Evidence for the recent origin of a bacterial protein-coding, overlapping orphan gene by evolutionary overprinting

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2015
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Fellner, Lea
Scherling, Christian
Witting, Michael
Schober, Steffen
Polte, Christine
Schmitt-Kopplin, Philippe
Scherer, Siegfried
Neuhaus, Klaus
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BMC Evolutionary Biology. 2015, 15, 283. eISSN 1471-2148. Available under: doi: 10.1186/s12862-015-0558-z
Zusammenfassung

Background
Gene duplication is believed to be the classical way to form novel genes, but overprinting may be an important alternative. Overprinting allows entirely novel proteins to evolve de novo, i.e., formerly non-coding open reading frames within functional genes become expressed. Only three cases have been described for Escherichia coli. Here, a fourth example is presented.

Results
RNA sequencing revealed an open reading frame weakly transcribed in cow dung, coding for 101 residues and embedded completely in the −2 reading frame of citC in enterohemorrhagic E. coli. This gene is designated novel overlapping gene, nog1. The promoter region fused to gfp exhibits specific activities and 5’ rapid amplification of cDNA ends indicated the transcriptional start 40-bp upstream of the start codon. nog1 was strand-specifically arrested in translation by a nonsense mutation silent in citC. This Nog1-mutant showed a phenotype in competitive growth against wild type in the presence of MgCl2. Small differences in metabolite concentrations were also found. Bioinformatic analyses propose Nog1 to be inner membrane-bound and to possess at least one membrane-spanning domain. A phylogenetic analysis suggests that the orphan gene nog1 arose by overprinting after Escherichia/Shigella separated from the other γ-proteobacteria.

Conclusions
Since nog1 is of recent origin, non-essential, short, weakly expressed and only marginally involved in E. coli’s central metabolism, we propose that this gene is in an initial stage of evolution. While we present specific experimental evidence for the existence of a fourth overlapping gene in enterohemorrhagic E. coli, we believe that this may be an initial finding only and overlapping genes in bacteria may be more common than is currently assumed by microbiologists.

Zusammenfassung in einer weiteren Sprache
Fachgebiet (DDC)
570 Biowissenschaften, Biologie
Schlagwörter
Overprinting, Overlapping gene, de novo evolution, Coding reserve, Orphan, EHEC, nog1/citC
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ISO 690FELLNER, Lea, Svenja SIMON, Christian SCHERLING, Michael WITTING, Steffen SCHOBER, Christine POLTE, Philippe SCHMITT-KOPPLIN, Daniel A. KEIM, Siegfried SCHERER, Klaus NEUHAUS, 2015. Evidence for the recent origin of a bacterial protein-coding, overlapping orphan gene by evolutionary overprinting. In: BMC Evolutionary Biology. 2015, 15, 283. eISSN 1471-2148. Available under: doi: 10.1186/s12862-015-0558-z
BibTex
@article{Fellner2015Evide-33391,
  year={2015},
  doi={10.1186/s12862-015-0558-z},
  title={Evidence for the recent origin of a bacterial protein-coding, overlapping orphan gene by evolutionary overprinting},
  volume={15},
  journal={BMC Evolutionary Biology},
  author={Fellner, Lea and Simon, Svenja and Scherling, Christian and Witting, Michael and Schober, Steffen and Polte, Christine and Schmitt-Kopplin, Philippe and Keim, Daniel A. and Scherer, Siegfried and Neuhaus, Klaus},
  note={Article Number: 283}
}
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