Abstract
The causal agents of Lyme disease in North America, Borrelia burgdorferi and Borrelia mayonii, are transmitted primarily by Ixodes scapularis ticks. Due to their limited metabolic capacity, spirochetes rely on the tick blood meal for nutrients and metabolic intermediates while residing in the tick vector, competing with the tick for nutrients in the blood meal. Metabolomics is an effective methodology to explore dynamics of spirochete survival and multiplication in tick vectors before transmission to a vertebrate host via tick saliva. Using gas chromatography coupled to mass spectrometry, we identified statistically significant differences in the metabolic profile among uninfected I. scapularis nymphal ticks, B. burgdorferi-infected nymphal ticks and B. mayonii-infected nymphal ticks by measuring metabolism every 24 hours over the course of their up to 96 hour blood meals. Specifically, differences in the abundance of purines, amino acids, carbohydrates, and fatty acids during the blood meal among the three groups of nymphal ticks suggest that B. mayonii and B. burgdorferi may have different metabolic capabilities, especially during later stages of nymphal feeding. Understanding mechanisms underlying variable metabolic requirements of different Lyme disease spirochetes within tick vectors could potentially aid development of novel methods to control spirochete transmission.
Highlights
The causal agents of Lyme disease in North America, Borrelia burgdorferi and Borrelia mayonii, are transmitted primarily by Ixodes scapularis ticks
Pathogens that are maintained exclusively in arthropod vector-vertebrate reservoir host transmission chains often have considerably limited metabolic capacity, requiring exploitation of major vector/reservoir host cell functions for the acquisition of metabolic intermediates for development[10,20]. This is the case for B. burgdorferi, which in the eastern United States is maintained in a transmission chain involving Ixodes ticks, I. scapularis, and various vertebrate reservoir hosts[21], and presumably for B. mayonii
We describe the metabolic phenotypes associated with infection by the Lyme disease spirochetes B. burgdorferi and B. mayonii in I. scapularis nymphal ticks
Summary
The causal agents of Lyme disease in North America, Borrelia burgdorferi and Borrelia mayonii, are transmitted primarily by Ixodes scapularis ticks. Lyme disease is the most commonly reported vector-borne disease in the United States, with more than 30,000 cases reported each year and indirect information sources indicating that the true numbers of annual Lyme disease cases are 10-fold higher[1,2,3] Most of these cases occur in the Northeast and Upper Midwest, caused by the spirochete Borrelia burgdorferi and transmitted to humans primarily by the nymphal stage of the blacklegged tick, Ixodes scapularis[4,5]. Pathogens that are maintained exclusively in arthropod vector-vertebrate reservoir host transmission chains often have considerably limited metabolic capacity, requiring exploitation of major vector/reservoir host cell functions for the acquisition of metabolic intermediates for development[10,20] This is the case for B. burgdorferi, which in the eastern United States is maintained in a transmission chain involving Ixodes ticks, I. scapularis, and various vertebrate reservoir hosts[21], and presumably for B. mayonii. The number of spirochetes within the tick gut remain at a low level during the first 24 hours of nymphal feeding[27,28], but increases exponentially as the feeding progresses[29], placing an increased metabolic demand on the tick
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