Varying conjunctival immune response adaptations of house finch populations to a rapidly evolving bacterial pathogen
Pathogen adaptations during host-pathogen co-evolution can cause the host balance between immunity and immunopathology to rapidly shift. However, little is known in natural disease systems about the immunological pathways optimised through the trade-off between immunity and self-damage. The evolutio...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2024-02-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1250818/full |
| _version_ | 1797334763835490304 |
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| author | Nithya Kuttiyarthu Veetil Amberleigh E. Henschen Dana M. Hawley Balraj Melepat Rami A. Dalloul Vladimír Beneš James S. Adelman Michal Vinkler |
| author_facet | Nithya Kuttiyarthu Veetil Amberleigh E. Henschen Dana M. Hawley Balraj Melepat Rami A. Dalloul Vladimír Beneš James S. Adelman Michal Vinkler |
| author_sort | Nithya Kuttiyarthu Veetil |
| collection | DOAJ |
| description | Pathogen adaptations during host-pathogen co-evolution can cause the host balance between immunity and immunopathology to rapidly shift. However, little is known in natural disease systems about the immunological pathways optimised through the trade-off between immunity and self-damage. The evolutionary interaction between the conjunctival bacterial infection Mycoplasma gallisepticum (MG) and its avian host, the house finch (Haemorhous mexicanus), can provide insights into such adaptations in immune regulation. Here we use experimental infections to reveal immune variation in conjunctival tissue for house finches captured from four distinct populations differing in the length of their co-evolutionary histories with MG and their disease tolerance (defined as disease severity per pathogen load) in controlled infection studies. To differentiate contributions of host versus pathogen evolution, we compared house finch responses to one of two MG isolates: the original VA1994 isolate and a more evolutionarily derived one, VA2013. To identify differential gene expression involved in initiation of the immune response to MG, we performed 3’-end transcriptomic sequencing (QuantSeq) of samples from the infection site, conjunctiva, collected 3-days post-infection. In response to MG, we observed an increase in general pro-inflammatory signalling, as well as T-cell activation and IL17 pathway differentiation, associated with a decrease in the IL12/IL23 pathway signalling. The immune response was stronger in response to the evolutionarily derived MG isolate compared to the original one, consistent with known increases in MG virulence over time. The host populations differed namely in pre-activation immune gene expression, suggesting population-specific adaptations. Compared to other populations, finches from Virginia, which have the longest co-evolutionary history with MG, showed significantly higher expression of anti-inflammatory genes and Th1 mediators. This may explain the evolution of disease tolerance to MG infection in VA birds. We also show a potential modulating role of BCL10, a positive B- and T-cell regulator activating the NFKB signalling. Our results illuminate potential mechanisms of house finch adaptation to MG-induced immunopathology, contributing to understanding of the host evolutionary responses to pathogen-driven shifts in immunity-immunopathology trade-offs. |
| first_indexed | 2024-03-08T08:25:54Z |
| format | Article |
| id | doaj.art-e0673b0fa2124b74b13c73cfad5b352f |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-03-08T08:25:54Z |
| publishDate | 2024-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-e0673b0fa2124b74b13c73cfad5b352f2024-02-02T04:40:09ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-02-011510.3389/fimmu.2024.12508181250818Varying conjunctival immune response adaptations of house finch populations to a rapidly evolving bacterial pathogenNithya Kuttiyarthu Veetil0Amberleigh E. Henschen1Dana M. Hawley2Balraj Melepat3Rami A. Dalloul4Vladimír Beneš5James S. Adelman6Michal Vinkler7Department of Zoology, Charles University, Faculty of Science, Prague, CzechiaDepartment of Biological Sciences, The University of Memphis, Memphis, TN, United StatesDepartment of Biological Sciences, Virginia Tech, Blacksburg, VA, United StatesDepartment of Zoology, Charles University, Faculty of Science, Prague, CzechiaDepartment of Poultry Science, The University of Georgia, Athens, GA, United StatesEuropean Molecular Biology Laboratory (EMBL), Genomics Core Facility, Heidelberg, GermanyDepartment of Biological Sciences, The University of Memphis, Memphis, TN, United StatesDepartment of Zoology, Charles University, Faculty of Science, Prague, CzechiaPathogen adaptations during host-pathogen co-evolution can cause the host balance between immunity and immunopathology to rapidly shift. However, little is known in natural disease systems about the immunological pathways optimised through the trade-off between immunity and self-damage. The evolutionary interaction between the conjunctival bacterial infection Mycoplasma gallisepticum (MG) and its avian host, the house finch (Haemorhous mexicanus), can provide insights into such adaptations in immune regulation. Here we use experimental infections to reveal immune variation in conjunctival tissue for house finches captured from four distinct populations differing in the length of their co-evolutionary histories with MG and their disease tolerance (defined as disease severity per pathogen load) in controlled infection studies. To differentiate contributions of host versus pathogen evolution, we compared house finch responses to one of two MG isolates: the original VA1994 isolate and a more evolutionarily derived one, VA2013. To identify differential gene expression involved in initiation of the immune response to MG, we performed 3’-end transcriptomic sequencing (QuantSeq) of samples from the infection site, conjunctiva, collected 3-days post-infection. In response to MG, we observed an increase in general pro-inflammatory signalling, as well as T-cell activation and IL17 pathway differentiation, associated with a decrease in the IL12/IL23 pathway signalling. The immune response was stronger in response to the evolutionarily derived MG isolate compared to the original one, consistent with known increases in MG virulence over time. The host populations differed namely in pre-activation immune gene expression, suggesting population-specific adaptations. Compared to other populations, finches from Virginia, which have the longest co-evolutionary history with MG, showed significantly higher expression of anti-inflammatory genes and Th1 mediators. This may explain the evolution of disease tolerance to MG infection in VA birds. We also show a potential modulating role of BCL10, a positive B- and T-cell regulator activating the NFKB signalling. Our results illuminate potential mechanisms of house finch adaptation to MG-induced immunopathology, contributing to understanding of the host evolutionary responses to pathogen-driven shifts in immunity-immunopathology trade-offs.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1250818/fulladaptations diversifying populationsemerging diseasecoevolutionparasitehost-pathogen interactioninflammatory immune response |
| spellingShingle | Nithya Kuttiyarthu Veetil Amberleigh E. Henschen Dana M. Hawley Balraj Melepat Rami A. Dalloul Vladimír Beneš James S. Adelman Michal Vinkler Varying conjunctival immune response adaptations of house finch populations to a rapidly evolving bacterial pathogen Frontiers in Immunology adaptations diversifying populations emerging disease coevolution parasite host-pathogen interaction inflammatory immune response |
| title | Varying conjunctival immune response adaptations of house finch populations to a rapidly evolving bacterial pathogen |
| title_full | Varying conjunctival immune response adaptations of house finch populations to a rapidly evolving bacterial pathogen |
| title_fullStr | Varying conjunctival immune response adaptations of house finch populations to a rapidly evolving bacterial pathogen |
| title_full_unstemmed | Varying conjunctival immune response adaptations of house finch populations to a rapidly evolving bacterial pathogen |
| title_short | Varying conjunctival immune response adaptations of house finch populations to a rapidly evolving bacterial pathogen |
| title_sort | varying conjunctival immune response adaptations of house finch populations to a rapidly evolving bacterial pathogen |
| topic | adaptations diversifying populations emerging disease coevolution parasite host-pathogen interaction inflammatory immune response |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1250818/full |
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