Adenine Enrichment at the Fourth CDS Residue in Bacterial Genes Is Consistent with Error Proofing for +1 Frameshifts

Beyond selection for optimal protein functioning, coding sequences (CDSs) are under selection at the RNA and DNA levels. Here, we identify a possible signature of "dual-coding," namely extensive adenine (A) enrichment at bacterial CDS fourth sites. In 99.07% of studied bacterial genomes, f...

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Published inMolecular Biology and Evolution Vol. 34; no. 12; pp. 3064 - 3080
Main Authors Abrahams, Liam, Hurst, Laurence D
Format Journal Article Web Resource
LanguageEnglish
Published United States Oxford University Press 01.12.2017
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Abstract Beyond selection for optimal protein functioning, coding sequences (CDSs) are under selection at the RNA and DNA levels. Here, we identify a possible signature of "dual-coding," namely extensive adenine (A) enrichment at bacterial CDS fourth sites. In 99.07% of studied bacterial genomes, fourth site A use is greater than expected given genomic A-starting codon use. Arguing for nucleotide level selection, A-starting serine and arginine second codons are heavily utilized when compared with their non-A starting synonyms. Several models have the ability to explain some of this trend. In part, A-enrichment likely reduces 5' mRNA stability, promoting translation initiation. However T/U, which may also reduce stability, is avoided. Further, +1 frameshifts on the initiating ATG encode a stop codon (TGA) provided A is the fourth residue, acting either as a frameshift "catch and destroy" or a frameshift stop and adjust mechanism and hence implicated in translation initiation. Consistent with both, genomes lacking TGA stop codons exhibit weaker fourth site A-enrichment. Sequences lacking a Shine-Dalgarno sequence and those without upstream leader genes, that may be more error prone during initiation, have greater utilization of A, again suggesting a role in initiation. The frameshift correction model is consistent with the notion that many genomic features are error-mitigation factors and provides the first evidence for site-specific out of frame stop codon selection. We conjecture that the NTG universal start codon may have evolved as a consequence of TGA being a stop codon and the ability of NTGA to rapidly terminate or adjust a ribosome.
AbstractList Beyond selection for optimal protein functioning, coding sequences (CDSs) are under selection at the RNA and DNA levels. Here, we identify a possible signature of “dual-coding,” namely extensive adenine ( A ) enrichment at bacterial CDS fourth sites. In 99.07% of studied bacterial genomes, fourth site A use is greater than expected given genomic A -starting codon use. Arguing for nucleotide level selection, A -starting serine and arginine second codons are heavily utilized when compared with their non- A starting synonyms. Several models have the ability to explain some of this trend. In part, A -enrichment likely reduces 5′ mRNA stability, promoting translation initiation. However T / U , which may also reduce stability, is avoided. Further, +1 frameshifts on the initiating ATG encode a stop codon (TGA) provided A is the fourth residue, acting either as a frameshift “catch and destroy” or a frameshift stop and adjust mechanism and hence implicated in translation initiation. Consistent with both, genomes lacking TGA stop codons exhibit weaker fourth site A -enrichment. Sequences lacking a Shine–Dalgarno sequence and those without upstream leader genes, that may be more error prone during initiation, have greater utilization of A , again suggesting a role in initiation. The frameshift correction model is consistent with the notion that many genomic features are error-mitigation factors and provides the first evidence for site-specific out of frame stop codon selection. We conjecture that the NTG universal start codon may have evolved as a consequence of TGA being a stop codon and the ability of NTGA to rapidly terminate or adjust a ribosome.
Beyond selection for optimal protein functioning, coding sequences (CDSs) are under selection at the RNA and DNA levels. Here, we identify a possible signature of "dual-coding," namely extensive adenine (A) enrichment at bacterial CDS fourth sites. In 99.07% of studied bacterial genomes, fourth site A use is greater than expected given genomic A-starting codon use. Arguing for nucleotide level selection, A-starting serine and arginine second codons are heavily utilized when compared with their non-A starting synonyms. Several models have the ability to explain some of this trend. In part, A-enrichment likely reduces 5' mRNA stability, promoting translation initiation. However T/U, which may also reduce stability, is avoided. Further, +1 frameshifts on the initiating ATG encode a stop codon (TGA) provided A is the fourth residue, acting either as a frameshift "catch and destroy" or a frameshift stop and adjust mechanism and hence implicated in translation initiation. Consistent with both, genomes lacking TGA stop codons exhibit weaker fourth site A-enrichment. Sequences lacking a Shine-Dalgarno sequence and those without upstream leader genes, that may be more error prone during initiation, have greater utilization of A, again suggesting a role in initiation. The frameshift correction model is consistent with the notion that many genomic features are error-mitigation factors and provides the first evidence for site-specific out of frame stop codon selection. We conjecture that the NTG universal start codon may have evolved as a consequence of TGA being a stop codon and the ability of NTGA to rapidly terminate or adjust a ribosome.
Author Hurst, Laurence D
Abrahams, Liam
AuthorAffiliation 1 Department of Biology and Biochemistry, The Milner Centre for Evolution, University of Bath, Bath, United Kingdom
AuthorAffiliation_xml – name: 1 Department of Biology and Biochemistry, The Milner Centre for Evolution, University of Bath, Bath, United Kingdom
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  givenname: Liam
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  surname: Hurst
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/28961919$$D View this record in MEDLINE/PubMed
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Issue 12
Keywords error mitigation, dual coding
translation initiation
frameshift
fourth site
Language English
License The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
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Snippet Beyond selection for optimal protein functioning, coding sequences (CDSs) are under selection at the RNA and DNA levels. Here, we identify a possible signature...
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SubjectTerms Adenine - metabolism
Bacteria - genetics
Base Sequence
Codon - metabolism
Codon, Initiator - genetics
Codon, Terminator - genetics
Discoveries
Evolution, Molecular
Frameshift Mutation - genetics
Genes, Bacterial - genetics
Genome, Bacterial - genetics
Ribosomes - metabolism
RNA Stability - genetics
RNA, Messenger - genetics
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Title Adenine Enrichment at the Fourth CDS Residue in Bacterial Genes Is Consistent with Error Proofing for +1 Frameshifts
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