Contrasting Genomic Evolution Between Domesticated and WildKluyveromyces lactisYeast Populations

Abstract

The process of domestication has variable consequences on genome evolution leading to different phenotypic signatures. Access to the complete genome sequences of a large number of individuals makes it possible to explore the different facets of this domestication process. Here, we sought to explore the genome evolution of Kluyveromyces lactis, a yeast species well-known for its involvement in dairy processes but also present in natural environments. Using a combination of short and long-read sequencing strategies, we investigated the genomic variability of 41 K. lactis isolates and found that the overall genetic diversity of this species is very high (θw = 3.3 × 10−2) compared to other species such as Saccharomyces cerevisiae (θw = 1.6 × 10−2). However, the domesticated dairy population shows a reduced level of diversity (θw = 1 × 10−3), probably due to a domestication bottleneck. In addition, this entire population is characterized by the introgression of the LAC4 and LAC12 genes, responsible for lactose fermentation and coming from the closely related species, Kluyveromyces marxianus, as previously described. Our results also highlighted that the LAC4/LAC12 gene cluster was acquired through multiple and independent introgression events. Finally, we also identified several genes that could play a role in adaptation to dairy environments through copy number variation. These genes are involved in sugar consumption, flocculation and drug resistance, and may play a role in dairy processes. Overall, our study illustrates contrasting genomic evolution and sheds new light on the impact of domestication processes on it.

Recurrent loss of crossover interference punctuates the recombination landscape across yeast species

“…A way to explore the recombination landscape is to genotype the meiotic progeny of an intra-species hybrid. The K. lactis species is characterized by a high level of genetic diversity (Figure 1) and post-zygotic reproductive isolation (Naumov and Naumova 2002; Friedrich et al . 2023).…”

“…To estimate the evolutionary rates of the ZMM genes, we calculated the mean pairwise dN/dS ratios for all genes present in species with available population genomic datasets, namely S. cerevisiae (1,011 isolates), L. kluyveri (28 isolates), and K. lactis (41 isolates) and having orthologs across the three species (n=3,305) (Friedrich et al . 2015, 2023; Peter et al . 2018).…”

“…Moreover, meiosis proteins in some pathogenic yeast species exhibit increased divergence, and such increased evolutionary rates in protein sequences have been linked to their abandonment (Clark et al 2013;Sun and Blanchard 2014). To estimate the evolutionary rates of the ZMM genes, we calculated the mean pairwise dN/dS ratios for all genes present in species with available population genomic datasets, namely S. cerevisiae (1,011 isolates), L. kluyveri (28 isolates), and K. lactis (41 isolates) and having orthologs across the three species (n=3,305) (Friedrich et al 2015(Friedrich et al , 2023Peter et al 2018). Additionally, we identified meiosis genes as those annotated with the gene ontology term 'meiosis' in S. cerevisiae (n=190) (Table S7).…”

“…Figure1. A) Population structure of K. lactis strains(Friedrich et al 2023). Haploids isolates used to generate the mapping population are highlighted in blue and red.…”

Spindle architecture constrains karyotype in budding yeast

“…Below that, cells experience reduced fitness. In nature, the lowest chromosome number observed in other yeast species with similar simple point centromeres is six, in Kluyveromyces lactis , a haploid species with a similar genome size to S. cerevisiae ( 25, 26 ). Budding yeasts have a small spindle with just a single kMT per chromosome, which may exacerbate the effect of low chromosome count on mitosis.…”