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Class-wide genomic tendency throughout specific extremes in black fungi

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Abstract

The classes Dothideomycetes and Eurotiomycetes include constitutively melanized fungi adapted to extreme conditions and they are widely distributed in diverse hostile habitats worldwide. Yet, despite the growing interest in these fungi, there is a considerable gap of knowledge on their functionality. Their genomic analysis is still in its infancy and the possibility to understand their adaptive strategies and exploit their potentialities in bioremediation is very limited. Here, we supply a genome catalog of 118 black fungi, encompassing different ecologies, phylogenies and lifestyles, as a first example of a comparative genomic study at high level of diversity. Results indicate that, as a rule, Dothideomycetes show more variable genome size and that larger genomes are associated with harshest conditions; low temperature tolerance and DNA repair capacity are overrepresented in their genomes. In Eurotiomycetes high temperature tolerance and capacity to metabolize hydrocarbons are more frequently present and these abilities are positively correlated with the human presence. The genomic features are consistent with the prevalent ecologies in the two classes. Indeed, Dothideomycetes are more common in cold and dry environments with high capacity for DNA repair being consistent with the normally highly UV-impacted conditions in their habitats; in contrast, Eurotiomycetes spread mainly in hot human-impacted sites with industrial pollution. Mean annual temperature and isothermality are positively correlated with tolerance to high temperatures in Dothideomycetes, suggesting that, despite their preference for the cold, they are potentially equipped to survive even when temperatures rise due to the global warming.

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Data availability

The genome assemblies and annotation datasets are available on Zenodo repository (https://doi.org/10.5281/zenodo.7764743, https://doi.org/https://doi.org/10.5281/zenodo.7764743).

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Acknowledgements

C.C. and L.S. wish to thank the Italian National Antarctic Research Program for funding sampling campaigns and research activities in Italy in the frame of PNRA projects. The Italian Antarctic National Museum (MNA) is kindly acknowledged for financial support to the Mycological Section of the MNA and for providing fungal specimens used in this study stored in the Culture Collection of Antarctic fungi (MNA-CCFEE), University of Tuscia, Italy.

Funding

C.C. is supported by the European Commission under the Marie Sklodowska-Curie Grant Agreement No. 702057 (DRYLIFE). M.D-B. is supported by a project from the Spanish Ministry of Science and Innovation (PID2020-115813RA-I00), and a project of the Fondo Europeo de Desarrollo Regional (FEDER) and the Consejería de Transformación Económica, Industria, Conocimiento y Universidades of the Junta de Andalucía (FEDER Andalucía 2014–2020 Objetivo temático '01 – Refuerzo de la investigación, el desarrollo tecnológico y la innovación') associated with the research project P20_00879 (ANDABIOMA). N.S. receives funding from the ERC (ERC-STG project MetaPG-716575 and ERC-CoG microTOUCH-101045015). J.E.S. is a CIFAR fellow in the Fungal Kingdom: Threats and Opportunities program. T.K. and J.E.S. were partially supported by NIH NIAID R01-GM108492. Data analyses performed at the High-Performance Computing Cluster at the University of California Riverside in the Institute of Integrative Genome Biology were supported by NSF grant DBI-1429826 and NIH grant S10-OD016290.

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Author notes

  1. Claudia Coleine, Tania Kurbessoian, and Giulia Calia have contributed equally to this work.

Authors and Affiliations

  1. Department of Ecological and Biological Sciences, University of Tuscia, Viterbo, Italy

    Claudia Coleine, Daniela Isola & Laura Selbmann

  2. Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA, USA

    Tania Kurbessoian & Jason E. Stajich

  3. Research and Innovation Centre, Fondazione Edmund Mach, San Michele All’Adige, Italy

    Giulia Calia, Alessandro Cestaro, Massimo Pindo & Claudio Donati

  4. Faculty of Science and Technology, Free University of Bozen-Bolzano, Bolzano, Italy

    Giulia Calia

  5. Laimburg Research Centre, Pfatten (Vadena), South Tyrol, Italy

    Giulia Calia

  6. Laboratorio de Biodiversidad y Funcionamiento Ecosistémico, Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSIC, Seville, Spain

    Manuel Delgado-Baquerizo

  7. National Research Council (CNR), Institute of Biomembranes, Bioenergetics and Molecular Biotechnologies (IBIOM), Bari, Italy

    Alessandro Cestaro

  8. Department CIBIO, University of Trento, Trento, Italy

    Federica Armanini, Francesco Asnicar & Nicola Segata

  9. Institute for Integrative Genome Biology, University of California, Riverside, Riverside, CA, USA

    Jason E. Stajich

  10. RadboudUMC/CWZ Center of Expertise for Mycology, Nijmegen, The Netherlands

    Sybren de Hoog

  11. Mycological Section, Italian Antarctic National Museum (MNA), Genoa, Italy

    Laura Selbmann

Authors
  1. Claudia Coleine
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  2. Tania Kurbessoian
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Contributions

Claudia Coleine, Sybren de Hoog, and Laura Selbmann conceived the study. Claudia Coleine, Nicola Segata, Jason E. Stajich e Claudio Donati produced the sequencing data. Tania Kurbessoian, Giulia Calia, Jason E. Stajich, Alessandro Cestaro, and Claudia Coleine assembled and annotated genomes. Manuel Delgado-Baquerizo has provided environmental metadata. Statistical analyses and environmental modeling were done by Claudia Coleine. The manuscript was written by Claudia Coleine, Sybren de Hoog, and Laura Selbmann with contributions from all authors. All authors read and approved the final manuscript.

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Correspondence to Claudia Coleine, Sybren de Hoog or Laura Selbmann.

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Coleine, C., Kurbessoian, T., Calia, G. et al. Class-wide genomic tendency throughout specific extremes in black fungi. Fungal Diversity 125, 121–138 (2024). https://doi.org/10.1007/s13225-024-00533-y

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