, using ATP translocase. In this study, we found that the CLas pathogen manipulates the energy metabolism of its insect vector. The accumulation of ATP in CLas-infected D. citri psyllids indicated that CLas 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.

Project description:AimUnderstanding how spatial scale of study affects observed dispersal patterns can provide insights into spatiotemporal population dynamics, particularly in systems with significant long-distance dispersal (LDD). We aimed to investigate the dispersal gradients of two rusts of wheat with spores of similar size, mass, and shape, over multiple spatial scales. We hypothesized that a single dispersal kernel could fit the dispersal from all spatial scales well, and that it would be possible to obtain similar results in spatiotemporal increase of disease when modeling based on differing scales.LocationCentral Oregon and St. Croix Island.TaxaPuccinia striiformis f. sp. tritici, Puccinia graminis f. sp. tritici, Triticum aestivum.MethodsWe compared empirically-derived primary disease gradients of cereal rust across three spatial scales: local (inoculum source and sampling unit = 0.0254 m, spatial extent = 1.52m) field-wide (inoculum source = 1.52 m, sampling unit = 0.305 m, and spatial extent = 91.44 m), and regional (inoculum source and sampling unit = 152 m, spatial extent = 10.7 km). We then examined whether disease spread in spatially explicit simulations depended upon the scale at which data were collected by constructing a compartmental time-step model.ResultsThe three data sets could be fit well by a single inverse-power law dispersal kernel. Simulating epidemic spread at different spatial resolutions resulted in similar patterns of spatiotemporal spread. Dispersal kernel data obtained at one spatial scale can be used to represent spatiotemporal disease spread at a larger spatial scale.Main conclusionsOrganisms spread by aerially dispersed small propagules that exhibit LDD may follow similar dispersal patterns over a several hundred- or thousand-fold expanse of spatial scale. Given that the primary mechanisms driving aerial dispersal remain constant, it may be possible to extrapolate across scales when empirical data are unavailable at a scale of interest.

Dataset Information

Infection of an Insect Vector with a Bacterial Plant Pathogen Increases Its Propensity for Dispersal.

Publications

Infection of an Insect Vector with a Bacterial Plant Pathogen Increases Its Propensity for Dispersal.

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