Abstract
Centromeres of Candida albicans form on unique and different DNA sequences but a closely related species, Candida tropicalis, possesses homogenized inverted repeat (HIR)-associated centromeres. To investigate the mechanism of centromere type transition, we improved the fragmented genome assembly and constructed a chromosome-level genome assembly of C. tropicalis by employing PacBio sequencing, chromosome conformation capture sequencing (3C-seq), chromoblot, and genetic analysis of engineered aneuploid strains. Further, we analyzed the 3D genome organization using 3C-seq data, which revealed spatial proximity among the centromeres as well as telomeres of seven chromosomes in C. tropicalis. Intriguingly, we observed evidence of inter-centromeric translocations in the common ancestor of C. albicans and C. tropicalis. Identification of putative centromeres in closely related Candida sojae, Candida viswanathii and Candida parapsilosis indicates loss of ancestral HIR-associated centromeres and establishment of evolutionary new centromeres (ENCs) in C. albicans. We propose that spatial proximity of the homologous centromere DNA sequences facilitated karyotype rearrangements and centromere type transitions in human pathogenic yeasts of the CUG-Ser1 clade.
Highlights
The efficient maintenance of the genetic material and its propagation to subsequent generations determine the fitness of an organism
Chromosomal rearrangements, on the other hand, are often observed during speciation (Searle, 1998). Such structural changes begin with the formation of at least one DNA double-strand break (DSB), which is generally repaired by homologous recombination (HR) or non-homologous end joining (NHEJ) in vivo
Based on the contour clamped homogenized electric field (CHEF)-gel karyotyping (Figure 1B) and 3C-seq data (Figure 1— figure supplement 1E–G), we joined two contigs and rectified a misjoin in Assembly C to produce an assembly of seven chromosomes and five short orphan haplotigs (OHs)
Summary
The efficient maintenance of the genetic material and its propagation to subsequent generations determine the fitness of an organism. Chromosomal rearrangements, on the other hand, are often observed during speciation (Searle, 1998) Such structural changes begin with the formation of at least one DNA double-strand break (DSB), which is generally repaired by homologous recombination (HR) or non-homologous end joining (NHEJ) in vivo. Studies using engineered in vivo model systems suggested that the success of DSB repair through HR depends upon an efficient identification of a template donor. This process of ‘homology search’ is facilitated by the physical proximity and the extent of DNA sequence homology (Lee et al, 2016; Agmon et al, 2013; Burgess and Kleckner, 1999). Apicomplexans, and certain plants, centromeres cluster inside the nucleus (Muller et al, 2019), which may facilitate translocations between two chromosomes involving their centromeric and adjacent pericentromeric loci
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