TY - JOUR TI - Parallel evolution of transcriptome architecture during genome reorganization. AU - Yoon, Sung Ho AU - Reiss, David J. AU - Bare, J. Christopher AU - Tenenbaum, Dan AU - Pan, Min AU - Slagel, Joseph AU - Moritz, Robert L. AU - Lim, Sujung AU - Hackett, Murray AU - Menon, Angeli Lal AU - Adams, Michael W. W. AU - Barnebey, Adam AU - Yannone, Steven M. AU - Leigh, John A. AU - Baliga, Nitin S. T2 - Genome research AB - Assembly of genes into operons is generally viewed as an important process during the continual adaptation of microbes to changing environmental challenges. However, the genome reorganization events that drive this process are also the roots of instability for existing operons. We have determined that there exists a statistically significant trend that correlates the proportion of genes encoded in operons in archaea to their phylogenetic lineage. We have further characterized how microbes deal with operon instability by mapping and comparing transcriptome architectures of four phylogenetically diverse extremophiles that span the range of operon stabilities observed across archaeal lineages: a photoheterotrophic halophile (Halobacterium salinarum NRC-1), a hydrogenotrophic methanogen (Methanococcus maripaludis S2), an acidophilic and aerobic thermophile (Sulfolobus solfataricus P2), and an anaerobic hyperthermophile (Pyrococcus furiosus DSM 3638). We demonstrate how the evolution of transcriptional elements (promoters and terminators) generates new operons, restores the coordinated regulation of translocated, inverted, and newly acquired genes, and introduces completely novel regulation for even some of the most conserved operonic genes such as those encoding subunits of the ribosome. The inverse correlation (r=-0.92) between the proportion of operons with such internally located transcriptional elements and the fraction of conserved operons in each of the four archaea reveals an unprecedented view into varying stages of operon evolution. Importantly, our integrated analysis has revealed that organisms adapted to higher growth temperatures have lower tolerance for genome reorganization events that disrupt operon structures. DA - 2011/11//undefined PY - 2011 DO - 10.1101/gr.122218.111 VL - 21 IS - 11 SP - 1892 EP - 1904 J2 - Genome Res LA - eng SN - 1549-5469 1088-9051 KW - *Evolution, Molecular KW - *Genome, Archaeal KW - *Transcriptome KW - Adenosine Triphosphatases/genetics KW - Archaea/classification/genetics KW - Gene Expression Profiling KW - Gene Expression Regulation, Archaeal KW - Genes, Archaeal KW - Operon KW - Phylogeny KW - Promoter Regions, Genetic KW - Protein Biosynthesis/genetics KW - RNA Transport KW - Transcription, Genetic KW - Transcriptional Activation ER -