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Discovery of novel intermediate forms redefines the fungal tree of life

Abstract

Fungi are the principal degraders of biomass in terrestrial ecosystems and establish important interactions with plants and animals1,2,3. However, our current understanding of fungal evolutionary diversity is incomplete4 and is based upon species amenable to growth in culture1. These culturable fungi are typically yeast or filamentous forms, bound by a rigid cell wall rich in chitin. Evolution of this body plan was thought critical for the success of the Fungi, enabling them to adapt to heterogeneous habitats and live by osmotrophy: extracellular digestion followed by nutrient uptake5. Here we investigate the ecology and cell biology of a previously undescribed and highly diverse form of eukaryotic life that branches with the Fungi, using environmental DNA analyses combined with fluorescent detection via DNA probes. This clade is present in numerous ecosystems including soil, freshwater and aquatic sediments. Phylogenetic analyses using multiple ribosomal RNA genes place this clade with Rozella, the putative primary branch of the fungal kingdom1. Tyramide signal amplification coupled with group-specific fluorescence in situ hybridization reveals that the target cells are small eukaryotes of 3–5 μm in length, capable of forming a microtubule-based flagellum. Co-staining with cell wall markers demonstrates that representatives from the clade do not produce a chitin-rich cell wall during any of the life cycle stages observed and therefore do not conform to the standard fungal body plan5. We name this highly diverse clade the cryptomycota in anticipation of formal classification.

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Figure 1: Identification of the cryptomycota.
Figure 2: Structural properties of cryptomycota cells and evidence for different life cycle stages.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

Novel sequence data have been deposited in GenBank under accession numbers FJ687265, FJ687267 and FJ687268.

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Acknowledgements

We thank: N. J. Talbot for advice, K. Gull for the TAT1 antibody, L. Guillou for access to curated SSU database and the Broad Institute of the Massachusetts Institute of Technology and Harvard for making their Rhizopus and Batrachochytrium genome sequence data publicly available. T.A.R. thanks the Leverhulme Trust for fellowship support. This work was primarily supported by a Natural Environment Research Council grant UK (NE/F011709/1). Additional support came from the Systematic Research Fund (awarded by the Systematics Association and the Linnean Society) to T.A.R., project FLAME (CGL2010-16304, MICINN) to R. M. and the BioMarKs project (European Funding Agencies from the ERA-net program BiodivERsA) to T.A.R. and R.M.

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Contributions

This study was conceived by T.A.R. and M.D.M.J. with assistance from D.B. and R.M.. M.D.M.J. performed the molecular biology experiments with assistance from I.F. (FISH), C.G. (immunolocalization) and M.J.E. (microscopy). T.A.R. performed the bioinformatics and phylogenetic analysis. T.A.R. and M.D.M.J. wrote the paper with assistance from D.B. and R.M.

Corresponding author

Correspondence to Thomas A. Richards.

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The authors declare no competing financial interests.

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This file contains Supplementary Figures 1-7 with legends and Supplementary Tables 1-6. (PDF 23617 kb)

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Jones, M., Forn, I., Gadelha, C. et al. Discovery of novel intermediate forms redefines the fungal tree of life. Nature 474, 200–203 (2011). https://doi.org/10.1038/nature09984

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