1887

Abstract

is a major component of dairy starter cultures used for the manufacture of yoghurt and cheese. In this study, the CO metabolism of DSM 20617, grown in either a N atmosphere or an enriched CO atmosphere, was analysed using both genetic and proteomic approaches. Growth experiments performed in a chemically defined medium revealed that CO depletion resulted in bacterial arginine, aspartate and uracil auxotrophy. Moreover, CO depletion governed a significant change in cell morphology, and a high reduction in biomass production. A comparative proteomic analysis revealed that cells of showed a different degree of energy status depending on the CO availability. In agreement with proteomic data, cells grown under N showed a significantly higher milk acidification rate compared with those grown in an enriched CO atmosphere. Experiments carried out on wild-type and its derivative mutant, which was inactivated in the phosphoenolpyruvate carboxylase and carbamoyl-phosphate synthase activities responsible for fixing CO to organic molecules, suggested that the anaplerotic reactions governed by these enzymes have a central role in bacterial metabolism. Our results reveal the capnophilic nature of this micro-organism, underlining the essential role of CO in physiology, and suggesting potential applications in dairy fermentation processes.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.024737-0
2009-06-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/6/1953.html?itemId=/content/journal/micro/10.1099/mic.0.024737-0&mimeType=html&fmt=ahah

References

  1. Altermann E., Russell W. M., Azcarate-Peril M. A., Barrangou R., Buck B. L., McAuliffe O., Souther N., Dobson A., Duong T. other authors 2005; Complete genome of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc Natl Acad Sci U S A 102:3906–3912
    [Google Scholar]
  2. Arena S., D'Ambrosio C., Renzone G., Rullo R., Ledda L., Vitale F., Maglione G., Varcamonti M., Ferrara L., Scaloni A. 2006; A study of Streptococcus thermophilus proteome by integrated analytical procedures and differential expression investigations. Proteomics 6:181–192
    [Google Scholar]
  3. Arioli S., Monnet C., Guglielmetti S., Parini C., De Noni I., Hogenboom J., Halami P. M., Mora D. 2007; Aspartate biosynthesis is essential for the growth of Streptococcus thermophilus in milk, and aspartate availability modulates the level of urease activity. Appl Environ Microbiol 73:5789–5796
    [Google Scholar]
  4. Arsène-Ploetze F., Kugler V., Martinussen J., Bringel F. 2006; Expression of the pyr operon of Lactobacillus plantarum is regulated by inorganic carbon availability through a second regulator, PyrR2, homologous to the pyrimidine-dependent regulator PyrR. J Bacteriol 188:8607–8616
    [Google Scholar]
  5. Bernhardt J., Weibezahn J., Scharf C., Hecker M. 2003; Bacillus subtilis during feast and famine: visualization of the overall regulation of protein synthesis during glucose starvation by proteome analysis. Genome Res 13:224–237
    [Google Scholar]
  6. Biswas I., Gruss A., Ehrlich D., Maguin E. 1993; High-efficiency gene inactivation and replacement system for Gram-positive bacteria. J Bacteriol 175:3628–3635
    [Google Scholar]
  7. Bolotin A., Wincker P., Mauger S., Jaillon O., Malarme K., Weissanbach J., Ehrlich S. D., Sorokin A. 2001; The complete genome sequence of lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res 11:731–753
    [Google Scholar]
  8. Bolotin A., Quinquis B., Renault P., Sorokin A., Ehrlich S. D., Kulakauskas S., Lapidus A., Goltsman E., Mazur M. other authors 2004; Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus . Nat Biotechnol 22:1554–1558
    [Google Scholar]
  9. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
    [Google Scholar]
  10. Callanan M., Kaleta P., O'Callaghan J., O'Sullivan O., Jordan K., McAuliffe O., Sangrador-Vegas A., Slattery L., Fitzgerald G. F. other authors 2008; Genome sequence of Lactobacillus helveticus : an organism distinguished by selective gene loss and insertion sequence element expansion. J Bacteriol 190:727–735
    [Google Scholar]
  11. Chaillou S., Champomier-Vergès M. C., Cornet M., Crutz-Le Coq A. M., Dudez A. M., Martin S., Beaufils S., Darbon-Rongère E., Bossy R. other authors 2005; The complete genome sequence of the meat-borne lactic acid bacterium Lactobacillus sakei 23K. Nat Biotechnol 23:1527–1533
