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Genome-Wide Transcriptional Response of Silurana (Xenopus) tropicalis to Infection with the Deadly Chytrid Fungus

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.

ORGANISM(S): Xenopus tropicalis

PROVIDER: GSE16852 | GEO | 2009/08/31

SECONDARY ACCESSION(S): PRJNA117625

REPOSITORIES: GEO

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Project description:Along with the prevalence of edible frog farming in China, the outbreak of a deadly infectious frog diseased, called frog meningitis (or cataracts and torticollis), has increased in frequency and geographical range dramatically. More than 10 bacterial species, belonging to 8 genera, has been reported as its potential pathogens. Diseased frogs typically manifest as torticollis, cataracts, edema and finally death, resulting in huge economic loss. Currently, the pathogenesis of this disease has not been investigated systematically. Here, we summarized the pathological stages of infected black-spotted frogs (Pelophylax nigromaculata) in Sichuan province according to their symptoms, typically progressing of pathological stage with only torticollis to stage with both torticollis and cataracts. On the basis, we analyzed the pathogenesis by a combination of comparative environmental analysis, microbiomics and transcriptomics. Results showed that more severely infected frog ponds tended to have lower water alkalinity. Elizabethkingia miricola was the only bacteria, whose abundance was positively correlated with the disease degree, and it has absolute dominance in the eyeball and brain of some torticollis-cataracts frogs. E. miricola and several other bacterial species, which belonged to pathogenic genera of meningitis, might be constitutively existed in the resident microbiome in frogs or their environment. Activations of infectious processes and immune responses related pathways were the major difference between health and diseased frogs at transcriptional level. Despite transcriptional activation of immunoglobulins was observed in both torticollis-only and torticollis-cataracts frogs, transcriptional activation of innate immune system (including MHC, toll-like receptor, and cathelicidins) in brain, inflammation system (including interleukins and receptors) in brain, and acute phase proteins (including transferrins and fibrinogens) in both liver and brain was only observed in torticollis-cataracts frogs. Activation of inflammation and the resulting higher vascular permeability in torticollis-cataracts frogs could explain the severe brain infection, cooccurrence of torticollis and cataracts, and systemic edema in torticollis-cataracts frogs. In addition, meningitis could also result in reduction in energy production in liver, and this was more severe in torticollis-cataracts frogs. In conclusion, our results suggested environment might have a role in susceptibility of frog meningitis. E. miricola was the most likely pathogen of meningitis of black-spotted frogs in Sichuan. Refer to the pathogenesis of human meningitis, excessive inflammation likely played a critical role in the progress of frog meningitis, and its resulted sepsis and organ failure might be the direct cause of infected frogs.

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Genome-Wide Transcriptional Response of Silurana (Xenopus) tropicalis to Infection with the Deadly Chytrid Fungus

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