This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Duwat, P.
Right arrow Articles by Gruss, A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Duwat, P.
Right arrow Articles by Gruss, A.

 Previous Article  |  Next Article 

Journal of Bacteriology, August 2001, p. 4509-4516, Vol. 183, No. 15
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.15.4509-4516.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Respiration Capacity of the Fermenting Bacterium Lactococcus lactis and Its Positive Effects on Growth and Survival†

Patrick Duwat,1 Sophie Sourice,1 Bénédicte Cesselin,1 Gilles Lamberet,1 Karin Vido,1 Philippe Gaudu,1 Yves Le Loir,1 Florent Violet,1 Pascal Loubière,2 and Alexandra Gruss1,*

Génétique Appliquée-URLGA, Institut National de la Recherche Agronomique, 78352 Jouy en Josas,1 and Centre de Bioingénierie Gilbert Durand, Institut National des Sciences Appliquées, Complexe Scientifique de Rangueil, F-31077 Toulouse Cedex 4,2 France

Received 12 February 2001/Accepted 2 May 2001

Oxygen is a major determinant of both survival and mortality of aerobic organisms. For the facultative anaerobe Lactococcus lactis, oxygen has negative effects on both growth and survival. We show here that oxygen can be beneficial to L. lactis if heme is present during aerated growth. The growth period is extended and long-term survival is markedly improved compared to results obtained under the usual fermentation conditions. We considered that improved growth and survival could be due to the capacity of L. lactis to undergo respiration. To test this idea, we confirmed that the metabolic behavior of lactococci in the presence of oxygen and hemin is consistent with respiration and is most pronounced late in growth. We then used a genetic approach to show the following. (i) The cydA gene, encoding cytochrome d oxidase, is required for respiration and plays a direct role in oxygen utilization. cydA expression is induced late in growth under respiration conditions. (ii) The hemZ gene, encoding ferrochelatase, which converts protoporphyrin IX to heme, is needed for respiration if the precursor, rather than the final heme product, is present in the medium. Surprisingly, survival improved by respiration is observed in a superoxide dismutase-deficient strain, a result which emphasizes the physiological differences between fermenting and respiring lactococci. These studies confirm respiratory metabolism in L. lactis and suggest that this organism may be better adapted to respiration than to traditional fermentative metabolism.

* Corresponding author. Mailing address: Génétique Appliquée-URLGA, Institut National de la Recherche Agronomique, Domaine de Vilvert, 78352 Jouy en Josas, France. Phone: 33-1 34 65 21 68. Fax: 33-1 34 65 20 65. E-mail: gruss{at}biotec.jouy.inra.fr.

dagger This paper is dedicated to Patrick Duwat (died 5 January 2000), who was a driving force of this work.

