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David, K. T.

Publications and source records attributed to David, K. T..

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Discovery of additional ancient genome duplications in yeasts

Whole genome duplication (WGD) has had profound macroevolutionary impacts on diverse lineages1,2, preceding adaptive radiations in vertebrates3-5, teleost fish6,7, and angiosperms8,9. In contrast to the many known ancient WGDs in animals10,11 and especially plants12-14, we are aware of evidence for only four in fungi15,16. The oldest of these occurred [~]100 million years ago (mya) and is shared by [~]60 extant Saccharomycetales species17,18, including the bakers yeast Saccharomyces cerevisiae (Fig. 1). Notably, this is the only known ancient WGD in the yeast subphylum Saccharomycotina. The dearth of ancient WGD events in fungi remains a mystery15. Some studies have suggested that fungal lineages that experience chromosome19 and genome15 duplication quickly go extinct, leaving no trace in the genomic record, while others contend that the lack of known WGD is due to an absence of data15,16. Under the second hypothesis, additional sampling and deeper sequencing of fungal genomes should lead to the discovery of more WGD events. Coupling hundreds of recently published genomes from nearly every described Saccharomycotina species with three additional long-read assemblies, we discovered three novel WGD events. While the functions of retained duplicate genes originating from these events are broad, they bear many similarities to the well-known WGD that occurred in the Saccharomycetales17. Our results suggest that WGD may be a more common evolutionary force in fungi than previously believed. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=111 SRC="FIGDIR/small/673279v1_fig1.gif" ALT="Figure 1"> View larger version (29K): org.highwire.dtl.DTLVardef@6a8f47org.highwire.dtl.DTLVardef@1e4a790org.highwire.dtl.DTLVardef@b4e0eforg.highwire.dtl.DTLVardef@11b7795_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOFigure 1.C_FLOATNO Three additional whole genome duplications in Saccharomycotina yeasts. Rates of gene duplication are mapped onto Saccharomycetales (left) and Dipodascales (right) phylogenies. Whole genome duplications indicated along the lineages in which they are predicted to occur. Trees have been pruned for visualization purposes. C_FIG HighlightsO_LIEvidence for three whole genome duplications (WGDs) in Dipodascales yeasts C_LIO_LIImpacts of WGD are broad but bear many similarities to the known WGD in Saccharomycetales yeasts C_LIO_LIDuplicates with many protein-protein interactions are more likely to be retained over long timescales C_LIO_LIWGD in fungi is likely underreported C_LI

evolutionary biology↗

Global patterns of species diversity and distribution in the biomedically and biotechnologically important fungal genus Aspergillus

Aspergillus fungi are key producers of pharmaceuticals, enzymes, and food products and exhibit diverse lifestyles, ranging from saprophytes to opportunistic pathogens. To improve understanding of Aspergillus species diversity, identify key environmental factors influencing their geographic distributions, and estimate the impact of future climate change, we trained a random forest machine learning classifier on 30,542 terrestrial occurrence records for 176 species ([~]40% of known species in the genus) and 96 environmental variables. We found that regions with high species diversity are concentrated in temperate forests, which suggests that areas with mild seasonal variation may serve as diversity hotspots. Species range estimates revealed extensive variability, both within and across taxonomic sections; while some species are cosmopolitan, others have more restricted ranges. Furthermore, range overlap between species is generally low. The top predictors of mean species richness were the index of cumulative human impact and five bioclimatic factors, such as temperature and temperate vs non-temperate ecoregions. Our future climate analyses revealed considerable variation in species range estimates in response to changing climates; some species ranges are predicted to expand (e.g., the food spoilage and mycotoxin-producing Aspergillus versicolor), and others are predicted to contract or remain stable. Notably, the predicted range of the major pathogen Aspergillus fumigatus was predicted to decrease in response to climate change, whereas the range of the major pathogen Aspergillus flavus was predicted to increase and gradually decrease. Our findings reveal how both natural and human factors influence Aspergillus species ranges and highlight their ecological diversity, including the diversity of their responses to changing climates, which is of relevance to pathogen and mycotoxin risk assessment.

ecology↗

Convergent expansions of keystone gene families drive metabolic innovation in a major eukaryotic clade

Many remarkable innovations have repeatedly occurred across vast evolutionary distances. When convergent traits emerge on the tree of life, they are sometimes driven by the same underlying gene families, while other times many different gene families are involved. Conversely, a gene family may be repeatedly recruited for a single trait or many different traits. To understand the general rules governing convergence at both genomic and phenotypic levels, we systematically tested associations between 56 binary metabolic traits and gene count in 14,710 gene families from 993 species of Saccharomycotina yeasts. Using a recently developed phylogenetic approach that reduces spurious correlations, we discovered that gene family expansion and contraction was significantly linked to trait gain and loss in 45/56 (80%) of traits. While 601/746 (81%) of significant gene families were associated with only one trait, we also identified several keystone gene families that were significantly associated with up to 13/56 (23%) of all traits. These results indicate that metabolic innovations in yeasts are governed by a narrow set of major genetic elements and mechanisms.

