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Basidiomycete yeasts in the cortex of ascomycete macrolichens - PubMed

  • ️Fri Jan 01 2016

. 2016 Jul 29;353(6298):488-92.

doi: 10.1126/science.aaf8287. Epub 2016 Jul 21.

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Basidiomycete yeasts in the cortex of ascomycete macrolichens

Toby Spribille et al. Science. 2016.

Abstract

For over 140 years, lichens have been regarded as a symbiosis between a single fungus, usually an ascomycete, and a photosynthesizing partner. Other fungi have long been known to occur as occasional parasites or endophytes, but the one lichen-one fungus paradigm has seldom been questioned. Here we show that many common lichens are composed of the known ascomycete, the photosynthesizing partner, and, unexpectedly, specific basidiomycete yeasts. These yeasts are embedded in the cortex, and their abundance correlates with previously unexplained variations in phenotype. Basidiomycete lineages maintain close associations with specific lichen species over large geographical distances and have been found on six continents. The structurally important lichen cortex, long treated as a zone of differentiated ascomycete cells, appears to consistently contain two unrelated fungi.

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Figures

Fig. 1
Fig. 1. Genome-wide divergence and transcript abundance of fungi and algae, based on symbiont subsets extracted from wild Bryoria metatranscriptomes.

(A and B) Unrooted maximum likelihood topologies for (A) the Ascomycota member (lecanoromycete) and (B) the Viridiplantae member (alga) within the lichen pair B. fremontii and B. tortuosa, based on 30,001 and 25,788 SNPs, respectively. Numbers refer to metatranscriptome sample IDs (table S2). Scale bars indicate the average number of substitutions per site. (C to E) Logarithm of the fold change (logFC) between vulpinic acid–deficient (B. fremontii) and vulpinic acid–rich (B. tortuosa) phenotypes in 15 Bryoria metatranscriptomes, plotted against transcript abundance (logCPM, logarithm of counts per million reads). Only transcripts found in all 15 samples were included. Ascomycota transcripts only are shown in (C). All fungal transcripts are shown in (D), with taxonomic assignments superimposed; a plot with statistically significant transcript differential abundance is shown as an inset. Viridiplantae transcripts are shown in (E). Red dots indicate a log fold change with P < 0.05 in (C), (E) (highlighted with arrows), and the inset of (D).

Fig. 2
Fig. 2. Placement of Cyphobasidiales members and their diversity within lichens.

(A) Maximum likelihood phylogenomic tree based on 39 fungal proteomes and 349 single-copy orthologous loci. Dating based on a 58-locus subsample shows relative splits between Cyphobasidiales and Cystobasidium minutum and splits leading to the lecanoromycete genera Xanthoria, Cladonia, and Bryoria (colored bars indicate 95% confidence intervals; fungi occurring in lichens are shown in green). (B) Maximum likelihood rDNA phylogeny of the class Cystobasidiomycetes, with images of representative lichen species from which sequences were obtained in each clade; thick branches indicate bootstrap support >70%. Shaded triangles are scaled to the earliest branch splits of underlying sequence divergence in each clade. Full versions of the trees are shown in fig. S3.

Fig. 3
Fig. 3. Differential abundance of Cyphobasidiales yeasts in B. fremontii and B. tortuosa.

(A) B. fremontii, with (B) few FISH-hybridized live yeast cells at the level of the cortex. (C) B. tortuosa, with (D) abundant FISH-hybridized cortical yeast cells (scale bars, 20 μm).

Fig. 4
Fig. 4. Fluorescent cell imaging of dual fungal elements in lichen thalli.

(A) Scanning electron microscopy image of a thallus filament of B. capillaris (scale bar, 200 μm). (B) FISH hybridization of B. capillaris thallus, showing Cyphobasidiales yeasts (green) and the lecanoromycete (blue) with algal chlorophyll A autofluorescence (red). The volume within the two vertical lines is visualized on the right; the unclipped frontal view is shown at the top. Movie S2 shows an animation of the three-dimensional ~100-μm z-stack. (C) Detail of yeast cells (scale bar, 5 μm).

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References

    1. De Bary A. Die Erscheinung der Symbiose. Verlag Karl Trübner; 1879.
    1. Gargas A, DePriest PT, Grube M, Tehler A. Multiple origins of lichen symbioses in fungi suggested by SSU rDNA phylogeny. Science. 1995;268:1492–1495. doi: 10.1126/science.7770775. - DOI - PubMed
    1. Lutzoni F, Pagel M, Reeb V. Major fungal lineages are derived from lichen symbiotic ancestors. Nature. 2001;411:937–940. doi: 10.1038/35082053. - DOI - PubMed
    1. Hawksworth DL. The variety of fungal-algal symbioses, their evolutionary significance, and the nature of lichens. Bot J Linn Soc. 1988;96:3–20. doi: 10.1111/j.1095-8339.1988.tb00623.x. - DOI
    1. Ahmadjian V. The Lichen Symbiosis. John Wiley & Sons; 1993.

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