Variation among strains of Borrelia burgdorferi in host tissue abundance and lifetime transmission determine the population strain structure in nature
- DOI
- Language of the publication
- English
- Date
- 2023-08-22
- Type
- Article
- Author(s)
- Zinck, Christopher B.
- Raveendram Thampy, Prasobh
- Uhlemann, Eva-Maria E.
- Adam, Hesham
- Wachter, Jenny
- Suchan, Danae
- Cameron, Andrew D. S.
- Rego, Ryan O. M.
- Brisson, Dustin
- Bouchard, Catherine
- Ogden, Nicholas H.
- Voordouw, Maarten J.
- Publisher
- Public Library of Science (PLoS)
Abstract
Pathogen life history theory assumes a positive relationship between pathogen load in host tissues and pathogen transmission. Empirical evidence for this relationship is surprisingly rare due to the difficulty of measuring transmission for many pathogens. The comparative method, where a common host is experimentally infected with a set of pathogen strains, is a powerful approach for investigating the relationships between pathogen load and transmission. The validity of such experimental estimates of strain-specific transmission is greatly enhanced if they can predict the pathogen population strain structure in nature. Borrelia burgdorferi is a multi-strain, tick-borne spirochete that causes Lyme disease in North America. This study used 11 field-collected strains of B. burgdorferi, a rodent host (Mus musculus, C3H/HeJ) and its tick vector (Ixodes scapularis) to determine the relationship between pathogen load in host tissues and lifetime host-to-tick transmission (HTT). Mice were experimentally infected via tick bite with 1 of 11 strains. Lifetime HTT was measured by infesting mice with I. scapularis larval ticks on 3 separate occasions. The prevalence and abundance of the strains in the mouse tissues and the ticks were determined by qPCR. We used published databases to obtain estimates of the frequencies of these strains in wild I. scapularis tick populations. Spirochete loads in ticks and lifetime HTT varied significantly among the 11 strains of B. burgdorferi. Strains with higher spirochete loads in the host tissues were more likely to infect feeding larval ticks, which molted into nymphal ticks that had a higher probability of B. burgdorferi infection (i.e., higher HTT). Our laboratory-based estimates of lifetime HTT were predictive of the frequencies of these strains in wild I. scapularis populations. For B. burgdorferi, the strains that establish high abundance in host tissues and that have high lifetime transmission are the strains that are most common in nature.
Plain language summary
For many pathogens, the benefit of higher abundance in host tissues is better transmission to uninfected hosts. Evidence for this relationship is rare because measuring pathogen transmission is difficult. Experimental infection with different pathogen strains in the same animal host allows scientists to test the relationship between abundance in host tissues versus transmission. We performed such a study using the tick-borne bacterium Borrelia burgdorferi, which causes Lyme disease in humans in North America. Laboratory mice were infected with 1 of 11 different strains of B. burgdorferi and ticks were fed on these mice to measure host-to-tick transmission. We determined the presence and abundance of B. burgdorferi in the mouse tissues and in the ticks using basic molecular methods. We found that strains with higher abundance in the mouse tissues had higher lifetime transmission to feeding ticks. We used published databases to obtain approximate estimates of the frequencies of our strains in nature. We found that strains that had higher transmission in the laboratory were also more common in nature. Studies that compare strain fitness between the lab versus nature can help scientists understand the evolution of multi-strain pathogens in response to human control measures.
Subject
- Health
Rights
Peer review
Yes
Identifiers
- PubMed ID
- 37607182
- ISSN
- 1553-7374
Article
- Journal title
- PLoS Pathogens
- Journal volume
- 19
- Journal issue
- 8
Citation(s)
Zinck, C. B., Raveendram Thampy, P., Uhlemann, E. E., Adam, H., Wachter, J., Suchan, D., Cameron, A. D. S., Rego, R. O. M., Brisson, D., Bouchard, C., Ogden, N. H., & Voordouw, M. J. (2023). Variation among strains of Borrelia burgdorferi in host tissue abundance and lifetime transmission determine the population strain structure in nature. PLoS pathogens, 19(8), e1011572. https://doi.org/10.1371/journal.ppat.1011572