evolutionary biology↗

Unique trajectory of gene family evolution from genomic analysis of nearly all known species in an ancient yeast lineage

Gene gains and losses are a major driver of genome evolution; their precise characterization can provide insights into the origin and diversification of major lineages. Here, we examined gene family evolution of 1,154 genomes from nearly all known species in the medically and technologically important yeast subphylum Saccharomycotina. We found that yeast gene family and genome evolution are distinct from plants, animals, and filamentous ascomycetes and are characterized by small genome sizes and smaller gene numbers but larger gene family sizes. Faster-evolving lineages (FELs) in yeasts experienced significantly higher rates of gene losses--commensurate with a narrowing of metabolic niche breadth--but higher speciation rates than their slower-evolving sister lineages (SELs). Gene families most often lost are those involved in mRNA splicing, carbohydrate metabolism, and cell division and are likely associated with intron loss, metabolic breadth, and non-canonical cell cycle processes. Our results highlight the significant role of gene family contractions in the evolution of yeast metabolism, genome function, and speciation, and suggest that gene family evolutionary trajectories have differed markedly across major eukaryotic lineages.

evolutionary biology↗

Functional and evolutionary integration of a fungal gene with a bacterial operon

Siderophores are crucial for iron-scavenging in microorganisms. While many yeasts can uptake siderophores produced by other organisms, they are typically unable to synthesize siderophores themselves. In contrast, Wickerhamiella/Starmerella (W/S) clade yeasts gained the capacity to make the siderophore enterobactin following the remarkable horizontal acquisition of a bacterial operon enabling enterobactin synthesis. Yet, how these yeasts absorb the iron bound by enterobactin remains unresolved. Here, we demonstrate that Enb1 is the key enterobactin importer in the W/S-clade species Starmerella bombicola. Through phylogenomic analyses, we show that ENB1 is present in all W/S clade yeast species that retained the enterobactin biosynthetic genes. Conversely, it is absent in species that lost the ent genes, except for Starmerella stellata, making this species the only cheater in the W/S clade that can utilize enterobactin without producing it. Through phylogenetic analyses, we infer that ENB1 is a fungal gene that likely existed in the W/S clade prior to the acquisition of the ent genes and subsequently experienced multiple gene losses and duplications. Through phylogenetic topology tests, we show that ENB1 likely underwent horizontal gene transfer from an ancient W/S clade yeast to the order Saccharomycetales, which includes the model yeast Saccharomyces cerevisiae, followed by extensive secondary losses. Taken together, these results suggest that the fungal ENB1 and bacterial ent genes were cooperatively integrated into a functional unit within the W/S clade that enabled adaptation to iron-limited environments. This integrated fungal-bacterial circuit and its dynamic evolution determines the extant distribution of yeast enterobactin producers and cheaters.

evolutionary biology↗

Saccharomycotina yeasts defy longstanding macroecological patterns

The Saccharomycotina yeasts ("yeasts" hereafter) are a fungal clade of scientific, economic, and medical significance. Yeasts are highly ecologically diverse, found across a broad range of environments in every biome and continent on earth1; however, little is known about what rules govern the macroecology of yeast species and their range limits in the wild2. Here, we trained machine learning models on 12,221 occurrence records and 96 environmental variables to infer global distribution maps for 186 yeast species ([~]15% of described species from 75% of orders) and to test environmental drivers of yeast biogeography and macroecology. We found that predicted yeast diversity hotspots occur in mixed montane forests in temperate climates. Diversity in vegetation type and topography were some of the greatest predictors of yeast species richness, suggesting that microhabitats and environmental clines are key to yeast diversification. We further found that range limits in yeasts are significantly influenced by carbon niche breadth and range overlap with other yeast species, with carbon specialists and species in high diversity environments exhibiting reduced geographic ranges. Finally, yeasts contravene many longstanding macroecological principles, including the latitudinal diversity gradient, temperature-dependent species richness, and latitude-dependent range size (Rapoports rule). These results unveil how the environment governs the global diversity and distribution of species in the yeast subphylum. These high-resolution models of yeast species distributions will facilitate the prediction of economically relevant and emerging pathogenic species under current and future climate scenarios.

ecology↗

Feature Frequency Profile-based phylogenies are inaccurate

Choi and Kim (PNAS, 117: 3678-3686; first published February 4, 2020; https://doi.org/10.1073/pnas.1915766117) used the alignment-free Feature Frequency Profile (FFP) method to reconstruct a broad sketch of the tree of life based on proteome data from 4,023 taxa. The FFP-based reconstruction reports many relationships that strongly contradict the current consensus view of the tree of life and its accuracy has not been tested. Comparison of FFP with current standard approaches, such as concatenation and coalescence, using simulation analyses shows that FFP performs poorly. We conclude that the phylogeny of the tree of life reconstructed by Choi and Kim is suspect based on methodology as well as prior phylogenetic evidence.

evolutionary biology↗