Abstract
Genomic rearrangements associated with speciation often result in variation in chromosome number among closely related species. Malassezia species show variable karyotypes ranging between six and nine chromosomes. Here, we experimentally identified all eight centromeres in M. sympodialis as 3-5-kb long kinetochore-bound regions that span an AT-rich core and are depleted of the canonical histone H3. Centromeres of similar sequence features were identified as CENP-A-rich regions in Malassezia furfur, which has seven chromosomes, and histone H3 depleted regions in Malassezia slooffiae and Malassezia globosa with nine chromosomes each. Analysis of synteny conservation across centromeres with newly generated chromosome-level genome assemblies suggests two distinct mechanisms of chromosome number reduction from an inferred nine-chromosome ancestral state: (a) chromosome breakage followed by loss of centromere DNA and (b) centromere inactivation accompanied by changes in DNA sequence following chromosome-chromosome fusion. We propose that AT-rich centromeres drive karyotype diversity in the Malassezia species complex through breakage and inactivation.
Highlights
Centromeres are the genomic loci on which the kinetochore, a multi-subunit complex, assembles to facilitate high-fidelity chromosome segregation
Previous reports that are based on pulsed-field gel electrophoresis (PFGE) have suggested that chromosome number varies within the Malassezia species complex
We sequenced and assembled the genomes of M. slooffiae, M. globosa, and M. furfur and compared each one with the genome of M. sympodialis in order to understand the karyotype differences observed in members of the Malassezia species complex
Summary
Centromeres are the genomic loci on which the kinetochore, a multi-subunit complex, assembles to facilitate high-fidelity chromosome segregation. A better understanding of how Malassezia organize their genetic material should enable in-depth studies of how these yeasts interact with their human hosts and how they contribute to skin disease, cancer, Crohn’s disease and other health conditions These findings may help scientists to better understand how changes in chromosomes cause new species to evolve. Several lines of evidence suggest that centromeres are species-specific and are among the most rapidly evolving genomic regions, showing variation even between closely related species (Bensasson et al, 2008; Padmanabhan et al, 2008; Rhind et al, 2011; Roy and Sanyal, 2011) This evolution is accompanied by the concomitant evolution of CENP-A and the associated kinetochore proteins (Talbert et al, 2004). On the basis of our results, we propose that centromere loss by two distinct mechanisms drives karyotype diversity
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