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Novel centromeric loci of the wine and beer yeast dekkera bruxellensis CEN1 and CEN2

Ishchuk, Olena P. LU ; Zeljko, Tanja Vojvoda ; Schifferdecker, Anna J. LU ; Wisén, Sofia Mebrahtu LU ; Hagström, Åsa K. ; Rozpedowska, Elzbieta LU ; Andersen, Mikael Rørdam ; Hellborg, Linda LU ; Ling, Zhihao and Sibirny, Andrei A. , et al. (2016) In PLoS ONE 11(8).
Abstract

The wine and beer yeast Dekkera bruxellensis thrives in environments that are harsh and limiting, especially in concentrations with low oxygen and high ethanol. Its different strains' chromosomes greatly vary in number (karyotype). This study isolates two novel centromeric loci (CEN1 and CEN2), which support both the yeast's autonomous replication and the stable maintenance of plasmids. In the sequenced genome of the D. bruxellensis strain CBS 2499, CEN1 and CEN2 are each present in one copy. They differ from the known "point" CEN elements, and their biological activity is retained within ~900-1300 bp DNA segments. CEN1 and CEN2 have features of both "point" and "regional" centromeres: They contain conserved DNA elements, ARSs, short... (More)

The wine and beer yeast Dekkera bruxellensis thrives in environments that are harsh and limiting, especially in concentrations with low oxygen and high ethanol. Its different strains' chromosomes greatly vary in number (karyotype). This study isolates two novel centromeric loci (CEN1 and CEN2), which support both the yeast's autonomous replication and the stable maintenance of plasmids. In the sequenced genome of the D. bruxellensis strain CBS 2499, CEN1 and CEN2 are each present in one copy. They differ from the known "point" CEN elements, and their biological activity is retained within ~900-1300 bp DNA segments. CEN1 and CEN2 have features of both "point" and "regional" centromeres: They contain conserved DNA elements, ARSs, short repeats, one tRNA gene, and transposon-like elements within less than 1 kb. Our discovery of a miniature inverted-repeat transposable element (MITE) next to CEN2 is the first report of such transposons in yeast. The transformants carrying circular plasmids with cloned CEN1 and CEN2 undergo a phenotypic switch: They form fluffy colonies and produce three times more biofilm. The introduction of extra copies of CEN1 and CEN2 promotes both genome rearrangements and ploidy shifts, with these effects mediated by homologous recombination (between circular plasmid and genome centromere copy) or by chromosome breakage when integrated. Also, the proximity of the MITE-like transposon to CEN2 could translocate CEN2 within the genome or cause chromosomal breaks, so promoting genome dynamics. With extra copies of CEN1 and CEN2, the yeast's enhanced capacities to rearrange its genome and to change its gene expression could increase its abilities for exploiting new and demanding niches.

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publishing date
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Contribution to journal
publication status
published
subject
in
PLoS ONE
volume
11
issue
8
article number
e0161741
publisher
Public Library of Science (PLoS)
external identifiers
  • wos:000382258600089
  • scopus:84991508707
ISSN
1932-6203
DOI
10.1371/journal.pone.0161741
language
English
LU publication?
yes
id
6eefd210-58c3-47ad-8125-3a7210a54ec0
date added to LUP
2016-11-07 09:35:42
date last changed
2024-01-04 15:41:03
@article{6eefd210-58c3-47ad-8125-3a7210a54ec0,
  abstract     = {{<p>The wine and beer yeast Dekkera bruxellensis thrives in environments that are harsh and limiting, especially in concentrations with low oxygen and high ethanol. Its different strains' chromosomes greatly vary in number (karyotype). This study isolates two novel centromeric loci (CEN1 and CEN2), which support both the yeast's autonomous replication and the stable maintenance of plasmids. In the sequenced genome of the D. bruxellensis strain CBS 2499, CEN1 and CEN2 are each present in one copy. They differ from the known "point" CEN elements, and their biological activity is retained within ~900-1300 bp DNA segments. CEN1 and CEN2 have features of both "point" and "regional" centromeres: They contain conserved DNA elements, ARSs, short repeats, one tRNA gene, and transposon-like elements within less than 1 kb. Our discovery of a miniature inverted-repeat transposable element (MITE) next to CEN2 is the first report of such transposons in yeast. The transformants carrying circular plasmids with cloned CEN1 and CEN2 undergo a phenotypic switch: They form fluffy colonies and produce three times more biofilm. The introduction of extra copies of CEN1 and CEN2 promotes both genome rearrangements and ploidy shifts, with these effects mediated by homologous recombination (between circular plasmid and genome centromere copy) or by chromosome breakage when integrated. Also, the proximity of the MITE-like transposon to CEN2 could translocate CEN2 within the genome or cause chromosomal breaks, so promoting genome dynamics. With extra copies of CEN1 and CEN2, the yeast's enhanced capacities to rearrange its genome and to change its gene expression could increase its abilities for exploiting new and demanding niches.</p>}},
  author       = {{Ishchuk, Olena P. and Zeljko, Tanja Vojvoda and Schifferdecker, Anna J. and Wisén, Sofia Mebrahtu and Hagström, Åsa K. and Rozpedowska, Elzbieta and Andersen, Mikael Rørdam and Hellborg, Linda and Ling, Zhihao and Sibirny, Andrei A. and Piskur, Jure}},
  issn         = {{1932-6203}},
  language     = {{eng}},
  month        = {{08}},
  number       = {{8}},
  publisher    = {{Public Library of Science (PLoS)}},
  series       = {{PLoS ONE}},
  title        = {{Novel centromeric loci of the wine and beer yeast dekkera bruxellensis CEN1 and CEN2}},
  url          = {{http://dx.doi.org/10.1371/journal.pone.0161741}},
  doi          = {{10.1371/journal.pone.0161741}},
  volume       = {{11}},
  year         = {{2016}},
}