Fighting a losing battle: vigorous immune response countered by pathogen suppression of host defenses in the chytridiomycosis-susceptible frog Atelopus zeteki.
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.
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853 are35@cornell.edu.
Amy R
AR
Ellison
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853 Center for Conservation and Evolutionary Genetics, Smithsonian Institution, Washington, DC 20013.
Anna E
AE
Savage
Department of Biology, University of Maryland, College Park, Maryland 20742.
Grace V
GV
DiRenzo
School of Life Sciences, Arizona State University, Tempe, Arizona 85287.
Penny
P
Langhammer
Department of Biology, University of Maryland, College Park, Maryland 20742.
Karen R
KR
Lips
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853.
Kelly R
KR
Zamudio
D056704:Adaptive Immunity; D000818:Animals; D002025:Bufonidae / Q000235:genetics* / Q000276:immunology; D002688:Chitinases / Q000235:genetics / Q000378:metabolism; D008411:Chytridiomycota / Q000472:pathogenicity*; D004198:Disease Susceptibility / Q000276:immunology; D007113:Immunity, Innate; D009181:Mycoses / Q000276:immunology / Q000382:microbiology; D017423:Sequence Analysis, RNA; D057057:Serine Proteases / Q000235:genetics / Q000378:metabolism; D059467:Transcriptome
D002688:Chitinases; D057057:Serine Proteases
Atelopus zeteki; Batrachochytrium dendrobatidis; acquired immunity; complex genetics; complex immunity; genetics of immunity; immunogenomics; immunosuppression; infection; innate immunity; resistance; tolerance