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Transfer of noncoding DNA drives regulatory rewiring in bacteria

Author(s)
Oren, Yaara; Johns, Nathan I.; Kaplan Zeevi, Millie; Biran, Dvora; Ron, Eliora Z.; Corander, Jukka; Wang, Harris H.; Alm, Eric J.; Pupko, Tal; Smith, Mark Burnham; ... Show more Show less
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Abstract
Understanding the mechanisms that generate variation is a common pursuit unifying the life sciences. Bacteria represent an especially striking puzzle, because closely related strains possess radically different metabolic and ecological capabilities. Differences in protein repertoire arising from gene transfer are currently considered the primary mechanism underlying phenotypic plasticity in bacteria. Although bacterial coding plasticity has been extensively studied in previous decades, little is known about the role that regulatory plasticity plays in bacterial evolution. Here, we show that bacterial genes can rapidly shift between multiple regulatory modes by acquiring functionally divergent nonhomologous promoter regions. Through analysis of 270,000 regulatory regions across 247 genomes, we demonstrate that regulatory “switching” to nonhomologous alternatives is ubiquitous, occurring across the bacterial domain. Using comparative transcriptomics, we show that at least 16% of the expression divergence between Escherichia coli strains can be explained by this regulatory switching. Further, using an oligonucleotide regulatory library, we establish that switching affects bacterial promoter architecture. We provide evidence that regulatory switching can occur through horizontal regulatory transfer, which allows regulatory regions to move across strains, and even genera, independently from the genes they regulate. Finally, by experimentally characterizing the fitness effect of a regulatory transfer on a pathogenic E. coli strain, we demonstrate that regulatory switching elicits important phenotypic consequences. Taken together, our findings expose previously unappreciated regulatory plasticity in bacteria and provide a gateway for understanding bacterial phenotypic variation and adaptation.
Date issued
2014-11
URI
http://hdl.handle.net/1721.1/96956
Department
Massachusetts Institute of Technology. Department of Biological Engineering
Journal
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences (U.S.)
Citation
Oren, Yaara, Mark B. Smith, Nathan I. Johns, Millie Kaplan Zeevi, Dvora Biran, Eliora Z. Ron, Jukka Corander, Harris H. Wang, Eric J. Alm, and Tal Pupko. “Transfer of Noncoding DNA Drives Regulatory Rewiring in Bacteria.” Proceedings of the National Academy of Sciences 111, no. 45 (October 13, 2014): 16112–16117.
Version: Final published version
ISSN
0027-8424
1091-6490

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