Abstract
Fungal pathogens have evolved a broad suite of strategies aiming at evading the host immune response. Amphibians are globally infected by the panzootic chytrid fungus Batrachochytrium dendrobatidis (Bd) and, while robust innate immune defences have been characterised, there is little evidence for the existence of effective adaptive immunity. We determine the immune response of the common midwife toad following challenge by Bd as larvae. Immune function was described for both the cell-mediated and antibody-mediated immune responses following infectious challenge as larval amphibians. While there were no significant differences in the ratio of neutrophils/lymphocytes between infected and uninfected individuals, early exposure of tadpoles to Bd significantly dampened the levels of circulating immunoglobulins (IgM and IgY) in the serum of juveniles after metamorphosis. Our results show that Bd immunosuppresses amphibians when infection occurs as larvae with potentially broad effects on the remodelling of immunity during metamorphosis.
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References
Boyle DG, Boyle DB, Olsen V, Morgan JAT, Hyatt AD (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis Aquat Org 60(2):141–148. https://doi.org/10.3354/dao060141
Cashins SD, Grogan LF, McFadden M, Hunter D, Harlow PS, Berger L, Skerratt LS (2013) Prior infection does not improve survival against the amphibian disease chytridiomycosis. PLoS One 8(2):e56747. https://doi.org/10.1371/journal.pone.0056747
Du Pasquier L, Haimovich J (1976) The antibody response during amphibian ontogeny. Immunogenetics 3(1):381–391. https://doi.org/10.1007/BF01576969
Fernández-Beaskoetxea S, Carrascal LM, Fernández-Loras A, Fisher MC, Bosch J (2015) Short term minimum water temperatures determine levels of infection by the amphibian chytrid fungus in Alytes obstetricans tadpoles. PLoS One 10(3):e0120237. https://doi.org/10.1371/journal.pone.0120237
Fites JS, Ramsey JP, Holden WM, Collier SP, Sutherland DM, Reinert LK, Gayek AS, Dermody TS, Aune TM, Oswald-Richter K, Rollins-Smith LA (2013) The invasive chytrid fungus of amphibians paralyzes lymphocyte responses. Science 342(6156):366–369. https://doi.org/10.1126/science.1243316
Flajnik MF, Hsu E, Kaufman JF, DuPasquier L (1987) Changes in the immune system during metamorphosis of Xenopus. Immunol Today 8(2):58–64. https://doi.org/10.1016/0167-5699(87)90240-4
Forzán MJ, Gunn H, Scott P (2008) Chytridiomycosis in an aquarium collection of frogs: diagnosis, treatment and control. J Zoo Wildl Med 39(3):406–411. https://doi.org/10.1638/2007-0091.1
Gabor CR, Fisher MC, Bosch J (2013) A non-invasive stress assay shows that tadpole populations infected with Batrachochytrium dendrobatidis have elevated corticosterone levels. PLoS One 8(2):e56054. https://doi.org/10.1371/journal.pone.0056054
Geiger CC, Küpfer E, Schär S, Wolf S, Schmidt BR (2011) Elevated temperature clears chytrid fungus infections from tadpoles of the midwife toad, Alytes obstetricans. Amphibia-Reptilia 32(2):276–280. https://doi.org/10.1163/017353711X556970
Gervasi SS, Foufopoulos J (2008) Costs of plasticity: responses to desiccation decrease post-metamorphic immune function in a pond-breeding amphibian. Funct Ecol 22:100–108
Harris RN, Brucker RM, Walke JB, Becker MH, Schwantes CR, Flaherty DC, Lam BA, Woodhams DC, Briggs CJ, Vredenburg VT, Minbiole KPC (2009) Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J 3(7):818–824. https://doi.org/10.1038/ismej.2009.27
Kindermann C, Narayan EJ, Hero JM (2012) Urinary corticosterone metabolites and chytridiomycosis disease prevalence in a free-living population of male stony creek frogs (Litoria wilcoxii). Comp Biochem Physiol Part A 162(3):171–176. https://doi.org/10.1016/j.cbpa.2012.02.018
McMahon TA, Sears BF, Venesky MD, Bessler SM, Brown JM, Deutsch K, Halstead NT, Lentz G, Tenouri N, Young S, Civitello DJ, Ortega N, Fites JS, Reinert LK, Rollins-Smith LA, Raffel TR, Rohr JR (2014) Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature 511(7508):224–227. https://doi.org/10.1038/nature13491
