This month’s Genome Watch highlights a large-scale sequencing project that enriches our understanding of yeast evolution and diversity. You have full access to this article via your

institution. Download PDF In contrast to most eukaryotes, fungi have relatively small and simple genomes, making them an attractive resource for large-scale genomic studies. Even more

attractive, the budding yeast subphylum (Saccharomycotina) has some of the most straightforward genomes to assemble and annotate, as they are generally small (10-20 Mb) and intron-poor. The

Saccharomycotina also harbour some of the most important fungi for bioindustry, being essential for converting sugars into ethanol and other valuable chemicals. The genome of _Saccharomyces

extraordinary range across their functional repertoire. Combining these data with 100 published yeast genomes and phenotypic information on metabolic capabilities for all species in their

study, the authors were able to make key connections between gene pathways and particular metabolic traits. For example, they inferred that the common ancestral budding yeast could

assimilate nitrate, xylose and galactose, but lacked the ability to ferment glucose. Credit: Philip Patenall/Springer Nature Limited This study also explored how distribution of these traits

across the subphylum came to be. Through phylogeny reconstruction paired with metabolic analysis, the authors were able to trace the loss and gain of new traits through subphylum history.

By inferring the traits of the budding yeast common ancestor, they implicate gene loss as a main driver of diversification. Since this work has been published, several follow-up studies have

been conducted that use subsets of the genomic data from this project to explore budding yeast diversity and evolution. To follow up on gene loss as the evolutionary driver of diversity,

Steenwyk et al.3 explored a fast-evolving lineage in the genus _Hanseniaspora_, a cosmopolitan lineage that is often found in high abundance on grapes and in wine must. They found that this

lineage lost many cell cycle and DNA repair genes and represents an unusual example of long-term survival of a hypermutator lineage. Hypermutator species have lost many genes in addition to

these, harbouring the lowest number of genes compared to any other budding yeast. Furthermore, the observed gene losses were consistent with their known metabolic traits (for example, the

inability to grow on various carbon sources). Although gene losses are important for driving diversification in budding yeasts, horizontal gene transfer (HGT) is another interesting

contributor to their evolution. Kominek et al.4 identified the first example of an HGT event involving transfer of a full operon from bacteria into yeasts. This operon contained siderophore

biosynthesis pathway genes, was functional, and enabled these yeasts to acquire a new metabolic trait for iron uptake. By exploring conservation of iron uptake and storage systems across 175

fungi including 17 closely related genomes from the clade encompassing _Wickerhamiella_ and _Starmerella_ yeasts, the authors found that this biosynthetic capability came from a single HGT

event at the root of _Wickerhamiella_ and _Starmerella_. From 186 budding yeast genomes, over 800 genes were predicted to be acquired from bacteria by HGT, and most of these genes are

associated with metabolism2. Thanks to the sequencing efforts of Shen et al. and others, we now have a rich sampling of an ancient (~400 million years old) eukaryotic subphylum. This

provides us with the first opportunity to explore eukaryotic evolution at this magnitude and has already provided various important insights into the basic biology of eukaryotes. In addition

to those discussed above, these data have been used to characterize variation and alterations of codon usage5 and reinvention of mating-type switching6. We expect that the completion of the

Y1000+ project will provide an even fuller picture of the subphylum and has the potential to reveal many new and important insights into the biology of yeasts and eukaryotes at large.

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subphylum. _Cell_ 175, 1533–1545 (2018). Article  CAS  Google Scholar  * Steenwyk, J. L. et al. Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding

yeasts. _PLOS Biology_ 17, e3000255 (2019). Article  CAS  Google Scholar  * Kominek, J. et al. Eukaryotic acquisition of a bacterial operon. _Cell_ 176, 1356–1366 (2019). Article  CAS 

Google Scholar  * Labella, A. L. et al. Variation and selection on codon usage bias across an entire subphylum. _PLOS Genetics_ 15, e1008304 (2019). Article  Google Scholar  * Krassowski, T.

et al. Multiple reinventions of mating-type switching during budding yeast evolution. _Current Biology_ 29, 2555–2562 (2019). Article  CAS  Google Scholar  Download references AUTHOR

INFORMATION AUTHORS AND AFFILIATIONS * DOE Joint Genome Institute Walnut Creek, California, USA Sara Calhoun, Stephen J. Mondo & Igor V. Grigoriev Authors * Sara Calhoun View author

publications You can also search for this author inPubMed Google Scholar * Stephen J. Mondo View author publications You can also search for this author inPubMed Google Scholar * Igor V.

Grigoriev View author publications You can also search for this author inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to Igor V. Grigoriev. ETHICS DECLARATIONS COMPETING

INTERESTS The authors declare no competing interests. RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Calhoun, S., Mondo, S.J. & Grigoriev, I.V.

Yeasts and how they came to be. _Nat Rev Microbiol_ 17, 649 (2019). https://doi.org/10.1038/s41579-019-0274-6 Download citation * Published: 26 September 2019 * Issue Date: November 2019 *

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