Genometric analyses of the organization of circular chromosomes: a universal pressure determines the direction of ribosomal RNA genes transcription relative to chromosome replication.
Selective pressures related to gene function and chromosomal architecture are acting on genome sequences and can be revealed, for instance, by appropriate genometric methods. Cumulative nucleotide skew analyses, i.e., GC, TA, and ORF orientation skews, predict the location of the origin of DNA replication for 88 out of 100 completely sequenced bacterial chromosomes. These methods appear fully reliable for proteobacteria, Gram-positives, and spirochetes as well as for euryarchaeotes. Based on this genome architecture information, coorientation analyses reveal that in prokaryotes, ribosomal RNA (rRNA) genes encoding the small and large ribosomal subunits are all transcribed in the same direction as DNA replication; that is, they are located along the leading strand. This result offers a simple and reliable method for circumscribing the region containing the origin of the DNA replication and reveals a strong selective pressure acting on the orientation of rRNA genes similar to the weaker one acting on the orientation of ORFs. Rate of coorientation of transfer RNA (tRNA) genes with DNA replication appears to be taxon-specific. Analyzing nucleotide biases such as GC and TA skews of genes and plotting one against the other reveals a taxonomic clusterization of species. All ribosomal RNA genes are enriched in Gs and depleted in Cs, the only so far known exception being the rRNA genes of deuterostomian mitochondria. However, this exception can be explained by the fact that in the chromosome of the human mitochondrion, the model of the deuterostomian organelle genome, DNA replication, and rRNA transcription proceed in opposite directions. A general rule is deduced from prokaryotic and mitochondrial genomes: ribosomal RNA genes that are transcribed in the same direction as the DNA replication are enriched in Gs, and those transcribed in the opposite direction are depleted in Gs.
Guy
Lionel
L
Département de Microbiologie Fondamentale, Faculté de Biologie et de Médecine, Université de Lausanne, CH-1015 Lausanne, Switzerland.
Roten
Claude-Alain H
CA
D001482:Base Composition / Q000235:genetics; D019847:Chromosomes, Archaeal / Q000235:genetics*; D002876:Chromosomes, Bacterial / Q000235:genetics*; D004261:DNA Replication / Q000235:genetics; D004270:DNA, Circular / Q000235:genetics; D004272:DNA, Mitochondrial / Q000235:genetics; D030561:Databases, Nucleic Acid; D020745:Genome, Archaeal; D016680:Genome, Bacterial; D006801:Humans; D008957:Models, Genetic; D010802:Phylogeny; D012335:RNA, Ribosomal / Q000235:genetics; D018741:Replication Origin / Q000235:genetics; D014158:Transcription, Genetic / Q000235:genetics
D004270:DNA, Circular; D004272:DNA, Mitochondrial; D012335:RNA, Ribosomal