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Compensatory gene amplification restores fitness after inter-species gene replacements

Lind, Peter A.; Tobin, Christina; Berg, Otto G.; Kurland, Charles LU and Andersson, Dan I. (2010) In Molecular Microbiology 75(5). p.1078-1089
Abstract
P>Genes introduced by gene replacements and other types of horizontal gene transfer (HGT) represent a significant presence in many archaeal and eubacterial genomes. Most alien genes are likely to be neutral or deleterious upon arrival and their long-term persistence may require a mechanism that improves their selective contribution. To examine the fate of inter-species gene replacements, we exchanged three native S. typhimurium genes encoding ribosomal proteins with orthologues from various other microbes. The results show that replacement of each of these three genes reduces fitness to such an extent that it would provide an effective barrier against inter-species gene replacements in eubacterial populations. However, these fitness... (More)
P>Genes introduced by gene replacements and other types of horizontal gene transfer (HGT) represent a significant presence in many archaeal and eubacterial genomes. Most alien genes are likely to be neutral or deleterious upon arrival and their long-term persistence may require a mechanism that improves their selective contribution. To examine the fate of inter-species gene replacements, we exchanged three native S. typhimurium genes encoding ribosomal proteins with orthologues from various other microbes. The results show that replacement of each of these three genes reduces fitness to such an extent that it would provide an effective barrier against inter-species gene replacements in eubacterial populations. However, these fitness defects could be partially ameliorated by gene amplification that augmented the dosage of the heterologous proteins. This suggests that suboptimal expression is a common fitness constraint for inter-species gene replacements, with fitness costs conferred by either a lower expression level of the alien protein compared with the native protein or a requirement for an increased amount of the alien protein to maintain proper function. Our findings can explain the observation that duplicated genes are over-represented among horizontally transferred genes, and suggest a potential coupling between compensatory gene amplification after HGT and the evolution of new genes. (Less)
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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
in
Molecular Microbiology
volume
75
issue
5
pages
1078 - 1089
publisher
Wiley-Blackwell
external identifiers
  • wos:000274808800004
  • scopus:77349104670
ISSN
1365-2958
DOI
10.1111/j.1365-2958.2009.07030.x
language
English
LU publication?
yes
id
a814790b-a748-46ca-b284-61cf32962127 (old id 1568073)
date added to LUP
2010-03-24 11:13:29
date last changed
2018-05-29 09:41:30
@article{a814790b-a748-46ca-b284-61cf32962127,
  abstract     = {P>Genes introduced by gene replacements and other types of horizontal gene transfer (HGT) represent a significant presence in many archaeal and eubacterial genomes. Most alien genes are likely to be neutral or deleterious upon arrival and their long-term persistence may require a mechanism that improves their selective contribution. To examine the fate of inter-species gene replacements, we exchanged three native S. typhimurium genes encoding ribosomal proteins with orthologues from various other microbes. The results show that replacement of each of these three genes reduces fitness to such an extent that it would provide an effective barrier against inter-species gene replacements in eubacterial populations. However, these fitness defects could be partially ameliorated by gene amplification that augmented the dosage of the heterologous proteins. This suggests that suboptimal expression is a common fitness constraint for inter-species gene replacements, with fitness costs conferred by either a lower expression level of the alien protein compared with the native protein or a requirement for an increased amount of the alien protein to maintain proper function. Our findings can explain the observation that duplicated genes are over-represented among horizontally transferred genes, and suggest a potential coupling between compensatory gene amplification after HGT and the evolution of new genes.},
  author       = {Lind, Peter A. and Tobin, Christina and Berg, Otto G. and Kurland, Charles and Andersson, Dan I.},
  issn         = {1365-2958},
  language     = {eng},
  number       = {5},
  pages        = {1078--1089},
  publisher    = {Wiley-Blackwell},
  series       = {Molecular Microbiology},
  title        = {Compensatory gene amplification restores fitness after inter-species gene replacements},
  url          = {http://dx.doi.org/10.1111/j.1365-2958.2009.07030.x},
  volume       = {75},
  year         = {2010},
}