Using heme as an energy boost for lactic acid bacteria

Current Opinion in Biotechnology

Volumn 22, Issue 2, 2011, Pages 143-149

  Lechardeur, Delphine ^a   Cesselin, Bénédicte ^a   Fernandez, Annabelle ^a   Lamberet, Gilles ^a   Garrigues, Christel ^b   Pedersen, Martin ^b   Gaudu, Philippe ^a   Gruss, Alexandra ^a  

^a UMR1319 MICALIS   (France)

^b CHR HANSEN A S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ACID STRESS; AEROBIC RESPIRATION; EXOGENOUS SOURCE; FOOD FERMENTATION; LACTIC ACID BACTERIA; MENAQUINONES; NATURAL ENVIRONMENTS; STARTER CULTURES;

BACTERIOLOGY; BODY FLUIDS; INDUSTRIAL APPLICATIONS; LABORATORIES; LACTIC ACID; METABOLISM; PORPHYRINS;

PHYSIOLOGY;

BINDING PROTEIN; HEME; HEME BINDING PROTEIN; MENAQUINONE; UNCLASSIFIED DRUG;

BACTERIAL GENE; BIOMASS PRODUCTION; BIOMEDICINE; BIOSYNTHESIS; ELECTRON TRANSPORT; ENERGY CONSERVATION; ENERGY METABOLISM; ENERGY YIELD; FERMENTATION TECHNIQUE; FOOD MICROBIOTECHNOLOGY; LACTIC ACID BACTERIUM; LACTOCOCCUS LACTIS; MICROBIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW;

BACTERIA; HEME; LACTIC ACID; LACTOBACILLACEAE;

EID: 79954421871     PISSN: 09581669     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.copbio.2010.12.001     Document Type: Review

References (49)

