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PNAS 108 (18): 7565-7570

Copyright © 2011 by the National Academy of Sciences.


BIOLOGICAL SCIENCES / MICROBIOLOGY

Light-dependent gene regulation by a coenzyme B12-based photoreceptor

Juan Manuel Ortiz-Guerreroa,1, María Carmen Polancoa,1, Francisco J. Murilloa, S. Padmanabhanb,2, and Montserrat Elías-Arnanza,2

aDepartment of Genetics and Microbiology, Area of Genetics (Unidad Asociada al Instituto de Química Física–Consejo Superior de Investigaciones Científicas), Faculty of Biology, Universidad de Murcia, Murcia 30100, Spain; and bInstituto de Química Física "Rocasolano," Consejo Superior de Investigaciones Científicas, 28006 Madrid, Spain

Edited by Margarita Salas, Consejo Superior de Investigaciones Científicas, Madrid, Spain, and approved March 24, 2011 (received for review December 17, 2010)

Abstract: Cobalamin (B12) typically functions as an enzyme cofactor but can also regulate gene expression via RNA-based riboswitches. B12-directed gene regulatory mechanisms via protein factors have, however, remained elusive. Recently, we reported down-regulation of a light-inducible promoter in the bacterium Myxococcus xanthus by two paralogous transcriptional repressors, of which one, CarH, but not the other, CarA, absolutely requires B12 for activity even though both have a canonical B12-binding motif. Unanswered were what underlies this striking difference, what is the specific cobalamin used, and how it acts. Here, we show that coenzyme B12 (5'-deoxyadenosylcobalamin, AdoB12), specifically dictates CarH function in the dark and on exposure to light. In the dark, AdoB12-binding to the autonomous domain containing the B12-binding motif foments repressor oligomerization, enhances operator binding, and blocks transcription. Light, at various wavelengths at which AdoB12 absorbs, dismantles active repressor oligomers by photolysing the bound AdoB12 and weakens repressor–operator binding to allow transcription. By contrast, AdoB12 alters neither CarA oligomerization nor operator binding, thus accounting for its B12-independent activity. Our findings unveil a functional facet of AdoB12 whereby it serves as the chromophore of a unique photoreceptor protein class acting in light-dependent gene regulation. The prevalence of similar proteins of unknown function in microbial genomes suggests that this distinct B12-based molecular mechanism for photoregulation may be widespread in bacteria.

Key Words: carotenogenesis • Thermus thermophilus • antirepressor • MerR • TtCarH


Author contributions: S.P. and M.E.-A. designed research; J.M.O.-G., M.C.P., S.P., and M.E.-A. performed research; J.M.O.-G., M.C.P., F.J.M., S.P., and M.E.-A. analyzed data; and S.P. and M.E.-A. wrote the paper.

1J.M.O.-G. and M.C.P. contributed equally to this work.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1018972108/-/DCSupplemental.

2To whom correspondence may be addressed. E-mail: padhu{at}iqfr.csic.es or melias{at}um.es.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Two Systems for Conditional Gene Expression in Myxococcus xanthus Inducible by Isopropyl-{beta}-D-Thiogalactopyranoside or Vanillate.
A. A. Iniesta, F. Garcia-Heras, J. Abellon-Ruiz, A. Gallego-Garcia, and M. Elias-Arnanz (2012)
J. Bacteriol. 194, 5875-5885
   Abstract »    Full Text »    PDF »
CarF Mediates Signaling by Singlet Oxygen, Generated via Photoexcited Protoporphyrin IX, in Myxococcus xanthus Light-Induced Carotenogenesis.
M. Galbis-Martinez, S. Padmanabhan, F. J. Murillo, and M. Elias-Arnanz (2012)
J. Bacteriol. 194, 1427-1436
   Abstract »    Full Text »    PDF »

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