Microbial genetic variation impacts host eco-immunological strategies and microparasite fitness in Lyme borreliae-reptile system
Tolerance and resistance are two host eco-immunological strategies in response to microparasite invasion. In the strategy of “resistance”, host responses are induced to decrease microparasite replication while the “tolerance” strategy allows hosts coexistence with microparasites by minimizing respon...
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| Format: | Article |
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Elsevier
2024-11-01
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| Series: | Ticks and Tick-Borne Diseases |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S1877959X24001031 |
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| author | Tristan A. Nowak Carly Fernandes Jill Malfetano Erica Lasek-Nesselquist Matthew Combs Klemen Strle Russell L. Burke Yi-Pin Lin |
| author_facet | Tristan A. Nowak Carly Fernandes Jill Malfetano Erica Lasek-Nesselquist Matthew Combs Klemen Strle Russell L. Burke Yi-Pin Lin |
| author_sort | Tristan A. Nowak |
| collection | DOAJ |
| description | Tolerance and resistance are two host eco-immunological strategies in response to microparasite invasion. In the strategy of “resistance”, host responses are induced to decrease microparasite replication while the “tolerance” strategy allows hosts coexistence with microparasites by minimizing responses to avoid immune-mediated damage. The causative agent of Lyme disease is a group of genotypically diverse bacterial species, Borrelia burgdorferi sensu lato (Bb), which is transmitted by Ixodes ticks and persists in different reservoir animals. In North America, eastern fence lizards (Sceloporus undulatus) can be fed on by Ixodes ticks but are incompetent to one genotype of Bb (i.e., ospC type A). However, field-collected lizards showed evidence of previous infection by Bb strains with undefined genotypes. Supporting this evidence, we introduced three genotypically different Bb strains individually to eastern fence lizards and found a Bb genotype-dependent manner of infectivity. We compared liver transcriptomics and observed elevated immune responses triggered by a lizard-incompetent Bb strain (strain B31). We showed two lizard-competent strains with one having no immunomodulation (strain B379) but the other developing upregulated immune responses (strain 297). These results suggest that genetic variation in microparasites both induces different host strategies for dealing with infection and determines microparasite fitness in the hosts. These findings demonstrate that Bb and eastern fence lizards can serve as a model to investigate the mechanisms underlying eco-immunological strategies of tolerance vs. resistance during host-microparasite interaction. |
| format | Article |
| id | doaj-art-ac47d12017874e7ebfc4a334d99a96c8 |
| institution | OA Journals |
| issn | 1877-9603 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Ticks and Tick-Borne Diseases |
| spelling | doaj-art-ac47d12017874e7ebfc4a334d99a96c82025-08-20T01:55:27ZengElsevierTicks and Tick-Borne Diseases1877-96032024-11-0115610241010.1016/j.ttbdis.2024.102410Microbial genetic variation impacts host eco-immunological strategies and microparasite fitness in Lyme borreliae-reptile systemTristan A. Nowak0Carly Fernandes1Jill Malfetano2Erica Lasek-Nesselquist3Matthew Combs4Klemen Strle5Russell L. Burke6Yi-Pin Lin7Division of Infectious Diseases, Wadsworth Center, NYSDOH, Albany, NY, USA; Department of Biomedical Sciences, SUNY Albany, Albany, NY, USADivision of Infectious Diseases, Wadsworth Center, NYSDOH, Albany, NY, USA; Department of Infectious Disease and Global Health, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA, USADivision of Infectious Diseases, Wadsworth Center, NYSDOH, Albany, NY, USADepartment of Biomedical Sciences, SUNY Albany, Albany, NY, USA; Bioinformatics Core, Wadsworth Center, NYSDOH, Albany, NY, USANational Wildlife Research Center, United State Department of Agriculture, Fort Collins, CO, USADepartment of Molecular Biology and Microbiology, School of Medicine, Tufts University, Boston, MA, USADepartment of Biology, Hofstra University, Hempstead, NY, USA.Division of Infectious Diseases, Wadsworth Center, NYSDOH, Albany, NY, USA; Department of Biomedical Sciences, SUNY Albany, Albany, NY, USA; Department of Infectious Disease and Global Health, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA, USA; Correspondence: Department of Infectious Disease and Global health, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA USA, Telephone: +1 508-887-4535.Tolerance and resistance are two host eco-immunological strategies in response to microparasite invasion. In the strategy of “resistance”, host responses are induced to decrease microparasite replication while the “tolerance” strategy allows hosts coexistence with microparasites by minimizing responses to avoid immune-mediated damage. The causative agent of Lyme disease is a group of genotypically diverse bacterial species, Borrelia burgdorferi sensu lato (Bb), which is transmitted by Ixodes ticks and persists in different reservoir animals. In North America, eastern fence lizards (Sceloporus undulatus) can be fed on by Ixodes ticks but are incompetent to one genotype of Bb (i.e., ospC type A). However, field-collected lizards showed evidence of previous infection by Bb strains with undefined genotypes. Supporting this evidence, we introduced three genotypically different Bb strains individually to eastern fence lizards and found a Bb genotype-dependent manner of infectivity. We compared liver transcriptomics and observed elevated immune responses triggered by a lizard-incompetent Bb strain (strain B31). We showed two lizard-competent strains with one having no immunomodulation (strain B379) but the other developing upregulated immune responses (strain 297). These results suggest that genetic variation in microparasites both induces different host strategies for dealing with infection and determines microparasite fitness in the hosts. These findings demonstrate that Bb and eastern fence lizards can serve as a model to investigate the mechanisms underlying eco-immunological strategies of tolerance vs. resistance during host-microparasite interaction.http://www.sciencedirect.com/science/article/pii/S1877959X24001031Lyme diseaseBorreliaToleranceResistanceGenetic variation |
| spellingShingle | Tristan A. Nowak Carly Fernandes Jill Malfetano Erica Lasek-Nesselquist Matthew Combs Klemen Strle Russell L. Burke Yi-Pin Lin Microbial genetic variation impacts host eco-immunological strategies and microparasite fitness in Lyme borreliae-reptile system Ticks and Tick-Borne Diseases Lyme disease Borrelia Tolerance Resistance Genetic variation |
| title | Microbial genetic variation impacts host eco-immunological strategies and microparasite fitness in Lyme borreliae-reptile system |
| title_full | Microbial genetic variation impacts host eco-immunological strategies and microparasite fitness in Lyme borreliae-reptile system |
| title_fullStr | Microbial genetic variation impacts host eco-immunological strategies and microparasite fitness in Lyme borreliae-reptile system |
| title_full_unstemmed | Microbial genetic variation impacts host eco-immunological strategies and microparasite fitness in Lyme borreliae-reptile system |
| title_short | Microbial genetic variation impacts host eco-immunological strategies and microparasite fitness in Lyme borreliae-reptile system |
| title_sort | microbial genetic variation impacts host eco immunological strategies and microparasite fitness in lyme borreliae reptile system |
| topic | Lyme disease Borrelia Tolerance Resistance Genetic variation |
| url | http://www.sciencedirect.com/science/article/pii/S1877959X24001031 |
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