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Horizontal gene transfer promoted evolution of the ability to propagate under anaerobic conditions in yeasts

Gojković, Z ; Knecht, W LU ; Zameitat, E ; Warneboldt, J ; Coutelis, J-B ; Pynyaha, Y ; Neuveglise, C ; Møller, K ; Löffler, M and Piskur, J LU (2004) In Molecular Genetics and Genomics 271(4). p.387-393
Abstract

The ability to propagate under anaerobic conditions is an essential and unique trait of brewer's or baker's yeast ( Saccharomyces cervisiae). To understand the evolution of facultative anaerobiosis we studied the dependence of de novo pyrimidine biosynthesis, more precisely the fourth enzymic activity catalysed by dihydroorotate dehydrogenase (DHODase), on the enzymes of the respiratory chain in several yeast species. While the majority of yeasts possess a mitochondrial DHODase, Saccharomyces cerevisiae has a cytoplasmatic enzyme, whose activity is independent of the presence of oxygen. From the phylogenetic point of view, this enzyme is closely related to a bacterial DHODase from Lactococcus lactis. Here we show that S. kluyveri, which... (More)

The ability to propagate under anaerobic conditions is an essential and unique trait of brewer's or baker's yeast ( Saccharomyces cervisiae). To understand the evolution of facultative anaerobiosis we studied the dependence of de novo pyrimidine biosynthesis, more precisely the fourth enzymic activity catalysed by dihydroorotate dehydrogenase (DHODase), on the enzymes of the respiratory chain in several yeast species. While the majority of yeasts possess a mitochondrial DHODase, Saccharomyces cerevisiae has a cytoplasmatic enzyme, whose activity is independent of the presence of oxygen. From the phylogenetic point of view, this enzyme is closely related to a bacterial DHODase from Lactococcus lactis. Here we show that S. kluyveri, which separated from the S. cerevisiae lineage more than 100 million years ago, represents an evolutionary intermediate, having both cytoplasmic and mitochondrial DHODases. We show that these two S. kluyveri enzymes, and their coding genes, differ in their dependence on the presence of oxygen. Only the cytoplasmic DHODase promotes growth in the absence of oxygen. Apparently a Saccharomyces yeast progenitor which had a eukaryotic-like mitochondrial DHODase acquired a bacterial gene for DHODase, which subsequently allowed cell growth gradually to become independent of oxygen.

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author
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publishing date
type
Contribution to journal
publication status
published
subject
keywords
Anaerobiosis, Biological Evolution, Cell Division, Cytoplasm/enzymology, DNA, Fungal/genetics, Electron Transport, Gene Transfer, Horizontal, Mitochondria/enzymology, Oxidoreductases Acting on CH-CH Group Donors/metabolism, Oxygen/metabolism, Phylogeny, Pyrimidines/biosynthesis, Saccharomyces cerevisiae/enzymology, Subcellular Fractions/enzymology
in
Molecular Genetics and Genomics
volume
271
issue
4
pages
387 - 393
publisher
Springer
external identifiers
  • scopus:3042677643
  • pmid:15014982
ISSN
1617-4615
DOI
10.1007/s00438-004-0995-7
language
English
LU publication?
no
id
96602576-4933-4636-bbf1-f5eb594ebd4f (old id 740192)
date added to LUP
2016-04-01 12:12:37
date last changed
2022-03-28 21:45:54
@article{96602576-4933-4636-bbf1-f5eb594ebd4f,
  abstract     = {{<p>The ability to propagate under anaerobic conditions is an essential and unique trait of brewer's or baker's yeast ( Saccharomyces cervisiae). To understand the evolution of facultative anaerobiosis we studied the dependence of de novo pyrimidine biosynthesis, more precisely the fourth enzymic activity catalysed by dihydroorotate dehydrogenase (DHODase), on the enzymes of the respiratory chain in several yeast species. While the majority of yeasts possess a mitochondrial DHODase, Saccharomyces cerevisiae has a cytoplasmatic enzyme, whose activity is independent of the presence of oxygen. From the phylogenetic point of view, this enzyme is closely related to a bacterial DHODase from Lactococcus lactis. Here we show that S. kluyveri, which separated from the S. cerevisiae lineage more than 100 million years ago, represents an evolutionary intermediate, having both cytoplasmic and mitochondrial DHODases. We show that these two S. kluyveri enzymes, and their coding genes, differ in their dependence on the presence of oxygen. Only the cytoplasmic DHODase promotes growth in the absence of oxygen. Apparently a Saccharomyces yeast progenitor which had a eukaryotic-like mitochondrial DHODase acquired a bacterial gene for DHODase, which subsequently allowed cell growth gradually to become independent of oxygen.</p>}},
  author       = {{Gojković, Z and Knecht, W and Zameitat, E and Warneboldt, J and Coutelis, J-B and Pynyaha, Y and Neuveglise, C and Møller, K and Löffler, M and Piskur, J}},
  issn         = {{1617-4615}},
  keywords     = {{Anaerobiosis; Biological Evolution; Cell Division; Cytoplasm/enzymology; DNA, Fungal/genetics; Electron Transport; Gene Transfer, Horizontal; Mitochondria/enzymology; Oxidoreductases Acting on CH-CH Group Donors/metabolism; Oxygen/metabolism; Phylogeny; Pyrimidines/biosynthesis; Saccharomyces cerevisiae/enzymology; Subcellular Fractions/enzymology}},
  language     = {{eng}},
  number       = {{4}},
  pages        = {{387--393}},
  publisher    = {{Springer}},
  series       = {{Molecular Genetics and Genomics}},
  title        = {{Horizontal gene transfer promoted evolution of the ability to propagate under anaerobic conditions in yeasts}},
  url          = {{http://dx.doi.org/10.1007/s00438-004-0995-7}},
  doi          = {{10.1007/s00438-004-0995-7}},
  volume       = {{271}},
  year         = {{2004}},
}