1. Blank L.M., Koebmann B.J., Michelsen O., Nielsen L.K., Jensen P.R. Hemin reconstitutes proton extrusion in an H(+)-ATPase-negative mutant of Lactococcus lactis. J Bacteriol 2001, 183:6707-6709.
2. Brooijmans R.J., de Vos W.M., Hugenholtz J. Lactobacillus plantarum WCFS1 electron transport chains. Appl Environ Microbiol 2009, 75:3580-3585.
3. Brooijmans R.J., Poolman B., Schuurman-Wolters G.K., de Vos W.M., Hugenholtz J. Generation of a membrane potential by Lactococcus lactis through aerobic electron transport. J Bacteriol 2007, 189:5203-5209.
4. Duwat P., Sourice S., Cesselin B., Lamberet G., Vido K., Gaudu P., Le Loir Y., Violet F., Loubiere P., Gruss A. Respiration capacity of the fermenting bacterium Lactococcus lactis and its positive effects on growth and survival. J Bacteriol 2001, 183:4509-4516.
5. Gaudu P., Vido K., Cesselin B., Kulakauskas S., Tremblay J., Rezaiki L., Lamberet G., Sourice S., Duwat P., Gruss A. Respiration capacity and consequences in Lactococcus lactis. Antonie Van Leeuwenhoek 2002, 82:263-269.
6. Huycke M.M., Moore D., Joyce W., Wise P., Shepard L., Kotake Y., Gilmore M.S. Extracellular superoxide production by Enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol Microbiol 2001, 42:729-740.
7. Koebmann B., Blank L.M., Solem C., Petranovic D., Nielsen L.K., Jensen P.R. Increased biomass yield of Lactococcus lactis during energetically limited growth and respiratory conditions. Biotechnol Appl Biochem 2008, 50:25-33.
8. Pedersen M.B., Garrigues C., Tuphile K., Brun C., Vido K., Bennedsen M., Mollgaard H., Gaudu P., Gruss A. Impact of aeration and heme-activated respiration on Lactococcus lactis gene expression: identification of a heme-responsive operon. J Bacteriol 2008, 190:4903-4911.
9. Sijpesteijn A.K. Induction of cytochrome formation and stimulation of oxidative dissimilation by hemin in Streptococcus lactis and Leuconostoc mesenteroides. Antonie Van Leeuwenhoek 1970, 36:335-348.
10. Winstedt L., Frankenberg L., Hederstedt L., von Wachenfeldt C. Enterococcus faecalis V583 contains a cytochrome bd-type respiratory oxidase. J Bacteriol 2000, 182:3863-3866.
11. Yamamoto Y., Poyart C., Trieu-Cuot P., Lamberet G., Gruss A., Gaudu P. Respiration metabolism of Group B Streptococcus is activated by environmental haem and quinone and contributes to virulence. Mol Microbiol 2005, 56:525-534.
12. Yamamoto Y., Poyart C., Trieu-Cuot P., Lamberet G., Gruss A., Gaudu P. Roles of environmental heme, and menaquinone, in Streptococcus agalactiae. Biometals 2006, 19:205-210.
13. Duwat P, Gruss A, Le Loir Y, Gaudu P: Lactic acid bacteria transformed to be provided with respiratory metabolism. US Patent 1999.
14. Duwat P, Sourice S, Gruss A: Process for preparing starter cultures of lactic acid bacteria. US Patent 1998.
15. Gennis R.B., Stewart V. Respiration. Escherichia coli and Salmonella 1996, 217-261. ASM press. F.C. Neidhardt (Ed.).
16. Brooijmans R., Smit B., Santos F., van Riel J., de Vos W.M., Hugenholtz J. Heme and menaquinone induced electron transport in lactic acid bacteria. Microb Cell Fact 2009, 8:28.
17. Rezaiki L., Lamberet G., Derre A., Gruss A., Gaudu P. Lactococcus lactis produces short-chain quinones that cross-feed Group B Streptococcus to activate respiration growth. Mol Microbiol 2008, 67:947-957.
18. Vido K., Le Bars D., Mistou M.Y., Anglade P., Gruss A., Gaudu P. Proteome analyses of heme-dependent respiration in Lactococcus lactis: involvement of the proteolytic system. J Bacteriol 2004, 186:1648-1657.
19. Garrigues C., Loubiere P., Lindley N.D., Cocaign-Bousquet M. Control of the shift from homolactic acid to mixed-acid fermentation in Lactococcus lactis: predominant role of the NADH/NAD+ ratio. J Bacteriol 1997, 179:5282-5287.
20. Lopez de Felipe F., Kleerebezem M., de Vos W.M., Hugenholtz J. Cofactor engineering: a novel approach to metabolic engineering in Lactococcus lactis by controlled expression of NADH oxidase. J Bacteriol 1998, 180:3804-3808.
21. Rezaiki L., Cesselin B., Yamamoto Y., Vido K., van West E., Gaudu P., Gruss A. Respiration metabolism reduces oxidative and acid stress to improve long-term survival of Lactococcus lactis. Mol Microbiol 2004, 53:1331-1342.
22. Wandersman C., Delepelaire P. Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 2004, 58:611-647.
23. Chang K.P., Chang C.S., Sassa S. Heme biosynthesis in bacterium-protozoon symbioses: enzymic defects in host hemoflagellates and complemental role of their intracellular symbiotes. Proc Natl Acad Sci USA 1975, 72:2979-2983.
24. Rao A.U., Carta L.K., Lesuisse E., Hamza I. Lack of heme synthesis in a free-living eukaryote. Proc Natl Acad Sci USA 2005, 102:4270-4275.
25. Warren W.C., Hillier L.W., Marshall Graves J.A., Birney E., Ponting C.P., Grutzner F., Belov K., Miller W., Clarke L., Chinwalla A.T., et al. Genome analysis of the platypus reveals unique signatures of evolution. Nature 2008, 453:175-183.