    [Google Scholar]
  12. Claesson M. J., Leahy S., Canchaya C., van Pijkeren J. P., Cerdeño-Tárraga A. M., Parkhill J., Flynn S., O'Sullivan G. C., Collins J. K. other authors 2006; Multireplicon genome architecture of Lactobacillus salivarius . Proc Natl Acad Sci U S A 103:6718–6723
    [Google Scholar]
  13. D'Ambrosio C., Arena S., Fulcoli G., Scheinfeld M. H., Zhou D., D'Adamio L., Scaloni A. 2006; Hyperphosphorylation of JNK-interacting protein 1, a protein associated with Alzheimer disease. Mol Cell Proteomics 5:97–113
    [Google Scholar]
  14. Eymann C., Dreisbach A., Albrecht D., Bernhardt J., Becher D., Gentner S., Tam le T., Büttner K., Buurman G. other authors 2004; A comprehensive proteome map of growing Bacillus subtilis cells. Proteomics 4:2849–2876
    [Google Scholar]
  15. Garrigues C., Loubiere P., Lindley D., Cocaign-Bousquet M. 1997; Control of the shift from homolactic acid to mixed-acid fermentation in Lactococcus lactis : predominant role of the NADH/NAD+ ratio. J Bacteriol 179:5282–5287
    [Google Scholar]
  16. Gaspar P., Neves A. R., Shearman C. A., Gasson M. J., Baptista A. M., Turner D. L., Soares C. M., Santos H. 2007; The lactate dehydrogenases encoded by the ldh and ldhB genes in Lactococcus lactis exibits distinct regulation and catalytic properties – comparative modelling to probe the molecular basis. FEBS J 274:5924–5936
    [Google Scholar]
  17. Giliberti G., Naclerio G., Martirani L., Ricca E., De Felice M. 2002; Alteration of cell morphology and viability in a recA mutant of Streptococcus thermophilus upon induction of heat shock and nutrient starvation. Gene 295:1–6
    [Google Scholar]
  18. Gunnewijk M. G. W., Poolman B. 2000a; Phosphorylation state of HPr determines the level of expression and the extent of phosphorylation of the lactose transport protein of Streptococcus thermophilus . J Biol Chem 275:34073–34079
    [Google Scholar]
  19. Gunnewijk M. G. W., Poolman B. 2000b; HPr(His-P)-mediated phosphorylation differently affects counterflow and proton motive force-driven uptake via the lactose transport protein of Streptococcus thermophilus . J Biol Chem 275:34080–34085
    [Google Scholar]
  20. Hols P., Hancy F., Fontaine L., Grossiord B., Prozzi D., Leblond-Bourget N., Decaris B., Bolotin A., Delorme C. other authors 2005; New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol Rev 29:435–463
    [Google Scholar]
  21. Kleerebezem M., Boekhorst J., van Kranenburg R., Molenaar D., Kuipers O., Leer R., Tarchini R., Peters S., Sandbrink H. M. other authors 2003; Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 100:1990–1995
    [Google Scholar]
  22. Link A. J., Eng J. K., Schieltz D. M., Carmack E., Mize G. J., Morris D. R., Garvik B. M., Yates J. R. III 1999; Direct analysis of protein complexes using mass spectrometry. Nat Biotechnol 17:676–682
    [Google Scholar]
  23. Louaileche H., Braquart P., Saulnier F., Desmazeud M., Linden G. 1993; Carbon dioxide effects on the growth and metabolites of morphological variants of Streptococcus thermophilus . J Dairy Sci 76:3683–3689
    [Google Scholar]
  24. Louaileche H., Bracquart P., Guimont C., Linden G. 1996; Carbon dioxide fixation by cells and cell-free extracts of Streptococcus thermophilus . J Dairy Res 63:321–325
    [Google Scholar]
  25. MacCoss M. J., Wu C. C., Yates J. R. III 2002; Probability based validation of protein identifications using a modified sequest algorithm. Anal Chem 74:5593–5599
    [Google Scholar]
  26. Makarova K., Slesarev A., Wolf Y., Sorokin A., Mirkin B., Koonin E., Pavolv A., Pavlova N., Karamychev V. other authors 2006; Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci U S A 103:15611–15616
    [Google Scholar]
  27. Manachini P. L., Fortina M. G., Parini C., Craveri R. 1985; Bacillus thermoruber sp. nov., nom. rev., a red pigmented thermophilic bacterium. Int J Syst Bacteriol 35:493–496
    [Google Scholar]
  28. Mastro R., Hall M. 1999; Protein delipidation and precipitation by tri- n -butylphosphate, acetone, and methanol treatment for isoelectric focusing and two-dimensional gel electrophoresis. Anal Biochem 273:313–315
    [Google Scholar]
  29. Mora D., Maguin E., Masiero M., Ricci G., Parini C., Manachini P. L., Daffonchio D. 2004; Characterization of urease genes cluster of Streptococcus thermophilus . J Appl Microbiol 96:209–219