Journal of Bacteriology, August 2001, p. 4509-4516, Vol. 183, No. 15
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.15.4509-4516.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Mifune, J., Grage, K., Rehm, B. H. A. (2009). Production of Functionalized Biopolyester Granules by Recombinant Lactococcus lactis. Appl. Environ. Microbiol. 75: 4668-4675 [Abstract] [Full Text]  
  • Cesselin, B., Ali, D., Gratadoux, J.-J., Gaudu, P., Duwat, P., Gruss, A., El Karoui, M. (2009). Inactivation of the Lactococcus lactis high-affinity phosphate transporter confers oxygen and thiol resistance and alters metal homeostasis. Microbiology 155: 2274-2281 [Abstract] [Full Text]  
  • Brooijmans, R. J. W., de Vos, W. M., Hugenholtz, J. (2009). Lactobacillus plantarum WCFS1 Electron Transport Chains. Appl. Environ. Microbiol. 75: 3580-3585 [Abstract] [Full Text]  
  • Lo, R., Turner, M. S., Barry, D. G., Sreekumar, R., Walsh, T. P., Giffard, P. M. (2009). Cystathionine {gamma}-Lyase Is a Component of Cystine-Mediated Oxidative Defense in Lactobacillus reuteri BR11. J. Bacteriol. 191: 1827-1837 [Abstract] [Full Text]  
  • Pedersen, M. B., Garrigues, C., Tuphile, K., Brun, C., Vido, K., Bennedsen, M., Mollgaard, H., Gaudu, P., Gruss, A. (2008). Impact of Aeration and Heme-Activated Respiration on Lactococcus lactis Gene Expression: Identification of a Heme-Responsive Operon. J. Bacteriol. 190: 4903-4911 [Abstract] [Full Text]  
  • Turner, M. S., Tan, Y. P., Giffard, P. M. (2007). Inactivation of an Iron Transporter in Lactococcus lactis Results in Resistance to Tellurite and Oxidative Stress. Appl. Environ. Microbiol. 73: 6144-6149 [Abstract] [Full Text]  
  • Brooijmans, R. J. W., Poolman, B., Schuurman-Wolters, G. K., de Vos, W. M., Hugenholtz, J. (2007). Generation of a Membrane Potential by Lactococcus lactis through Aerobic Electron Transport. J. Bacteriol. 189: 5203-5209 [Abstract] [Full Text]  
  • Wegmann, U., O'Connell-Motherway, M., Zomer, A., Buist, G., Shearman, C., Canchaya, C., Ventura, M., Goesmann, A., Gasson, M. J., Kuipers, O. P., van Sinderen, D., Kok, J. (2007). Complete Genome Sequence of the Prototype Lactic Acid Bacterium Lactococcus lactis subsp. cremoris MG1363. J. Bacteriol. 189: 3256-3270 [Abstract] [Full Text]  
  • Rochat, T., Miyoshi, A., Gratadoux, J. J., Duwat, P., Sourice, S., Azevedo, V., Langella, P. (2005). High-level resistance to oxidative stress in Lactococcus lactis conferred by Bacillus subtilis catalase KatE. Microbiology 151: 3011-3018 [Abstract] [Full Text]  
  • Vido, K., Diemer, H., Van Dorsselaer, A., Leize, E., Juillard, V., Gruss, A., Gaudu, P. (2005). Roles of Thioredoxin Reductase during the Aerobic Life of Lactococcus lactis. J. Bacteriol. 187: 601-610 [Abstract] [Full Text]  
  • Goffin, P., Lorquet, F., Kleerebezem, M., Hols, P. (2004). Major Role of NAD-Dependent Lactate Dehydrogenases in Aerobic Lactate Utilization in Lactobacillus plantarum during Early Stationary Phase. J. Bacteriol. 186: 6661-6666 [Abstract] [Full Text]  
  • Vido, K., le Bars, D., Mistou, M.-Y., Anglade, P., Gruss, A., Gaudu, P. (2004). Proteome Analyses of Heme-Dependent Respiration in Lactococcus lactis: Involvement of the Proteolytic System. J. Bacteriol. 186: 1648-1657 [Abstract] [Full Text]  
  • Sybesma, W., Starrenburg, M., Tijsseling, L., Hoefnagel, M. H. N., Hugenholtz, J. (2003). Effects of Cultivation Conditions on Folate Production by Lactic Acid Bacteria. Appl. Environ. Microbiol. 69: 4542-4548 [Abstract] [Full Text]  
  • Bates, C. S., Montanez, G. E., Woods, C. R., Vincent, R. M., Eichenbaum, Z. (2003). Identification and Characterization of a Streptococcus pyogenes Operon Involved in Binding of Hemoproteins and Acquisition of Iron. Infect. Immun. 71: 1042-1055 [Abstract] [Full Text]  
  • Galagan, J. E., Nusbaum, C., Roy, A., Endrizzi, M. G., Macdonald, P., FitzHugh, W., Calvo, S., Engels, R., Smirnov, S., Atnoor, D., Brown, A., Allen, N., Naylor, J., Stange-Thomann, N., DeArellano, K., Johnson, R., Linton, L., McEwan, P., McKernan, K., Talamas, J., Tirrell, A., Ye, W., Zimmer, A., Barber, R. D., Cann, I., Graham, D. E., Grahame, D. A., Guss, A. M., Hedderich, R., Ingram-Smith, C., Kuettner, H. C., Krzycki, J. A., Leigh, J. A., Li, W., Liu, J., Mukhopadhyay, B., Reeve, J. N., Smith, K., Springer, T. A., Umayam, L. A., White, O., White, R. H., de Macario, E. C., Ferry, J. G., Jarrell, K. F., Jing, H., Macario, A. J.L., Paulsen, I., Pritchett, M., Sowers, K. R., Swanson, R. V., Zinder, S. H., Lander, E., Metcalf, W. W., Birren, B. (2002). The Genome of M. acetivorans Reveals Extensive Metabolic and Physiological Diversity. Genome Res 12: 532-542 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»