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A first glimpse at the peculiar genome and population structure of Brettanomyces bruxellensis

To date, genome assemblies of six B. bruxellensis strains have been published, with several more on the way. Five of these six strains originate from the wine industry (Borneman et al., 2014; Curtin et al., 2012; Piskur et al., 2012; Valdes et al., 2014; Woolfit et al., 2007), while one was isolated from lambic beer (Crauwels et al., 2014). In 2007, Woolfit and coworkers published the first exploratory genome survey of the French wine spoilage strain CBS2499, providing a first glimpse of the surprising features of the B. bruxellensis genome (Woolfit et al., 2007). Initially, CBS2499 was believed to be haploid, but this was quickly debunked by a follow-up study in which a more in-depth de-novo assembly was performed, showing that the strain was actually diploid (Piskur et al., 2012). This latter study described a total assembly size of 13.4 Mb and was able to identify 5600 genes, from which 75% could be functionally annotated. Around the same time, a second strain was sequenced (AWRI 1499), yielding a 12.7-Mb assembly and 4969 predicted genes (Curtin et al., 2012). ST05.12/22, the only non-wine isolate sequenced to date, was shown to be 13.0 Mbp and 5255 genes were predicted (Crauwels et al., 2014). Recently, the first South American isolate was sequenced (Valdes et al., 2014), and Borneman and coworkers published an in-depth genomic comparison of four wine isolates: the previously sequenced AWRI 1499 and CBS2499 and two newly sequenced strains, AWRI 1608 and AWRI 1613 (Borneman et al., 2014). Analysis of the sequences revealed some interesting similarities of, but also peculiar differences between, the different strains.

First, it was shown that the ploidy of B. bruxellensis is variable: while CBS2499, AWRI 1613, and ST05.12/22 were shown to be diploid, haplotyping analysis revealed that AWRI 1499 and AWRI 1608 consist of two moderately heterozygous sets of chromosomes (a core, diploid fraction) and a third haploid set that is divergent (Borneman et al., 2014; Crauwels et al., 2014). Fascinatingly, the variable haploid fraction was shown to be phylogenetically distant, suggesting that multiple independent hybridization events were involved in the emergence of these allotriploids. It is not yet clear if the divergent haploid set originates from a separate species or distantly related B. bruxellensis strains.

Second, it was shown that the karyotype varies drastically from strain to strain (Hellborg and Piskur, 2009). B. bruxellensis strains can contain between four and nine chromosomes, and the size of these chromosomes can range from 1 to 6 Mbp. This is peculiar, since chromosome configuration is usually well preserved among populations belonging to the same species; for example, different strains of S. cerevisiae are collinear and consist of 16 chromosomes. However, since newly formed hybrid genomes tend to be very unstable (as often shown for Saccharomyces hybrids; Antunovics et al., 2005; Dunn et al., 2013; Piotrowski et al., 2012), mechanisms that drive genome stabilization could at least explain some of the extreme karyotype variability observed. Additionally, the karyotype variability could suggest that B. bruxellensis might employ frequent variations in chromosome structure to increase their genome variability and competitiveness. However, although genomic mutability is beneficial for the adaptability of the species, it can impede sexual reproduction and drive speciation (Fischer et al., 2000). This could explain the absence (or very low frequency) of sexual reproduction in B. bruxellensis (see further).

Third, even though Brettanomyces did not undergo a whole genome duplication (WGD) event, many localized duplications (CNVs)] and even opposing copy number changes in the same region between strains, were observed (Borneman et al., 2014; Crauwels et al., 2014, 2015b). Since gene duplication is a major source of new genes, it is a central factor influencing genome evolution (Ohno, 1970; Wolfe and Li, 2003). The observed CNVs were frequent in subtelomeric regions and often included genes involved in nutrient (sugar) metabolism, indicating that they might affect utilization of specific carbon sources (Borneman et al., 2014). However, a more in-depth study on the paralogues is required to draw strong conclusion.

 
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