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Journal of Bacteriology, July 2008, p. 4903-4911, Vol. 190, No. 14
0021-9193/08/$08.00+0     doi:10.1128/JB.00447-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Impact of Aeration and Heme-Activated Respiration on Lactococcus lactis Gene Expression: Identification of a Heme-Responsive Operon ^,

Martin Bastian Pedersen,^1* Christel Garrigues,¹ Karine Tuphile,⁴ Célia Brun,⁴ Karin Vido,⁴ Mads Bennedsen,³ Henrik Møllgaard,² Philippe Gaudu,⁴ and Alexandra Gruss^4*

Department of Physiology,¹ Department of Fermentation Technology,² Department of Identification, Chr. Hansen A/S, DK-2970 Hørsholm, Denmark,³ Unité Bactéries Lactiques et Pathogènes Opportunistes, INRA UR888, Jouy en Josas, 78352, France⁴

Received 1 April 2008/ Accepted 6 May 2008

Lactococcus lactis is a widely used food bacterium mainly characterized for its fermentation metabolism. However, this species undergoes a metabolic shift to respiration when heme is added to an aerobic medium. Respiration results in markedly improved biomass and survival compared to fermentation. Whole-genome microarrays were used to assess changes in L. lactis expression under aerobic and respiratory conditions compared to static growth, i.e., nonaerated. We observed the following. (i) Stress response genes were affected mainly by aerobic fermentation. This result underscores the differences between aerobic fermentation and respiration environments and confirms that respiration growth alleviates oxidative stress. (ii) Functions essential for respiratory metabolism, e.g., genes encoding cytochrome bd oxidase, menaquinone biosynthesis, and heme uptake, are similarly expressed under the three conditions. This indicates that cells are prepared for respiration once O₂ and heme become available. (iii) Expression of only 11 genes distinguishes respiration from both aerobic and static fermentation cultures. Among them, the genes comprising the putative ygfCBA operon are strongly induced by heme regardless of respiration, thus identifying the first heme-responsive operon in lactococci. We give experimental evidence that the ygfCBA genes are involved in heme homeostasis.

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* Corresponding authors. Mailing address for M. B. Pedersen: Department of Physiology, Chr. Hansen A/S, DK-2970 Hørsholm, Denmark. Phone: 45 45748479. Fax: 45 45748816. E-mail: dkmbp{at}chr-hansen.com. Mailing address for A. Gruss: Unité Bactéries Lactiques et Pathogènes Opportunistes, INRA UR888, Jouy en Josas 78352, France. Phone: 33(1) 34652168. Fax: 33(1) 34652065. E-mail: alexandra.gruss{at}jouy.inra.fr.

Published ahead of print on 16 May 2008.

Supplemental material for this article may be found at http://jb.asm.org/.

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Journal of Bacteriology, July 2008, p. 4903-4911, Vol. 190, No. 14
0021-9193/08/$08.00+0     doi:10.1128/JB.00447-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

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