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Science 326 (5957): 1268-1271

Copyright © 2009 by the American Association for the Advancement of Science

Transcriptome Complexity in a Genome-Reduced Bacterium

Marc Güell,1 Vera van Noort,2 Eva Yus,1 Wei-Hua Chen,2 Justine Leigh-Bell,1 Konstantinos Michalodimitrakis,1 Takuji Yamada,2 Manimozhiyan Arumugam,2 Tobias Doerks,2 Sebastian Kühner,2 Michaela Rode,2 Mikita Suyama,2,* Sabine Schmidt,2 Anne-Claude Gavin,2 Peer Bork,2,{dagger} Luis Serrano1,3,{dagger}

Abstract: To study basic principles of transcriptome organization in bacteria, we analyzed one of the smallest self-replicating organisms, Mycoplasma pneumoniae. We combined strand-specific tiling arrays, complemented by transcriptome sequencing, with more than 252 spotted arrays. We detected 117 previously undescribed, mostly noncoding transcripts, 89 of them in antisense configuration to known genes. We identified 341 operons, of which 139 are polycistronic; almost half of the latter show decaying expression in a staircase-like manner. Under various conditions, operons could be divided into 447 smaller transcriptional units, resulting in many alternative transcripts. Frequent antisense transcripts, alternative transcripts, and multiple regulators per gene imply a highly dynamic transcriptome, more similar to that of eukaryotes than previously thought.

1 Centre for Genomic Regulation (CRG), Universitat Pompeu Fabra, Barcelona, Spain.
2 European Molecular Biology Laboratory (EMBL), Heidelberg, Germany.
3 Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.

* Present address: Center for Genomic Medicine, Graduate School of Medicine, University of Kyoto, Kyoto, Japan.

{dagger}To whom correspondence should be addressed. E-mail: bork{at}embl.de (P.B.); luis.serrano{at}crg.es (L.S.)


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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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