Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data
- Erica Bree Rosenbluma,1,
- Timothy Y. Jamesb,
- Kelly R. Zamudioc,
- Thomas J. Poortena,
- Dan Ilutc,
- David Rodriguezc,
- Jonathan M. Eastmand,
- Katy Richards-Hrdlickae,
- Suzanne Jonesond,
- Thomas S. Jenkinsonb,
- Joyce E. Longcoref,
- Gabriela Parra Oleag,
- Luís Felipe Toledoh,
- Maria Luz Arellanoi,
- Edgar M. Medinaj,
- Silvia Restrepoj,
- Sandra Victoria Flechasj,
- Lee Bergerk,
- Cheryl J. Briggsl, and
- Jason E. Stajichm
- aDepartment of Environmental Science Policy and Management, University of California, Berkeley, CA 94720;
- bDepartment of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109;
- cDepartment of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853;
- dInstitute of Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, ID 83844;
- eSchool of Forestry and Environmental Studies, Yale University, New Haven, CT 06511;
- fSchool of Biology and Ecology, University of Maine, Orono, ME 04469;
- gInstituto de Biologia, Universidad Nacional Autonoma de Mexico, Mexico City, AP 70153, Mexico;
- hInstituto de Biologia, Universidade Estadual de Campinas, 13083-970, São Paulo, Brazil;
- iInstituto de Botánica Spegazzini, Universidad Nacional de La Plata, La Plata, 1900 Buenos Aires, Argentina;
- jDepartamento de Ciencias Biológicas, Universidad de los Andes, Bogotá, AA 4976, Colombia;
- kSchool of Public Health, Tropical Medicine and Rehabilitation Sciences, James Cook University, Townsville, QLD 4811, Australia;
- lDepartment of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106; and
- mDepartment of Plant Pathology and Microbiology, University of California, Riverside, CA 92521
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Edited by David M. Hillis, University of Texas at Austin, Austin, TX, and approved March 15, 2013 (received for review January 4, 2013)
Abstract
Understanding the evolutionary history of microbial pathogens is critical for mitigating the impacts of emerging infectious diseases on economically and ecologically important host species. We used a genome resequencing approach to resolve the evolutionary history of an important microbial pathogen, the chytrid Batrachochytrium dendrobatidis (Bd), which has been implicated in amphibian declines worldwide. We sequenced the genomes of 29 isolates of Bd from around the world, with an emphasis on North, Central, and South America because of the devastating effect that Bd has had on amphibian populations in the New World. We found a substantial amount of evolutionary complexity in Bd with deep phylogenetic diversity that predates observed global amphibian declines. By investigating the entire genome, we found that even the most recently evolved Bd clade (termed the global panzootic lineage) contained more genetic variation than previously reported. We also found dramatic differences among isolates and among genomic regions in chromosomal copy number and patterns of heterozygosity, suggesting complex and heterogeneous genome dynamics. Finally, we report evidence for selection acting on the Bd genome, supporting the hypothesis that protease genes are important in evolutionary transitions in this group. Bd is considered an emerging pathogen because of its recent effects on amphibians, but our data indicate that it has a complex evolutionary history that predates recent disease outbreaks. Therefore, it is important to consider the contemporary effects of Bd in a broader evolutionary context and identify specific mechanisms that may have led to shifts in virulence in this system.
Footnotes
- ↵1To whom correspondence should be addressed. E-mail: rosenblum{at}berkeley.edu.
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Author contributions: E.B.R., T.Y.J., K.R.Z., and J.E.S. designed research; E.B.R., T.J.P., D.R., K.R.-H., S.J., and T.S.J. performed research; J.E.L., G.P.O., L.F.T., M.L.A., E.M.M., S.R., S.V.F., L.B., and C.J.B. contributed new reagents/analytic tools; E.B.R., T.Y.J., T.J.P., D.I., D.R., J.M.E., and J.E.S. analyzed data; and E.B.R., T.Y.J., K.R.Z., T.J.P., J.M.E., and J.E.S. wrote the paper.
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The authors declare no conflict of interest.
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This article is a PNAS Direct Submission.
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Data deposition: The genomic data reported in this paper have been deposited in the NCBI Sequence Read Archive (accession no. SRA062886).
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See Commentary on page 9193.
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This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1300130110/-/DCSupplemental.
Freely available online through the PNAS open access option.
