The yeast mating-type switching endonuclease HO is a domesticated member of an unorthodox homing genetic element family

Abstract

<jats:title>Summary</jats:title><jats:p>The mating-type switching endonuclease HO plays a central role in the natural life cycle of <jats:italic>Saccharomyces cerevisiae</jats:italic>, but its evolutionary origin is unknown. <jats:italic>HO</jats:italic> is a recent addition to yeast genomes, present in only a few genera. It resembles a degenerated intein fused to a zinc finger domain. Here we show that <jats:italic>HO</jats:italic> is structurally and phylogenetically related to a family of unorthodox homing genetic elements found in <jats:italic>Torulaspora</jats:italic> and <jats:italic>Lachancea</jats:italic> yeasts. These <jats:italic>WHO</jats:italic> elements integrate into the aldolase gene <jats:italic>FBA1</jats:italic>, replacing its 3’ end each time. Their structural organization is different from all known classes of homing elements. We show that a WHO protein cleaves <jats:italic>Torulaspora delbrueckii FBA1</jats:italic> efficiently and in an allele-specific manner, leading to DNA repair by gene conversion or NHEJ. The DNA rearrangement steps during <jats:italic>WHO</jats:italic> element homing are very similar to those during mating-type switching, and indicate that <jats:italic>HO</jats:italic> is a domesticated <jats:italic>WHO</jats:italic>-like element.</jats:p>

Improvement of Torulaspora delbrueckii Genome Annotation: Towards the Exploitation of Genomic Features of a Biotechnologically Relevant Yeast

“…Furthermore, of particular interest was the homology detected for the genus Lachancea : 93.1% of genes were found to be homologous between T. delbrueckii COFT1 and species L. lanzarotensis and 92.8% with species L. thermotolerans . This proximity between Lachancea and T. delbrueckii was shown before, detailing shared traits that were mainly related with osmotolerance and ethanol resistance [ 25 , 65 ], but also remarkable similarity considering the clusters of the mating-type switching endonuclease HO genes [ 38 ]. L. thermotolerans, especially, has been associated with a strain-dependent production of a diverse range of metabolic intermediates for L-lactic acid production [ 65 , 66 ], as well as ethyl lactate [ 67 ].…”

“…Finally, the genome of SRCM101298 strain, which was added to the database in July 2017, is considerably less explored and is assembled at the contig level. Additional genomes of T. delbrueckii were recently released [ 38 ]; however, not in the timeframe of the current work.…”

Giant GAL gene clusters for the melibiose‐galactose pathway in Torulaspora

“…T. globosa is a sister species to T. maleeae . We sequenced the genomes of 12 strains of T. globosa (Coughlan et al, 2020 and A.Y.C. and K.H.W., unpublished) and found that 11 of them, including the type strain CBS764 T , have no GAL genes.…”

“…Coverage was approximately 85×. All other genome sequences are from sources cited in Coughlan et al (2020).…”

“…In this study, we used genome sequences from additional species and strains of Torulaspora , generated in other studies (Coughlan et al, 2020; Galeote et al, 2018; Shen et al, 2018), to investigate the origin and evolution of GAL clusters in Torulaspora and related genera. We find that the large GAL cluster in the type strain of T. delbrueckii is atypical of this species, because all 14 other T. delbrueckii strains that we examined have no cluster, and we show that the cluster in the type strain of T. delbrueckii was acquired from T. franciscae recently by horizontal gene transfer.…”