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Metagenomic data reveal diverse fungal and algal communities associated with the lichen symbiosis

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Abstract

Lichens have traditionally been considered the symbiotic phenotype from the interactions of a single fungal partner and one or few photosynthetic partners. However, lichen symbioses have been shown to be far more complex and may include a wider range of other interacting organisms, including non-photosynthetic bacteria, accessory fungi, and algae. In this study, we analyzed metagenomic shotgun sequences in an attempt to characterize lichen mycobiomes. Specifically, we inferred the range of fungi associated within lichen thalli from five groups of lichens – horsehair lichens (mycobiont = Bryoria spp.), shadow lichens (taxa in Physciaceae), rock posies (Rhizoplaca spp.), rock tripes (Umbilicaria spp.), and green rock shields (Xanthoparmelia spp.). Metagenomic reads from the multi-copy nuclear ribosomal internal transcribed spacer region, the standard DNA barcode region for fungi, were extracted, clustered, and used to infer taxonomic assignments. Our data revealed diverse lichen-associated mycobiomes. Many of the members of the lichen-associated mycobiomes that were identified here have not previously been found in association with lichens. Furthermore, closely related mycobionts tended to have more similar mycobiomes. We found little evidence supporting the ubiquitous presence of Cystobasidiales yeasts in macrolichens, although reads representing this putative symbiotic partner were found in samples of Bryoria lichens, albeit in low abundance. Our study further highlights the ecosystem-like features of lichens, with partners and interactions far from being completely understood. Future research is needed to more fully and accurately characterize lichen mycobiomes and how these fungi interact with the major lichen components, the photo- and mycobionts.

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Acknowledgements

We dedicate this publication to our friend and colleague, Dr. Eva Barreno. We gratefully acknowledge the fruitful discussions with Toby Spribille, Diane Haughland, Curtis Björk, and Trevor Goward. We gratefully acknowledge valuable feedback from anonymous reviewers and the editor that greatly improved this study. This research was supported by College of Life Sciences at Brigham Young University, Provo, Utah, USA. We thank Ed Wilcox, DNA Sequencing Center, Brigham Young University, Provo, Utah, USA, for help with sequencing. We also express appreciation to Gretchen Baker for organizing a lichen BioBlitz in Great Basin National Park, Nevada, USA that resulted in a number of collections used in this study (NPS Scientific Collecting and Research Permit number GRBA-2017-SCI-0012).

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Authors and Affiliations

  1. Department of Biology and M. L. Bean Life Science Museum, Brigham Young University, Provo, UT, USA

    Hayden B. Smith, Rachel Keuler & Steven D. Leavitt

  2. Senckenberg Biodiversity and Climate Research Centre (SBiK-F), Senckenberganlage 25, D-60325, Frankfurt, Germany

    Francesco Dal Grande & Imke Schmitt

  3. LOEWE Centre for Translational Biodiversity Genomics (TBG), Senckenberganlage 25, D-60325, Frankfurt, Germany

    Francesco Dal Grande

  4. Department of Life Sciences, University of Trieste, via Giorgieri 10, 34127, Trieste, Italy

    Lucia Muggia

  5. Departamento de Farmacología, Farmacognosia y Botánica, Facultad de Farmacia, Universidad Complutense de Madrid, 28040, Madrid, Spain

    Pradeep K. Divakar

  6. Grainger Bioinformatics Center, Science & Education, The Field Museum, Chicago, IL, USA

    Felix Grewe

  7. Department of Ecology, Evolution and Diversity, Goethe Universität Frankfurt, Max-von-Laue Str. 11, D-60438, Frankfurt, Germany

    Imke Schmitt

  8. Science & Education, The Field Museum, Chicago, IL, USA

    H. Thorsten Lumbsch

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Smith, H.B., Dal Grande, F., Muggia, L. et al. Metagenomic data reveal diverse fungal and algal communities associated with the lichen symbiosis. Symbiosis 82, 133–147 (2020). https://doi.org/10.1007/s13199-020-00699-4

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