Adaptation to low parasite abundance affects immune investment and immunopathological responses of cavefish


Por: Peuss, Robert, Box, Andrew C., Chen, Shiyuan, Wang, Yongfu, Tsuchiya, Dai, Persons, Jenna L., Kenzior, Alexander, Maldonado, Ernesto, Krishnan, Jaya, Scharsack, Joern P., Slaughter, Brian D., Rohner, Nicolas

Publicada: 1 oct 2020 Ahead of Print: 1 ene 2020
Resumen:
Reduced parasitic infection rates in the developed world are suspected to underlie the rising prevalence of autoimmune disorders. However, the long-term evolutionary consequences of decreased parasite exposure on an immune system are not well understood. We used the Mexican tetra Astyanax mexicanus to understand how loss of parasite diversity influences the evolutionary trajectory of the vertebrate immune system, by comparing river with cave morphotypes. Here, we present field data affirming a strong reduction in parasite diversity in the cave ecosystem, and show that cavefish immune cells display a more sensitive pro-inflammatory response towards bacterial endotoxins. Surprisingly, other innate cellular immune responses, such as phagocytosis, are drastically decreased in cavefish. Using two independent single-cell approaches, we identified a shift in the overall immune cell composition in cavefish as the underlying cellular mechanism, indicating strong differences in the immune investment strategy. While surface fish invest evenly into the innate and adaptive immune systems, cavefish shifted immune investment to the adaptive immune system, and here, mainly towards specific T-cell populations that promote homeostasis. Additionally, inflammatory responses and immunopathological phenotypes in visceral adipose tissue are drastically reduced in cavefish. Our data indicate that long-term adaptation to low parasite diversity coincides with a more sensitive immune system in cavefish, which is accompanied by a reduction in the immune cells that play a role in mediating the pro-inflammatory response. © 2020, The Author(s), under exclusive licence to Springer Nature Limited.

Filiaciones:
Peuss, Robert:
 Stowers Institute for Medical Research, Kansas City, MO, United States

 Stowers Inst Med Res, Kansas City, MO 64110 USA

Box, Andrew C.:
 Stowers Institute for Medical Research, Kansas City, MO, United States

 Stowers Inst Med Res, Kansas City, MO 64110 USA

Chen, Shiyuan:
 Stowers Institute for Medical Research, Kansas City, MO, United States

 Stowers Inst Med Res, Kansas City, MO 64110 USA

Wang, Yongfu:
 Stowers Institute for Medical Research, Kansas City, MO, United States

 Stowers Inst Med Res, Kansas City, MO 64110 USA

Tsuchiya, Dai:
 Stowers Institute for Medical Research, Kansas City, MO, United States

 Stowers Inst Med Res, Kansas City, MO 64110 USA

Persons, Jenna L.:
 Stowers Institute for Medical Research, Kansas City, MO, United States

 Stowers Inst Med Res, Kansas City, MO 64110 USA

Kenzior, Alexander:
 Stowers Institute for Medical Research, Kansas City, MO, United States

 Stowers Inst Med Res, Kansas City, MO 64110 USA

Maldonado, Ernesto:
 EvoDevo Research Group, Unidad Académica de Sistemas Arrecifales, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Puerto Morelos, Mexico

 Univ Nacl Autonoma Mexico, Inst Ciencias Mar & Limnol, EvoDevo Res Grp, Unidad Acad Sistemas Arrecifales, Puerto Morelos, Mexico

Krishnan, Jaya:
 Stowers Institute for Medical Research, Kansas City, MO, United States

 Stowers Inst Med Res, Kansas City, MO 64110 USA

Scharsack, Joern P.:
 Institute for Evolution and Biodiversity, University of Münster, Münster, Germany

 Thünen Institute of Fisheries Ecology, Bremerhaven, Germany

 Univ Munster, Inst Evolut & Biodivers, Munster, Germany

 Thunen Inst Fisheries Ecol, Bremerhaven, Germany

Slaughter, Brian D.:
 Stowers Institute for Medical Research, Kansas City, MO, United States

 Stowers Inst Med Res, Kansas City, MO 64110 USA

Rohner, Nicolas:
 Stowers Institute for Medical Research, Kansas City, MO, United States

 Department of Molecular & Integrative Physiology, University of Kansas Medical Center, Kansas City, KS, United States

 Stowers Inst Med Res, Kansas City, MO 64110 USA

 Univ Kansas, Med Ctr, Dept Mol & Integrat Physiol, Kansas City, KS 66103 USA
ISSN: 2397334X
Editorial
Nature Publishing Group, MACMILLAN BUILDING, 4 CRINAN ST, LONDON N1 9XW, ENGLAND, Reino Unido
Tipo de documento: Article
Volumen: 4 Número: 10
Páginas: 1416-1416
WOS Id: 000550647300001
ID de PubMed: 32690906