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Journal of Bacteriology, December 2009, p. 7323-7332, Vol. 191, No. 23
0021-9193/09/$08.00+0     doi:10.1128/JB.01042-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Identification of a Stress-Induced Factor of Corynebacterineae That Is Involved in the Regulation of the Outer Membrane Lipid Composition{triangledown}

Xavier Meniche,1,2,4,{dagger} Cécile Labarre,3,{dagger} Célia de Sousa-d'Auria,3 Emilie Huc,1,2 Françoise Laval,1,2 Marielle Tropis,1,2 Nicolas Bayan,4 Damien Portevin,1,2 Christophe Guilhot,1,2 Mamadou Daffé,1,2* and Christine Houssin3*

Centre National de la Recherche Scientifique (CNRS), Institut de Pharmacologie et de Biologie Structurale (IPBS), Département Mécanismes Moléculaires des Infections Mycobactériennes, 205 Route de Narbonne, F-31077 Toulouse Cedex 04, France,1 Université de Toulouse (Toulouse III), 118 Route de Narbonne, F-31062 Toulouse, France,2 Université Paris Sud-11, CNRS UMR 8621, Institut de Génétique et Microbiologie, Bâtiment 360, F-91405 Orsay, France,3 Université Paris Sud-11, CNRS UMR8619, Institut de Biochimie et Biophysique Moléculaire et Cellulaire, F-91405 Orsay, France4

Received 7 August 2009/ Accepted 23 September 2009

Corynebacterineae are gram-positive bacteria that possess a true outer membrane composed of mycolic acids and other lipids. Little is known concerning the modulation of mycolic acid composition and content in response to changes in the bacterial environment, especially temperature variations. To address this question, we investigated the function of the Rv3802c gene, a gene conserved in Corynebacterineae and located within a gene cluster involved in mycolic acid biosynthesis. We showed that the Rv3802 ortholog is essential in Mycobacterium smegmatis, while its Corynebacterium glutamicum ortholog, NCgl2775, is not. We provided evidence that the NCgl2775 gene is transcriptionally induced under heat stress conditions, and while the corresponding protein has no detectable activity under normal growth conditions, the increase in its expression triggers an increase in mycolic acid biosynthesis concomitant with a decrease in phospholipid content. We demonstrated that these lipid modifications are part of a larger outer membrane remodeling that occurs in response to exposure to a moderately elevated temperature (42°C). In addition to showing an increase in the ratio of saturated corynomycolates to unsaturated corynomycolates, our results strongly suggested that the balance between mycolic acids and phospholipids is modified inside the outer membrane following a heat challenge. Furthermore, we showed that these lipid modifications help the bacteria to protect against heat damage. The NCgl2775 protein and its orthologs thus appear to be a protein family that plays a role in the regulation of the outer membrane lipid composition of Corynebacterineae under stress conditions. We therefore propose to name this protein family the envelope lipids regulation factor (ElrF) family.


* Corresponding author. Mailing address for Christine Houssin: Université Paris Sud-11, CNRS UMR 8621, Institut de Génétique et Microbiologie, Bâtiment 360, F-91405 Orsay, France. Phone: 33 1 69 15 69 20. Fax: 33 1 69 15 63 34. E-mail: christine.houssin{at}igmors.u-psud.fr. Mailing address for Mamadou Daffé: Centre National de la Recherche Scientifique (CNRS), Institut de Pharmacologie et de Biologie Structurale (IPBS), Département Mécanismes Moléculaires des Infections Mycobactériennes, 205 Route de Narbonne, F-31077 Toulouse Cedex 04, France. Phone: 33 5 61 175 569. Fax: 33 561 175 580. E-mail: mamadou.daffe{at}ipbs.fr

{triangledown} Published ahead of print on 2 October 2009.

{dagger} These authors contributed equally to the present work.


Journal of Bacteriology, December 2009, p. 7323-7332, Vol. 191, No. 23
0021-9193/09/$08.00+0     doi:10.1128/JB.01042-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.