Edited by Nancy A. Moran, University of Texas, Austin, TX, and approved February 9, 2016 (received for review September 23, 2015)
Many organisms are specialists living within a narrow range of conditions. Pathogens are often adapted to efficiently exploit only a few hosts species, or sometimes, only some genotypes within a species. The genomes of such parasites are predicted to maintain genes critical for host utilization and to lose genes no longer necessary outside their constrained lifestyle. We demonstrate that the genomic content of a fungal pathogen specialized to attack and consume fungus cultivated by ants meets these predictions. Despite a reduced genome size and gene content in comparison with less specialized relatives, the genome of this agricultural pathogen retains genes necessary for production of toxins, a step critical to host attack, and for breaking down nutrients abundant in its host.
Many microorganisms with specialized lifestyles have reduced genomes. This is best understood in beneficial bacterial symbioses, where partner fidelity facilitates loss of genes necessary for living independently. Specialized microbial pathogens may also exhibit gene loss relative to generalists. Here, we demonstrate that Escovopsis weberi, a fungal parasite of the crops of fungus-growing ants, has a reduced genome in terms of both size and gene content relative to closely related but less specialized fungi. Although primary metabolism genes have been retained, the E. weberi genome is depleted in carbohydrate active enzymes, which is consistent with reliance on a host with these functions. E. weberi has also lost genes considered necessary for sexual reproduction. Contrasting these losses, the genome encodes unique secondary metabolite biosynthesis clusters, some of which include genes that exhibit up-regulated expression during host attack. Thus, the specialized nature of the interaction between Escovopsis and ant agriculture is reflected in the parasite’s genome.
Author contributions: T.J.B.d.M., J.E.S., C.P.K., C.T., K.C., L.A., I.S.D., N.L., S.S.L.B., S.M.B., G.S., C.R.C., and N.M.G. designed research; T.J.B.d.M., J.E.S., C.P.K., K.C., L.A., I.S.D., N.L., S.S.L.B., and S.M.B. performed research; T.J.B.d.M., J.E.S., C.P.K., K.C., L.A., I.S.D., N.L., B.A.B., and N.M.G. analyzed data; and T.J.B.d.M., J.E.S., C.P.K., S.S.L.B., B.A.B., G.S., C.R.C., and N.M.G. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The raw dataset has been deposited at DNA Data Bank of Japan/European Molecular Biology Laboratory/GenBank under accession PRJNA253870, and the whole-genome assembly has been deposited under accession LGSR00000000. The version described here is version LGSR01000000. RNA-seq reads have been deposited in the Sequence Read Archive under accession SRP049545.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1518501113/-/DCSupplemental.
