Genome-scale data suggest an ancestral rock-inhabiting life-style of Dothideomycetes (Ascomycota)

Authors: AMETRANO, CLAUDIO - UNIVERSITY OF TRIESTE; GREWE, FELIX - FIELD MUSEUM NATURAL HISTORY; CROUS, PEDRO - FUNGAL BIODIVERSITY; Goodwin, Stephen - Steve; LIANG, CHEN - QINGDAO AGRICULTURAL UNIVERSITY; SELBMANN, LAURA - UNIVERSITY OF TUSCIA; LUMBSCH, H. THOSTEN - FIELD MUSEUM NATURAL HISTORY; LEAVITT, STEVEN - BRIGHAM YOUNG UNIVERSITY; MUGGIA, LUCIA - (NCE, CECR)NETWORKS OF CENTRES OF EXELLENCE OF CANADA, CENTRES OF EXCELLENCE FOR COMMERCILIZATION AND RESEARCH

Submitted to: IMA Fungus
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/5/2019
Publication Date: 10/30/2019
Citation: Ametrano, C.G., Grewe, F., Crous, P.W., Goodwin, S.B., Liang, C., Selbmann, L., Lumbsch, H., Leavitt, S.D., Muggia, L. 2019. Genome-scale data suggest an ancestral rock-inhabiting life-style of Dothideomycetes (Ascomycota). IMA Fungus. 10:19. https://doi.org/10.1186/s43008-019-0018-2.
DOI: https://doi.org/10.1186/s43008-019-0018-2

Interpretive Summary: Dothideomycetes is the most diverse class of fungi and includes species with a wide range of lifestyles, including plant, animal and insect pathogens, and numerous saprobes, many of which have developed the ability to live in extreme environments. However, the evolutionary origin of this class is not known. To determine the likely lifestyle of the earliest Dothideomycetes, genome sequences of four species of pigmented, extremotolerant rock-inhabiting fungi were determined and used to reconstruct the past evolutionary history of the class. The four new genome sequences were compared to those of previously available genomes from 242 species. The resulting evolutionary trees provided consistent results showing that the rock-inhabiting lifestyle is likely ancestral within the class. Additional analyses tested the minimal numbers of genes that could be used to reconstruct the likely evolutionary relationships. This information will be of interest to fungal biologists working on understanding the evolutionary history of the class Dothideomycetes, and to plant pathologists and geneticists trying to understand the origins of pathogenicity to plants and other organisms.

Technical Abstract: Dothideomycetes is the most diverse fungal class in Ascomycota and includes species with a wide range of lifestyles. Previous multilocus studies have investigated the taxonomic and evolutionary relationships of these taxa but often failed to resolve the early diverging nodes and frequently generated inconsistent placements of some clades. Here, we use a phylogenomic approach to resolve relationships in Dothideomycetes, focusing on two genera of melanized, extremotolerant rock-inhabiting fungi, Lichenothelia and Saxomyces, that have been suggested to be early diverging lineages. We generated phylogenomic datasets from newly sequenced and previously available genomes from 242 taxa. We explored the influence of tree inference methods, supermatrix vs. coalescent-based species tree, and the impact of varying amounts of genomic data. Overall, our phylogenetic reconstructions provide consistent and well-supported topologies for Dothideomycetes, recovering Lichenothelia and Saxomyces among the earliest diverging lineages in the class. In addition, many of the major lineages within Dothideomycetes are recovered as monophyletic, and the phylogenomic approach implemented here recovers relationships among these lineages with strong support. Ancestral character state reconstructions suggest that the rock-inhabiting life-style is ancestral within the class.