Living with chronic infection: Persistent immunomodulation during avirulent haemoparasitic infection in a wild rodent

Taylor, Christopher H.; Friberg, Ida M; Jackson, Joseph A.; Arriero, Elena; Begon, Mike; Wanelik, Klara M.; Paterson, Steve; Bradley, Janette E; Friberg, Ida M.; Bradley, Janette E.

Abstract

Apicomplexans are a protozoan phylum of obligate parasites which may be highly virulent during acute infections, but may also persist as chronic infections which appear to have little fitness cost. Babesia microti is an apicomplexan haemoparasite that, in immunocompromised individuals, can cause severe, potentially fatal disease. However, in its natural host, wild field voles (Microtus agrestis), it exhibits chronic infections that have no detectable impact on survival or female fecundity. How is damage minimized, and what is the impact on the host's immune state and health? We examine the differences in immune state (here represented by expression of immune‐related genes in multiple tissues) associated with several common chronic infections in a population of wild field voles. While some infections show little impact on immune state, we find strong associations between immune state and B. microti. These include indications of clearance of infected erythrocytes (increased macrophage activity in the spleen) and activity likely associated with minimizing damage from the infection (anti‐inflammatory and antioxidant activity in the blood). By analysing gene expression from the same individuals at multiple time points, we show that the observed changes are a response to infection, rather than a risk factor. Our results point towards continual investment to minimize the damage caused by the infection. Thus, we shed light on how wild animals can tolerate some chronic infections, but emphasize that this tolerance does not come without a cost.

Citation

Taylor, C. H., Friberg, I. M., Jackson, J. A., Arriero, E., Begon, M., Wanelik, K. M., Paterson, S., Bradley, J. E., Friberg, I. M., & Bradley, J. E. (2023). Living with chronic infection: Persistent immunomodulation during avirulent haemoparasitic infection in a wild rodent. Molecular Ecology, 32(5), 1197-1210. https://doi.org/10.1111/mec.16819

• Journal Article Type: Article
• Acceptance Date: Nov 30, 2022
• Online Publication Date: Dec 8, 2022
• Publication Date: 2023-03
• Deposit Date: Feb 15, 2023
• Publicly Available Date: Feb 21, 2023
• Journal: Molecular Ecology
• Print ISSN: 0962-1083
• Electronic ISSN: 1365-294X
• Publisher: Wiley
• Peer Reviewed: Peer Reviewed
• Volume: 32
• Issue: 5
• Pages: 1197-1210
• DOI: https://doi.org/10.1111/mec.16819
• Keywords: Babesia microti, chronic infection, immune state, longitudinal sampling, Microtus agrestis, wild immunology
• Public URL: https://nottingham-repository.worktribe.com/output/15431413
• Publisher URL: https://onlinelibrary.wiley.com/doi/10.1111/mec.16819