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Fighting a losing battle: vigorous immune response countered by pathogen suppression of host defenses in the chytridiomycosis-susceptible frog Atelopus zeteki.

ABSTRACT: The emergence of the disease chytridiomycosis caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd) has been implicated in dramatic global amphibian declines. Although many species have undergone catastrophic declines and/or extinctions, others appear to be unaffected or persist at reduced frequencies after Bd outbreaks. The reasons behind this variance in disease outcomes are poorly understood: differences in host immune responses have been proposed, yet previous studies suggest a lack of robust immune responses to Bd in susceptible species. Here, we sequenced transcriptomes from clutch-mates of a highly susceptible amphibian, Atelopus zeteki, with different infection histories. We found significant changes in expression of numerous genes involved in innate and inflammatory responses in infected frogs despite high susceptibility to chytridiomycosis. We show evidence of acquired immune responses generated against Bd, including increased expression of immunoglobulins and major histocompatibility complex genes. In addition, fungal-killing genes had significantly greater expression in frogs previously exposed to Bd compared with Bd-naïve frogs, including chitinase and serine-type proteases. However, our results appear to confirm recent in vitro evidence of immune suppression by Bd, demonstrated by decreased expression of lymphocyte genes in the spleen of infected compared with control frogs. We propose susceptibility to chytridiomycosis is not due to lack of Bd-specific immune responses but instead is caused by failure of those responses to be effective. Ineffective immune pathway activation and timing of antibody production are discussed as potential mechanisms. However, in light of our findings, suppression of key immune responses by Bd is likely an important factor in the lethality of this fungus.

SUBMITTER: Ellison AR

PROVIDER: S-EPMC4455776 | biostudies-literature | 2014 May

REPOSITORIES: biostudies-literature

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Fighting a losing battle: vigorous immune response countered by pathogen suppression of host defenses in the chytridiomycosis-susceptible frog Atelopus zeteki.

Ellison Amy R AR Savage Anna E AE DiRenzo Grace V GV Langhammer Penny P Lips Karen R KR Zamudio Kelly R KR

G3 (Bethesda, Md.) 20140519 7

The emergence of the disease chytridiomycosis caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd) has been implicated in dramatic global amphibian declines. Although many species have undergone catastrophic declines and/or extinctions, others appear to be unaffected or persist at reduced frequencies after Bd outbreaks. The reasons behind this variance in disease outcomes are poorly understood: differences in host immune responses have been proposed, yet previous studies suggest a la ...[more]

PMID: 24841130

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Project description:In the past century, recently emerged infectious diseases have become major drivers of species decline and extinction. Amphibian declines have occurred due to the fungal disease chytridiomycosis, which has exacerbated the conservation crisis of this taxonomic group. Biologists are beginning to understand what traits are important for susceptibility to this disease, but more work is needed to determine why some species succumb to disease while others do not. We conducted a laboratory experiment to examine how two toad species respond to infection in controlled environment. We selected two related species thought to differ in susceptibility â?? Bufo marinus (an invasive and putatively resistant species) and B. boreas (an endangered and putatively susceptible species). We measured infection intensity, body weight, histological changes at the site of infection, and genome-wide gene expression changes using a custom assay developed from transcriptome sequencing. Our results confirmed that the two species differ in susceptibility. The more susceptible species, B. boreas, experienced higher infection intensities, loss in body weight, more dramatic histological changes, and larger perturbations in gene expression. We found key differences in skin expression responses in multiple pathways including up-regulation of skin integrity-related genes in the resistant B. marinus. Together our results show intrinsic differences in host response between related species, which are likely to be an important factor in explaining variation in response to a deadly emerging pathogen in wild populations. We processed 72 tissue samples in total: six biological replicates, three tissue types (ventral skin, liver, spleen), two treatment groups (pathogen exposed, control), and two host species (Bufo marinus, Bufo boreas). The custom Nimblegen microarray design included 135,200 60-bp probes (excluding control probes) targeting 31,367 transcript contigs from Bufo marinus, Bufo boreas, and model species Xenopus tropicalis, with 4 probes per probe-set. We used the 12-plex microarray platform (12 arrays per glass slide). Differential expression analyses were performed separately for each tissue type and host species.

Dataset Information

Fighting a losing battle: vigorous immune response countered by pathogen suppression of host defenses in the chytridiomycosis-susceptible frog Atelopus zeteki.

Publications

Fighting a losing battle: vigorous immune response countered by pathogen suppression of host defenses in the chytridiomycosis-susceptible frog Atelopus zeteki.

Similar Datasets

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