Different trajectories of polyploidization shape the genomic landscape of theBrettanomyces bruxellensisyeast species

Abstract

Polyploidization events are observed across the tree of life and occurred in many fungi, plant and animal species. Polyploidy is thought to be an important source of speciation and tumorigenesis. However, the origins of polyploid populations are not always clear and little is known about the precise nature and structure of their complex genome. Using a long-read sequencing strategy, we sequenced a large number of isolates from the Brettanomyces bruxellensis yeast species, which is found in anthropized environments (e.g. beer, contaminant of wine, kombucha and ethanol production) and characterized by several polyploid subpopulations. To reconstruct the polyploid genomes, we phased them by using different strategies and we found that each subpopulation had a unique polyploidization history with distinct trajectories. The polyploid genomes contain either genetically closely related (with a genetic divergence < 1%) or diverged copies (> 3%), indicating auto- as well as allopolyploidization events. These latest events have occurred independently with a specific and unique donor in each of the polyploid subpopulations, and exclude the known Brettanomyces sister species as possible donors. Finally, loss of heterozygosity events have shaped the structure of these polyploid genomes and underline their dynamic. Overall, our study highlights the multiplicity of the trajectories leading to polyploid genomes within a same species.

Loss of heterozygosity results in rapid but variable genome homogenization across yeast genetic backgrounds

“…Hybridization is a process common to the life history of many organisms and rapidly generates genomic diversity (14,79,80). Even though new hybrids tend to exhibit a low spore fertility, natural hybridizations have played an essential role in the diversification and evolution of the genome of many fungal, plant, and animal species.…”

“…The diploid organisms (or those with a higher ploidy) are usually heterozygous for many of these genetic variants across the genome. Nevertheless, a large number of studies have pointed out that regions of the genome can frequently become homozygous for these polymorphisms during mitotic divisions (7)(8)(9)(10)(11)(12)(13)(14)(15). These loss of heterozygosity (LOH) events result from the transfer of information from one homologous chromosome to the other, primarily a consequence of mitotic recombination, among other mechanisms (16).…”

Brettanomyces bruxellensis: Overview of the genetic and phenotypic diversity of an anthropized yeast

“…This large population study allowed the identification of different genetic subpopulations within B. bruxellensis, which were subsequently validated and refined by whole genome sequencing approaches (Eberlein et al, 2021;Gounot et al, 2020;Serra Colomer, Chailyan, et al, 2020;Table S1). At least six subgroups can now be considered, either diploid (two groups) or triploid (four groups; Figure 1b).…”

“…Over the past decade, several de novo assemblies have been published with increasing quality (Table 1), in particular thanks to the combination of long-read sequencing (e.g., Oxford Nanopore sequencing) with short-read sequencing (Fournier et al, 2017). Such high quality assemblies were used as reference genomes for population genomic surveys (Eberlein et al, 2021;Gounot et al, 2020;Serra Colomer, Chailyan, et al, 2020). These population studies revealed that the pangenome is composed of 5,409 ORFs (open reading frames) with 5,106 core and 303 accessory ORFs within the species.…”

“…Brettanomyces bruxellensis subpopulations are represented by different colours and named from previous reports (Avramova, Cibrario, et al, 2018;Gounot et al, 2020). The tree was built from whole genome Illumina short-read sequencing of 71 B. bruxellensis isolates aligned to the reference genome B. bruxellensis (Fournier et al, 2017) and 24,313 genetic variants evenly distributed across the genome (Eberlein et al, 2021). The ploidy level of each population was schematized, two chromosomes represent diploid groups, three chromosomes represent triploids ones.…”