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Yeast-bacteria competition induced new metabolic traits through large-scale genomic rearrangements in Lachancea kluyveri

Zhou, Nerve LU ; Bottagisi, Samuele; Katz, Michael LU ; Schacherer, Joseph; Friedrich, Anne; Gojkovic, Zoran; Swamy, Krishna B.S.; Knecht, Wolfgang LU ; Compagno, Concetta and Piškur, Jure LU (2017) In FEMS Yeast Research 17(6).
Abstract

Large-scale chromosomal rearrangements are an important source of evolutionary novelty that may have reshaped the genomes of existing yeast species. They dramatically alter genome organization and gene expression fueling a phenotypic leap in response to environmental constraints. Although the emergence of such signatures of genetic diversity is thought to be associated with human exploitation of yeasts, less is known about the driving forces operating in natural habitats. Here we hypothesize that an ecological battlefield characteristic of every autumn when fruits ripen accounts for the genomic innovations in natural populations. We described a long-term cross-kingdom competition experiment between Lachancea kluyveri and five species of... (More)

Large-scale chromosomal rearrangements are an important source of evolutionary novelty that may have reshaped the genomes of existing yeast species. They dramatically alter genome organization and gene expression fueling a phenotypic leap in response to environmental constraints. Although the emergence of such signatures of genetic diversity is thought to be associated with human exploitation of yeasts, less is known about the driving forces operating in natural habitats. Here we hypothesize that an ecological battlefield characteristic of every autumn when fruits ripen accounts for the genomic innovations in natural populations. We described a long-term cross-kingdom competition experiment between Lachancea kluyveri and five species of bacteria. Now, we report how we further subjected the same yeast to a sixth species of bacteria, Pseudomonas fluorescens, resulting in the appearance of a fixed and stably inherited large-scale genomic rearrangement in two out of three parallel evolution lines. The 'extra-banded' karyotype, characterized by a higher fitness and an elevated fermentative capacity, conferred the emergence of new metabolic traits in most carbon sources and osmolytes. We tracked down the event to a duplication and translocation event involving a 261-kb segment. Such an experimental setup described here is an attractive method for developing industrial strains without genetic engineering strategies.

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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Experimental evolution, Genome evolution, Large-scale genomic rearrangements, Strain development, Yeast-bacteria co-evolution
in
FEMS Yeast Research
volume
17
issue
6
publisher
Elsevier
external identifiers
  • scopus:85037524388
  • wos:000412838700007
ISSN
1567-1356
DOI
10.1093/femsyr/fox060
language
English
LU publication?
yes
id
2df5e2d7-dd35-4f0a-8a78-ca6d020d0037
date added to LUP
2018-01-02 10:52:28
date last changed
2018-04-22 04:34:29
@article{2df5e2d7-dd35-4f0a-8a78-ca6d020d0037,
  abstract     = {<p>Large-scale chromosomal rearrangements are an important source of evolutionary novelty that may have reshaped the genomes of existing yeast species. They dramatically alter genome organization and gene expression fueling a phenotypic leap in response to environmental constraints. Although the emergence of such signatures of genetic diversity is thought to be associated with human exploitation of yeasts, less is known about the driving forces operating in natural habitats. Here we hypothesize that an ecological battlefield characteristic of every autumn when fruits ripen accounts for the genomic innovations in natural populations. We described a long-term cross-kingdom competition experiment between Lachancea kluyveri and five species of bacteria. Now, we report how we further subjected the same yeast to a sixth species of bacteria, Pseudomonas fluorescens, resulting in the appearance of a fixed and stably inherited large-scale genomic rearrangement in two out of three parallel evolution lines. The 'extra-banded' karyotype, characterized by a higher fitness and an elevated fermentative capacity, conferred the emergence of new metabolic traits in most carbon sources and osmolytes. We tracked down the event to a duplication and translocation event involving a 261-kb segment. Such an experimental setup described here is an attractive method for developing industrial strains without genetic engineering strategies.</p>},
  articleno    = {fox060},
  author       = {Zhou, Nerve and Bottagisi, Samuele and Katz, Michael and Schacherer, Joseph and Friedrich, Anne and Gojkovic, Zoran and Swamy, Krishna B.S. and Knecht, Wolfgang and Compagno, Concetta and Piškur, Jure},
  issn         = {1567-1356},
  keyword      = {Experimental evolution,Genome evolution,Large-scale genomic rearrangements,Strain development,Yeast-bacteria co-evolution},
  language     = {eng},
  month        = {09},
  number       = {6},
  publisher    = {Elsevier},
  series       = {FEMS Yeast Research},
  title        = {Yeast-bacteria competition induced new metabolic traits through large-scale genomic rearrangements in Lachancea kluyveri},
  url          = {http://dx.doi.org/10.1093/femsyr/fox060},
  volume       = {17},
  year         = {2017},
}