Evidence for the recent origin of a bacterial protein-coding, overlapping orphan gene by evolutionary overprinting. (December 2015)

• Record Type: Journal Article
• Authors: Fellner, Lea; Simon, Svenja; Scherling, Christian; Witting, Michael; Schober, Steffen; Polte, Christine; Schmitt-Kopplin, Philippe; Keim, Daniel; Scherer, Siegfried; Neuhaus, Klaus
• Is Part Of: BMC evolutionary biology. Volume 15(2015)Supplement 1
• Page Start: 1
• Page End: 14
• Publication Date: 2015-12
• Subjects: Overprinting -- Overlapping gene -- de novo evolution -- Coding reserve -- Orphan -- EHEC -- nog1/citC; Evolution (Biology) -- Periodicals; 576.805
• DOI: 10.1186/s12862-015-0558-z
• Languages: English
• ISSNs: 1471-2148

Abstract

Abstract 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 evolvede novo, i.e., formerly non-coding open reading frames within functional genes become expressed. Only three cases have been described forEscherichia 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 ofcitC in enterohemorrhagicE. coli . This gene is designated novel overlapping gene, nog1 . The promoter region fused togfp 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 incitC . 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 genenog1 arose by overprinting afterEscherichia/Shigella separated from the other γ-proteobacteria. Conclusions Sincenog1 is of recent origin, non-essential, short, weakly expressed and only marginally involved inE. 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 enterohemorrhagicE. 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.