Abstract

Emerging infectious diseases are of great concern for both wildlife and humans. Several highly virulent fungal pathogens have recently been discovered in natural populations, highlighting the need for a better understanding of fungal-vertebrate host-pathogen interactions. Because most fungal pathogens are not fatal in the absence of other predisposing conditions, host-pathogen dynamics for deadly fungal pathogens are of particular interest. The chytrid fungus Batrachochytrium dendrobatidis (hereafter Bd) infects hundreds of species of frogs in the wild. It is found worldwide and is a significant contributor to the current global amphibian decline. However, the mechanism by which Bd causes death in amphibians, and the response of the host to Bd infection, remain largely unknown. Here we use whole-genome microarrays to monitor the transcriptional responses to Bd infection in the model frog species, Silurana (Xenopus) tropicalis, which is susceptible to chytridiomycosis. To elucidate the immune response to Bd and evaluate the physiological effects of chytridiomycosis, we measured gene expression changes in several tissues (liver, skin, spleen) following exposure to Bd. We detected a strong transcriptional response for genes involved in physiological processes that can help explain some clinical symptoms of chytridiomycosis at the organismal level. However, we detected surprisingly little evidence of an immune response to Bd exposure, suggesting that this susceptible species may not be mounting efficient innate and adaptive immune responses against Bd. The weak immune response may be partially explained by the thermal conditions of the experiment, which were optimal for Bd growth. However, many immune genes exhibited decreased expression in Bd-exposed frogs compared to control frogs, suggesting a more complex effect of Bd on the immune system than simple temperature-mediated immune suppression. This study generates important baseline data for ongoing efforts to understand differences in response to Bd between susceptible and resistant frog species and the effects of chytridiomycosis in natural populations.

Highlights

  • Emerging infectious diseases are receiving increasing attention for their role in precipitous population declines and extinctions in natural populations (e.g., [1])

  • One of the most dramatic examples of the impact of pathogenic fungi on vertebrate populations is the chytrid Batrachochytrium dendrobatidis, which has been implicated in global amphibian declines

  • We present data on the genetic pathways perturbed in response to Bd and discuss the implications for understanding disease-related amphibian declines

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Summary

Introduction

Emerging infectious diseases are receiving increasing attention for their role in precipitous population declines and extinctions in natural populations (e.g., [1]). The recent discovery of deadly fungal skin infections in natural vertebrate populations (e.g., [3]) raises a number of questions about how a pathogen localized to the skin can lead so quickly to death and threaten entire populations. One of the most dramatic examples of the impact of pathogenic fungi on vertebrate populations is the chytrid Batrachochytrium dendrobatidis (hereafter Bd), which has been implicated in global amphibian declines. This pathogen, discovered and described only 10 years ago [4], infects hundreds of amphibian species worldwide [5]. Chytridiomycosis, the disease caused by Bd is often fatal, and is the clear cause of catastrophic reductions in many frog populations around the world (e.g., [7,8])

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