Saccharomycetaceae: delineation of fungal genera based on phylogenomic analyses, genomic relatedness indices and genomics-based synapomorphies

Abstract

A correct classification of fungi, including yeasts, is of prime importance to understand fungal biodiversity and to communicate about this diversity. Fungal genera are mainly defined based on phenotypic characteristics and the results of single or multigene-based phylogenetic analyses. However, because yeasts often have less phenotypic characters, their classification experienced a strong move towards DNA-based data, from short ribosomal sequences to multigene phylogenies and more recently to phylogenomics. Here, we explore the usefulness of various genomics-based parameters to circumscribe fungal genera more correctly taking the yeast domain as an example. Therefore, we compared the results of a phylogenomic analysis, average amino acid identity (AAI) values, the presence of conserved signature indels (CSIs), the percentage of conserved proteins (POCP) and the presence-absence patterns of orthologs (PAPO). These genome-based metrics were used to investigate their usefulness in demarcating 13 hitherto relatively well accepted genera in Saccharomycetaceae, namely Eremothecium, Grigorovia, Kazachstania, Kluyveromyces, Lachancea, Nakaseomyces, Naumovozyma, Saccharomyces, Tetrapisispora, Torulaspora, Vanderwaltozyma, Zygosaccharomyces and Zygotorulaspora. As a result, most of these genera are supported by the genomics-based metrics, but the genera Kazachstania, Nakaseomyces and Tetrapisispora were shown to be genetically highly diverse based on the above listed analyses. Considering the results obtained for the presently recognized genera, a range of 80-92 % POCP values and a range of 60-70 % AAI values might be valuable thresholds to discriminate genera in Saccharomycetaceae. Furthermore, the genus-specific genes identified in the PAPO analysis and the CSIs were found to be useful as synapomorphies to characterize and define genera in Saccharomycetaceae. Our results indicate that the combined monophyly-based phylogenomic analysis together with genomic relatedness indices and synapomorphies provide promising approaches to delineating yeast genera and likely those of filamentous fungi as well. The genera Kazachstania, Nakaseomyces and Tetrapisispora are revised and we propose eight new genera and 41 new combinations. Citation: Liu F, Hu Z-D, Yurkov A, et al. 2024. Saccharomycetaceae: delinaeation of fungal genera based on phylogenomic analyses, genomic relatedness indices and genomics-based synapomorphies. Persoonia 52: 1-21. https://doi.org/10.3767/persoonia.2024.52.01.

Keywords: AAI; CSI; PAPO; POCP; barcode; new taxa; phenotypic comparisons; phylogenomics; taxonomy; yeasts.

Fig. 1

Phylogenomics tree inferred using 115 single copy orthologue proteins showing the phylogenetic relationship between genera in Saccharomycetaceae. Bootstrap percentages of maximum likelihood analysis over 50 % from 1 000 bootstrap replicates are shown on the major branches. Bar = 0.2 substitutions per nucleotide position.

Fig. 2

Phylogenetic tree inferred using a combined dataset of SSU, ITS, D1/D2, RPB1, RPB2 and TEF1 nucleotide sequences, showing the phylogenetic relationship between genera in Saccharomycetaceae. Bootstrap percentages of maximum likelihood analysis over 50 % from 1 000 bootstrap replicates are shown on the major branches. Bar = 0.1 substitutions per nucleotide position.

Fig. 3

Phylogenetic tree inferred using the concatenated ITS and D1/D2 sequences showing the phylogenetic relationship between genera in Saccharomycetaceae. Bootstrap percentages of maximum likelihood analysis over 50 % from 1 000 bootstrap replicates are shown on the major branches. Bar = 0.2 substitutions per nucleotide position.

Fig. 4

Interrelationship between shared gene content and AAI values of 13 well-defined genera of Saccharomycetaceae. The X-axis displays the AAI similarity between strains. The Y-axis shows the rate of genome sharing between strains (the genome sharing rate = number of orthologous genes/the genes number in the minimum genome between two strains). Green dots indicate AAI values between strains of the same genus, but not of the same species. The blue dots indicate the AAI values between strains of the same family and different genera. The red dots indicate the AAI values of the same order and different family (Saccharomycetaceae and Saccharomycodaceae).