    [Google Scholar]
  30. Mora D., Monnet C., Parini C., Guglielmetti S., Mariani A., Pintus P., Molinari F., Daffonchio D., Manachini P. L. 2005; Urease biogenesis in Streptococcus thermophilus . Res Microbiol 156:897–903
    [Google Scholar]
  31. Morita H., Toh H., Fukuda S., Horikawa H., Oshima K., Suzuki T., Murakami M., Hisamatsu S., Kato Y. other authors 2008; Comparative genome analysis of Lactobacillus reuteri and Lactobacillus fermentum reveal a genomic island for reuterin and cobolamin production. DNA Res 15:151–161
    [Google Scholar]
  32. Nicoloff H., Hubert J.-C., Bringel F. 2000; In Lactobacillus plantarum , carbamoyl phosphate is synthesized by two carbamoyl-phosphate synthetases (CPS): carbon dioxide differentiates the arginine-repressed from the pyrimidine-regulated CPS. J Bacteriol 182:3416–3422
    [Google Scholar]
  33. Nicoloff H., Elagöz A., Arsène-Ploetze F., Kammerer B., Martinussen J., Bringel F. 2005; Repression of the pyr operon in Lactobacillus plantarum prevents its ability to grow at low carbon dioxide levels. J Bacteriol 187:2093–2104
    [Google Scholar]
  34. Palmfeldt J., Levander F., Hahn-Hägerdal B., Peter J. 2004; Acidic proteome of growing and resting Lactococcus lactis metabolizing maltose. Proteomics 4:3881–3898
    [Google Scholar]
  35. Peng J., Elias J. E., Thoreen C. C., Licklider L. J., Gygi S. P. 2003; Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J Proteome Res 2:43–50
    [Google Scholar]
  36. Perkins D. N., Pappin D. J., Creasy D. M., Cottrell J. S. 1999; Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20:3551–3567
    [Google Scholar]
  37. Pridmore R. D., Berger B., Desiere F., Vilanova D., Barretto C., Pittet A. C., Zwahlen M. C., Rouvet M., Altermann E. other authors 2004; The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. 2004. Proc Natl Acad Sci U S A 101:2512–2517
    [Google Scholar]
  38. Reiter B., Oram J. D. 1962; Nutritional studies on cheese starters. I. Vitamin and amino acid requirements of single strain starters. J Dairy Res 29:63–77
    [Google Scholar]
  39. Rocco M., D'Ambrosio C., Arena S., Faurobert M., Scaloni A., Marra R. 2006; Proteomic analysis of tomato fruits from two ecotypes during ripening. Proteomics 6:3781–3791
    [Google Scholar]
  40. Salzano A. M., Arena S., Tenzone G., D'Ambrosio C., Rullo R., Bruschi M., Ledda L., Maglione G., Candiano G. other authors 2007; A widespread picture of the Streptococcus thermophilus proteome by cell lysate fractionation and gel-based/gel-free approaches. Proteomics 7:1420–1433
    [Google Scholar]
  41. Sciochetti S. A., Blakely G. W., Piggot P. J. 2001; Growth phase variation in cell and nucleoid morphology in a Bacillus subtilis recA mutant. J Bacteriol 183:2963–2968
    [Google Scholar]
  42. Talamo F., D'Ambrosio C., Arena S., Del Vecchio P., Ledda L., Zehender G., Ferrara L., Scaloni A. 2003; Proteins from bovine tissues and biological fluids: defining a reference electrophoresis map for liver, kidney, muscle, plasma and red blood cells. Proteomics 3:440–460
    [Google Scholar]
  43. Van de Guchte M., Penaud S., Grimaldi C., Berbe V., Bryson K., Nicolas P., Robert C., Oztas S., Mangenot S. other authors 2006; The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. Proc Natl Acad Sci U S A 103:9274–9279
    [Google Scholar]
  44. van den Bogaard P. T., Kleerebezem M., Kuipers O. P., de Vos W. M. 2000; Control of lactose transport, β -galactosidase activity, and glycolysis by CcpA in Streptococcus thermophilus : evidence for carbon catabolite repression by a non-phosphoenolpyruvate-dependent phosphotransferase system sugar. J Bacteriol 182:5982–5989
    [Google Scholar]
  45. Wang H., Weizhu Y., Coolbear T., O'Sullivan D., McKay L. L. 1998; A deficiency in aspartate biosynthesis in Lactococcus lactis subsp. lactis C2 causes slow milk coagulation. Appl Environ Microbiol 64:1673–1679
    [Google Scholar]
  46. Wang H., O'Sullivan D. J., Baldwin K. A., McKay L. L. 2000; Cloning, sequencing, and expression of the pyruvate carboxylase gene in Lactococcus lactis subsp. lactis C2. Appl Environ Microbiol 66:1223–1227
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.024737-0
Loading
/content/journal/micro/10.1099/mic.0.024737-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error