26. Kumar S., Bandyopadhyay U. Free heme toxicity and its detoxification systems in human. Toxicol Lett 2005, 157:175-188.
27. Lechardeur D., Fernandez A., Robert B., Gaudu P., Trieu-Cuot P., Lamberet G., Gruss A. The 2-Cys peroxiredoxin alkyl hydroperoxide reductase c binds heme and participates in its intracellular availability in Streptococcus agalactiae. J Biol Chem 2010, 285:16032-16041.
28. Poole L.B. Bacterial defenses against oxidants: mechanistic features of cysteine-based peroxidases and their flavoprotein reductases. Arch Biochem Biophys 2005, 433:240-254.
29. Chelikani P., Fita I., Loewen P.C. Diversity of structures and properties among catalases. Cell Mol Life Sci 2004, 61:192-208.
30. Furuyama K., Kaneko K., Vargas P.D. Heme as a magnificent molecule with multiple missions: heme determines its own fate and governs cellular homeostasis. Tohoku J Exp Med 2007, 213:1-16.
31. Mense S.M., Zhang L. Heme: a versatile signaling molecule controlling the activities of diverse regulators ranging from transcription factors to MAP kinases. Cell Res 2006, 16:681-692.
32. Fernandez A., Lechardeur D., Derre-Bobillot A., Couve E., Gaudu P., Gruss A. Two coregulated efflux transporters modulate intracellular heme and protoporphyrin IX availability in Streptococcus agalactiae. PLoS Pathog 2010, 6:e1000860.
33. Stauff D.L., Bagaley D., Torres V.J., Joyce R., Anderson K.L., Kuechenmeister L., Dunman P.M., Skaar E.P. Staphylococcus aureus HrtA is an ATPase required for protection against heme toxicity and prevention of a transcriptional heme stress response. J Bacteriol 2008, 190:3588-3596.
34. Torres V.J., Stauff D.L., Pishchany G., Bezbradica J.S., Gordy L.E., Iturregui J., Anderson K.L., Dunman P.M., Joyce S., Skaar E.P. A Staphylococcus aureus regulatory system that responds to host heme and modulates virulence. Cell Host Microbe 2007, 1:109-119.
35. Fenton M.P. An investigation into the sources of lactic acid bacteria in grass silage. J Appl Bacteriol 1987, 62:181-188.
36. Kelly W.J., Davey G.P., Ward L.J. Characterization of lactococci isolated from minimally processed fresh fruit and vegetables. Int J Food Microbiol 1998, 45:85-92.
37. Ahrne S., Nobaek S., Jeppsson B., Adlerberth I., Wold A.E., Molin G. The normal Lactobacillus flora of healthy human rectal and oral mucosa. J Appl Microbiol 1998, 85:88-94.
38. Dubos R., Schaedler R.W., Costello R., Hoet P. Indigenous normal, and autochthonous flora of the gastrointestinal tract. J Exp Med 1965, 122:67-76.
39. Stougaard J., Petersen T.E., Marcker K.A. Expression of a complete soybean leghemoglobin gene in root nodules of transgenic Lotus corniculatus. Proc Natl Acad Sci USA 1987, 84:5754-5757.
40. Razvi A., Zhang Z., Lan C.Q. Effects of glucose and nitrogen source concentration on batch fermentation kinetics of Lactococcus lactis under hemin-stimulated respirative condition. Biotechnol Prog 2008, 24:852-858.
41. Kringelum BW, Sørensen NM, Garrigues C, Pedersen MB, Grøn S: Use of compounds involved in biosynthesis of nucleic acids to increase yield of bacterial cultures. US Patent 2006.
42. Garrigues C., Johansen E., Pedersen M.B., Mollgaard H., Sorensen K.I., Gaudu P., Gruss A., Lamberet G. Getting high (OD) on heme. Nat Rev Microbiol 2006, 4:c2. author reply c3.
43. Teusink B., Smid E.J. Modelling strategies for the industrial exploitation of lactic acid bacteria. Nat Rev Microbiol 2006, 4:46-56.
44. Høier E., Janzen T., Rattray F., Sørensen K., Børsting M.W., Brockmann E., Johansen E. The production, application and action of lactic cheese starter cultures. Technology of Cheesemaking 2010, 166-192. Wiley, Blackwell Publishing Ltd. 2nd ed. B.A. Law, A.Y. Tamime (Eds.).
45. Pedersen M.B., Iversen S.L., Sorensen K.I., Johansen E. The long and winding road from the research laboratory to industrial applications of lactic acid bacteria. FEMS Microbiol Rev 2005, 29:611-624.
46. Kaneko T., Takahashi M., Suzuki H. Acetoin fermentation by citrate-positive Lactococcus lactis subsp. lactis 3022 grown aerobically in the presence of hemin or Cu. Appl Environ Microbiol 1990, 56:2644-2649.
47. Berlec A., Tompa G., Slapar N., Fonovic U.P., Rogelj I., Strukelj B. Optimization of fermentation conditions for the expression of sweet-tasting protein brazzein in Lactococcus lactis. Lett Appl Microbiol 2008, 46:227-231.
48. Mifune J., Grage K., Rehm B.H. Production of functionalized biopolyester granules by recombinant Lactococcus lactis. Appl Environ Microbiol 2009, 75:4668-4675.
49. Gaudu P., Yamamoto Y., Jensen P.R., Hammer K., Gruss A. Genetics of lactococci. Gram-Positive Pathogens 2006, ASM Press. 2nd ed. V.A. Fischetti, R.P. Novick, J.J. Ferretti, D.A. Portnoy, J.I. Rood (Eds.).