Winter is coming-Temperature affects immune defenses and susceptibility to Batrachochytrium salamandrivorans

PLoS Pathog. 2021 Feb 18;17(2):e1009234. doi: 10.1371/journal.ppat.1009234. eCollection 2021 Feb.

Abstract

Environmental temperature is a key factor driving various biological processes, including immune defenses and host-pathogen interactions. Here, we evaluated the effects of environmental temperature on the pathogenicity of the emerging fungal pathogen, Batrachochytrium salamandrivorans (Bsal), using controlled laboratory experiments, and measured components of host immune defense to identify regulating mechanisms. We found that adult and juvenile Notophthalmus viridescens died faster due to Bsal chytridiomycosis at 14°C than at 6 and 22°C. Pathogen replication rates, total available proteins on the skin, and microbiome composition likely drove these relationships. Temperature-dependent skin microbiome composition in our laboratory experiments matched seasonal trends in wild N. viridescens, adding validity to these results. We also found that hydrophobic peptide production after two months post-exposure to Bsal was reduced in infected animals compared to controls, perhaps due to peptide release earlier in infection or impaired granular gland function in diseased animals. Using our temperature-dependent susceptibility results, we performed a geographic analysis that revealed N. viridescens populations in the northeastern United States and southeastern Canada are at greatest risk for Bsal invasion, which shifted risk north compared to previous assessments. Our results indicate that environmental temperature will play a key role in the epidemiology of Bsal and provide evidence that temperature manipulations may be a viable disease management strategy.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Batrachochytrium / pathogenicity*
  • Mycoses / epidemiology
  • Mycoses / immunology*
  • Mycoses / microbiology
  • Notophthalmus viridescens / immunology*
  • Notophthalmus viridescens / microbiology
  • Seasons*
  • Skin / immunology*
  • Skin / microbiology
  • Temperature

Grant support

MJG, DLM, DCW, and LAR-S received funds from the National Science Foundation Division of Environmental Biology (Ecology and Evolution of Infectious Diseases Program, https://www.nsf.gov/funding/pgm_summ.jsp?pims_id=5269) Grant #1814520. DCW and LAR-S were partially supported by the U.S. Department of Defense Strategic Environmental Research and Development Program (https://www.serdp-estcp.org/) Grant #W912HQ-16-C-0033). MJG and DLM were supported by U.S. Department of Agriculture National Institute of Food and Agriculture (https://nifa.usda.gov/program/hatch-act-1887-multistate-research-fund), Hatch Project #1012932. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.