pubmed.ncbi.nlm.nih.gov

Small genome of the fungus Escovopsis weberi, a specialized disease agent of ant agriculture - PubMed

  • ️Fri Jan 01 2016

Small genome of the fungus Escovopsis weberi, a specialized disease agent of ant agriculture

Tom J B de Man et al. Proc Natl Acad Sci U S A. 2016.

Abstract

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.

Keywords: Atta cephalotes; attine; genome reduction; mycoparasitism; repeat-induced point mutation.

PubMed Disclaimer

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.

Escovopsis weberi, a specialized mycoparasite of the fungus-growing ant symbiosis, has a small genome compared with other Pezizomycotina fungi. (A) Both fungus-growing ants and the mycoparasite E. weberi use the ants’ cultivated fungi as their primary food source. The ability of the cultivated fungi to efficiently break down plant material gives both consumers access to the biomass of neotropical plants. (B) Size and protein-coding gene content of genomes of diverse fungi in the Pezizomycotina. Bayesian phylogeny estimated using partial amino acid alignments of three genes (Rpb1, Rpb2, ef1-α). All posterior probabilities are greater than 0.95. Phylogeny is rooted with Sacchormyces cervesiae (not shown). (C) Relationship between genome size and gene content. A list of genomes included in this panel is in SI Appendix, Table S1.

Fig. 2.
Fig. 2.

Similarities between Escovopsis and Trichoderma. (A) Mesosynteny between E. weberi and T. virens. Scaffolds of E. weberi are multicolored. T. virens scaffolds are black. Only scaffolds containing syntenic regions are shown. (B) Gene content overlap between E. weberi and three Trichoderma species. Like Escovopsis spp., Trichoderma spp. are mycoparasites (fungi that attack and consume other fungi), although they are less specialized and are also able to obtain nutrients from dead organic matter. Orthologs were assigned using all-against-all BLASTP for amino acids and inparanoid/multiparanoid (sequence overlap coverage ≥50%).

Fig. 3.
Fig. 3.

The E. weberi genome encodes a reduced number of carbohydrate active enzymes. Carbohydrate active enzymes are divided into families. Each point represents the relation between the number of members of a given CAZmye family for E. weberi plotted against the average number of family members for the less specialized mycoparasites T. virens and T. atroviride. Members of some of these families, indicated in orange, are known to be highly expressed in E. weberi’s host fungus (2, 3). Additional details are in SI Appendix, Table S10.

Fig. 4.
Fig. 4.

Up-regulation of gene expression within a secondary metabolite cluster during interaction with cultivated host fungi. Gbrowse genome browser view of 1 of 16 secondary metabolite clusters in the E. weberi genome. Below the scaffold are three tracks illustrating RNAseq-based gene expression when E. weberi is growing toward its host (Top), when it has overgrown its host (Middle), and in the absence of its host (Bottom); MAKER2 gene model predictions are illustrated below. Photographs next to each RNAseq track illustrate the growth of E. weberi under each condition. Each Petri dish was inoculated with the cultivated fungus near the top (when present) and E. weberi near the center 1 wk later; photographs were taken 3–4 d after E. weberi inoculation. Note that E. weberi grows much more rapidly in the presence than in the absence of its host. See SI Appendix, Fig. S1 for additional images.

Similar articles

Cited by

References

    1. Weber NA. Fungus-growing ants. Science. 1966;153(3736):587–604. - PubMed
    1. Grell MN, et al. The fungal symbiont of Acromyrmex leaf-cutting ants expresses the full spectrum of genes to degrade cellulose and other plant cell wall polysaccharides. BMC Genomics. 2013;14:928. - PMC - PubMed
    1. Aylward FO, et al. Leucoagaricus gongylophorus produces diverse enzymes for the degradation of recalcitrant plant polymers in leaf-cutter ant fungus gardens. Appl Environ Microbiol. 2013;79(12):3770–3778. - PMC - PubMed
    1. Schiøtt M, De Fine Licht HH, Lange L, Boomsma JJ. Towards a molecular understanding of symbiont function: Identification of a fungal gene for the degradation of xylan in the fungus gardens of leaf-cutting ants. BMC Microbiol. 2008;8(1):40. - PMC - PubMed
    1. Moller IE, De Fine Licht HH, Harholt J, Willats WGT, Boomsma JJ. The dynamics of plant cell-wall polysaccharide decomposition in leaf-cutting ant fungus gardens. PLoS One. 2011;6(3):e17506–e17509. - PMC - PubMed

Publication types

MeSH terms