Spotted fever group Rickettsia infection kinetics and cutaneous host response during single tick feeding events
- 1Department of Microbiology and Immunology, Frederick P. Whiddon College of Medicine, University of South Alabama, Mobile, Alabama, United States of America
- 2Global Discovery Pathology & Multimodal Imaging, Translation Models Research Platform, Sanofi, Cambridge, Massachusetts, United States of America
- 3Department of Pathobiological Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, Louisiana, United States of America
Abstract
Rickettsia parkeri, an emerging tick-borne pathogen, is transmitted by Amblyomma maculatum. Initial bacterial inoculation occurs in the skin via infected tick bite. During blood acquisition, tick salivary factors manipulate host hemostatic and immune responses. Examination of rickettsial pathogenesis and the host response to infection in murine models primarily utilize needle inoculation. As a result, biological variables including transmission dynamics and the influence of vector saliva on the host response at the infection site are undefined. To test the hypothesis that a distinct host cutaneous immune response will be elicited based on the infection status of the tick, a single tick feeding model was developed to assess the transmission and dissemination kinetics of R. parkeri from the early stage of tick attachment (1 hour) to late feeding stage (144 hours). Furthermore, changes in the cutaneous immune response were characterized through immunophenotyping, cytokine and chemokine profiling, and histopathological analysis. The data show that transmission of R. parkeri from the infected tick to the host occurs within 1 hour-post tick attachment (hpa), with rapid dissemination to lymph nodes and internal tissues. The quantifiable bacterial load in the mouse skin delivered by an infected tick was 9,500 bacteria at 3 hours, increasing to 15,000 and 22,000 rickettsiae at 48 and 144 hours, respectively. Independent of tick infection status, the degree of time-dependent inflammation was similar at 3 and 48 hpa. However, in R. parkeri-infected skin at 144 hpa, macrophages were the dominant cell type, with enhanced levels of IFN-γ and TNF-α while IL-10 production was reduced. The data suggest delayed pro-inflammatory activation in response to rickettsial infection when delivered by ticks. This study yields valuable insights into the early events of Rickettsia transmission and the host response, providing the basis for the development of preventive strategies against tick-borne rickettsial disease. Author summary: Tick-borne diseases have become a significant public health concern in the United States over the past few decades, including spotted fever group Rickettsia. Rickettsia parkeri is transmitted to vertebrate hosts by ticks as they take a blood meal. Currently, the minimal time for rickettsial transmission from ticks, the number of rickettsiae inoculated by ticks, and the dissemination pattern to the host tissues, as well as the host response at the tick attachment site, is unknown. Accurate enumeration of rickettsiae delivered by a tick vector and the host response are critical for examining rickettsial pathogenesis and developing disease intervention strategies. Here, we use a natural tick vector and molecular techniques to determine the rickettsial inoculation dose at various timepoints. We observed that R. parkeri was transmitted to the host as early as 1 hour after tick feeding, and the inoculation dose by the tick vector is much lower than what is used in needle-inoculation studies. Additionally, we show the impact of tick feeding on the progress of skin inflammation and the host immune response over time at the tick attachment site. Our study provides new insights into rickettsial transmission and dissemination kinetics, the host response, and the interactions between the pathogen with its tick vector and vertebrate host.
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BibTeX
@article{suwanbongkot2026spotted,
title = {{Spotted fever group Rickettsia infection kinetics and cutaneous host response during single tick feeding events}},
author = {Chanakan Suwanbongkot and Ingeborg M. Langohr and Killian Z. Brewer and Robert A. Barrington and Kevin R. Macaluso},
journal = {PLOS Pathogens},
year = {2026},
month = sep,
doi = {10.1371/journal.ppat.1014626},
url = {https://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1014626},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Spotted fever group Rickettsia infection kinetics and cutaneous host response during single tick feeding events
AU - Chanakan Suwanbongkot
AU - Ingeborg M. Langohr
AU - Killian Z. Brewer
AU - Robert A. Barrington
AU - Kevin R. Macaluso
PY - 2026
DA - 2026/09/28
JO - PLOS Pathogens
DO - 10.1371/journal.ppat.1014626
UR - https://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1014626
AB - Rickettsia parkeri, an emerging tick-borne pathogen, is transmitted by Amblyomma maculatum. Initial bacterial inoculation occurs in the skin via infected tick bite. During blood acquisition, tick salivary factors manipulate host hemostatic and immune responses. Examination of rickettsial pathogenesis and the host response to infection in murine models primarily utilize needle inoculation. As a result, biological variables including transmission dynamics and the influence of vector saliva on the host response at the infection site are undefined. To test the hypothesis that a distinct host cutaneous immune response will be elicited based on the infection status of the tick, a single tick feeding model was developed to assess the transmission and dissemination kinetics of R. parkeri from the early stage of tick attachment (1 hour) to late feeding stage (144 hours). Furthermore, changes in the cutaneous immune response were characterized through immunophenotyping, cytokine and chemokine profiling, and histopathological analysis. The data show that transmission of R. parkeri from the infected tick to the host occurs within 1 hour-post tick attachment (hpa), with rapid dissemination to lymph nodes and internal tissues. The quantifiable bacterial load in the mouse skin delivered by an infected tick was 9,500 bacteria at 3 hours, increasing to 15,000 and 22,000 rickettsiae at 48 and 144 hours, respectively. Independent of tick infection status, the degree of time-dependent inflammation was similar at 3 and 48 hpa. However, in R. parkeri-infected skin at 144 hpa, macrophages were the dominant cell type, with enhanced levels of IFN-γ and TNF-α while IL-10 production was reduced. The data suggest delayed pro-inflammatory activation in response to rickettsial infection when delivered by ticks. This study yields valuable insights into the early events of Rickettsia transmission and the host response, providing the basis for the development of preventive strategies against tick-borne rickettsial disease. Author summary: Tick-borne diseases have become a significant public health concern in the United States over the past few decades, including spotted fever group Rickettsia. Rickettsia parkeri is transmitted to vertebrate hosts by ticks as they take a blood meal. Currently, the minimal time for rickettsial transmission from ticks, the number of rickettsiae inoculated by ticks, and the dissemination pattern to the host tissues, as well as the host response at the tick attachment site, is unknown. Accurate enumeration of rickettsiae delivered by a tick vector and the host response are critical for examining rickettsial pathogenesis and developing disease intervention strategies. Here, we use a natural tick vector and molecular techniques to determine the rickettsial inoculation dose at various timepoints. We observed that R. parkeri was transmitted to the host as early as 1 hour after tick feeding, and the inoculation dose by the tick vector is much lower than what is used in needle-inoculation studies. Additionally, we show the impact of tick feeding on the progress of skin inflammation and the host immune response over time at the tick attachment site. Our study provides new insights into rickettsial transmission and dissemination kinetics, the host response, and the interactions between the pathogen with its tick vector and vertebrate host.
SN - 1553-7374
ER -