Murphy PJ, St-Hilaire S, Corn PS (2011) Temperature, hydric environment, and prior pathogen exposure alter the experimental severity of chytridiomycosis in boreal toads. Dis Aquat Org 95(1):31–42. https://doi.org/10.3354/dao02336
Ribas L, Li M-S, Doddington BJ, Robert J, Seidel JA, Kroll JS, Zimmerman LB, Grassly NC, Garner TWJ, Fisher MC (2009) Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis. PLoS One 4(12):e8408. https://doi.org/10.1371/journal.pone.0008408
Robert J, Ohta Y (2009) Comparative and developmental study of the immune system in Xenopus. Dev Dynam 238(6):1249–1270. https://doi.org/10.1002/dvdy.21891
Rollins-Smith LA (1998) Metamorphosis and the amphibian immune system. Immunol Rev 166(1):221–230. https://doi.org/10.1111/j.1600-065X.1998.tb01265.x
Rollins-Smith LA (2001) Neuroendocrine-immune system interactions in amphibians: implications for understanding global amphibian declines. Immunol Res 23(2-3):273–280. https://doi.org/10.1385/IR:23:2-3:273
Rollins-Smith LA, Woodhams DC (2012) Amphibian immunity: staying in tune with the environment. In: Demas GE, Nelson RJ (eds) Ecoimmunology. Oxford University Press, Oxford, pp 92–143
Rollins-Smith LA, Ramsey JP, Reinert LK, Woodhams DC, Livo LJ, Carey C (2009) Immune defenses of Xenopus laevis against Batrachochytrium dendrobatidis. Front Biosci 1:68–91
Rosenblum EB, Poorten TJ, Settles M, Murdoch GK, Robert J, Maddox N, Eisen MB (2009) Genome-wide transcriptional response of Silurana (Xenopus) tropicalis to infection with the deadly chytrid fungus. PLoS One 4(8):e6494. https://doi.org/10.1371/journal.pone.0006494
Savage AE, Terrell KA, Gratwicke B, Mattheus NM, Augustine L, Fleischer RC (2016) Reduced immune function predicts disease susceptibility in frogs infected with a deadly fungal pathogen. Conserv Physiol 4(1):cow011. https://doi.org/10.1093/conphys/cow011
Shaw SD, Bishop PJ, Berger L, Skerratt LF, Garland S, Gleeson DM, Haigh A, Herbert S, Speare R (2010) Experimental infection of self-cured Leiopelma archeyi with the amphibian chytrid Batrachochytrium dendrobatidis. Dis Aquat Org 92(3):159–163. https://doi.org/10.3354/dao02227
Stice MJ, Briggs CJ (2010) Immunization is ineffective at preventing infection and mortality due to the amphibian chytrid fungus Batrachochytrium dendrobatidis. J Wildl Dis 46(1):70–77. https://doi.org/10.7589/0090-3558-46.1.70
Woodhams DC, Vredenburg VT, Simon MA, Billheimer D, Shakhtour B, Shyr Y, Briggs CJ, Rollins-Smith LA, Harris RN (2007) Symbiotic bacteria contribute to innate immune defenses of the threatened mountain yellow-legged frog, Rana muscosa. Biol Conserv 138(3–4):390–398. https://doi.org/10.1016/j.biocon.2007.05.004
Acknowledgements
Belén Patiño (University Complutense of Madrid) helped with fungus culture. Robert Jacques (University of Rochester Medical Center, NY) provided monoclonal antibodies. Yolanda Jiménez (MNCN-CSIC) helped with the indirect enzyme-linked immunosorbent assay. Ma. Carmen Aceña Fabián (Veterinary Faculty of Zaragoza) helped with blood smears staining and white blood cell identification.
Funding
AFL was funded by Fundación General CSIC and Banco Santander. MCF was funded by the Leverhulme Trust RPG 2014 273.
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All animal experiments were conducted in compliance of the Directive 2010/63/EU for the protection of animals used for scientific purposes in facilities of the regional government and under permit of the competent authorities (permits 10/032921.9/12 and 10/071126.9/13, Consejería de Medio Ambiente of Madrid).
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Fernández-Loras, A., Fernández-Beaskoetxea, S., Arriero, E. et al. Early exposure to Batrachochytrium dendrobatidis causes profound immunosuppression in amphibians. Eur J Wildl Res 63, 99 (2017). https://doi.org/10.1007/s10344-017-1161-y
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DOI: https://doi.org/10.1007/s10344-017-1161-y