Metabolic footprint analysis uncovers strain specific overflow metabolism and D-isoleucine production of Staphylococcus aureus COL and HG001

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Dörries, Kirsten ^a   Lalk, Michael ^a  

^a UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYPHENYLLACTATE; ACETIC ACID; BRANCHED CHAIN AMINO ACID; CARBON; GLUTAMINE; ISOLEUCINE; LACTIC ACID; NITROGEN; UNCLASSIFIED DRUG;

AMINO ACID SYNTHESIS; AMINO ACID TRANSPORT; ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM CULTURE; BIOACCUMULATION; CHEMICAL ANALYSIS; CITRIC ACID CYCLE; GLUCOSE INTAKE; GLUCOSE TRANSPORT; METABOLIC FOOTPRINT ANALYSIS; METABOLITE; NONHUMAN; PHENOTYPE; PROTEIN SECRETION; STAPHYLOCOCCUS AUREUS;

BIOLOGICAL TRANSPORT; CARBON; CITRIC ACID CYCLE; GLUCOSE; GLUTAMINE; ISOLEUCINE; PHENOTYPE; PHENYLPROPIONATES; SPECIES SPECIFICITY; STAPHYLOCOCCUS AUREUS;

EID: 84891758227     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081500     Document Type: Article

References (55)

1. Schaberg DR, Culver DH, Gaynes RP (1991) Major trends in the microbial etiology of nosocomial infection. Am J Med 91: 72-75.
2. Lowy FD (1998) Staphylococcus aureus infections. N Engl J Med 339: 520-532.
3. Hamill RJ, Vann JM, Proctor RA (1986) Phagocytosis of Staphylococcus aureus by cultured bovine aortic endothelial cells: model for postadherence events in endovascular infections. Infect Immun 54: 833-836.
4. Vann JM, Proctor RA (1987) Ingestion of Staphylococcus aureus by bovine endothelial cells results in time- and inoculum-dependent damage to endothelial cell monolayers. Infect Immun 55: 2155-2163.
5. Sachse F, Becker K, von Eiff C, Metze D, Rudack C (2010) Staphylococcus aureus invades the epithelium in nasal polyposis and induces IL-6 in nasal epithelial cells in vitro. Allergy 65: 1430-1437.
6. Garzoni C, Francois P, Huyghe A, Couzinet S, Tapparel C, et al. (2007) A global view of Staphylococcus aureus whole genome expression upon internalization in human epithelial cells. BMC Genomics 8: 171.
7. Burian M, Wolz C, Goerke C (2010) Regulatory adaptation of Staphylococcus aureus during nasal colonization of humans. PLoS One 5: e10040.
8. Giese B, Glowinski F, Paprotka K, Dittmann S, Steiner T, et al. (2011) Expression of delta-toxin by Staphylococcus aureus mediates escape from phagoendosomes of human epithelial and endothelial cells in the presence of beta-toxin. Cell Microbiol 13: 316-329.
9. Shi L, Adkins JN, Coleman JR, Schepmoes AA, Dohnkova A, et al. (2006) Proteomic analysis of Salmonella enterica serovar typhimurium isolated from RAW 264.7 macrophages: identification of a novel protein that contributes to the replication of serovar typhimurium inside macrophages. J Biol Chem 281: 29131-29140.
10. Pöther DC, Gierok P, Harms M, Mostertz J, Hochgräfe F, et al. (2013) Distribution and infection-related functions of bacillithiol in Staphylococcus aureus. Int J Med Microbiol 303: 114-123.
11. Schmidt F, Scharf SS, Hildebrandt P, Burian M, Bernhardt J, et al. (2010) Time-resolved quantitative proteome profiling of host-pathogen interactions: the response of Staphylococcus aureus RN1HG to internalisation by human airway epithelial cells. Proteomics 10: 2801-2811.
12. Pförtner H, Wagner J, Surmann K, Hildebrandt P, Ernst S, et al. (2013) A proteomics workflow for quantitative and time-resolved analysis of adaptation reactions of internalized bacteria. Methods 61: 244-250.
13. Somerville GA, Chaussee MS, Morgan CI, Fitzgerald JR, Dorward DW, et al. (2002) Staphylococcus aureus aconitase inactivation unexpectedly inhibits post-exponential-phase growth and enhances stationary-phase survival. Infect Immun 70: 6373-6382.
14. Pohl K, Francois P, Stenz L, Schlink F, Geiger T, et al. (2009) CodY in Staphylococcus aureus: a regulatory link between metabolism and virulence gene expression. J Bacteriol 191: 2953-2963.
15. Majerczyk CD, Dunman PM, Luong TT, Lee CY, Sadykov MR, et al. (2010) Direct targets of CodY in Staphylococcus aureus. J Bacteriol 192: 2861-2877.
16. Goldschmidt MC, Powelson DM (1953) Effect of the culture medium on the oxidation of acetate by Micrococcus pyogenes var. aureus . Arch Biochem Biophys 46: 154-163.
17. Gaupp R, Schlag S, Liebeke M, Lalk M, Götz F (2010) Advantage of upregulation of succinate dehydrogenase in Staphylococcus aureus biofilms. J Bacteriol 192: 2385-2394.
18. Herbert S, Ziebandt AK, Ohlsen K, Schäfer T, Hecker M, et al. (2010) Repair of global regulators in Staphylococcus aureus 8325 and comparative analysis with other clinical isolates. Infect Immun 78: 2877-2889.
19. Shafer WM, Iandolo JJ (1979) Genetics of staphylococcal enterotoxin B in methicillin-resistant isolates of Staphylococcus aureus. Infect Immun 25: 902-911.
20. Somerville GA, Said-Salim B, Wickman JM, Raffel SJ, Kreiswirth BN, et al. (2003) Correlation of acetate catabolism and growth yield in Staphylococcus aureus: implications for host-pathogen interactions. Infect Immun 71: 4724-4732.
21. Allen J, Davey HM, Broadhurst D, Heald JK, Rowland JJ, et al. (2003) High-throughput classification of yeast mutants for functional genomics using metabolic footprinting. Nat Biotechnol 21: 692-696.
22. Gertz S, Engelmann S, Schmid R, Ohlsen K, Hacker J, et al. (1999) Regulation of sigmaB-dependent transcription of sigB and asp23 in two different Staphylococcus aureus strains. Mol Gen Genet 261: 558-566.
23. Fuchs S, Pané-Farré J, Kohler C, Hecker M, Engelmann S (2007) Anaerobic gene expression in Staphylococcus aureus. J Bacteriol 189: 4275-4289.
24. Klukas C, Schreiber F (2010) Integration of -omics data and networks for biomedical research with VANTED. J Integr Bioinform 7: 112.
25. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics software package for education and data analysis. Palaeontol Electronica 4: http://palaeo-electronica.org/2001-2001/past/issue2001-2001.htm.
26. Saeed AI, Sharov V, White J, Li J, Liang W, et al. (2003) TM4: a free, opensource system for microarray data management and analysis. Biotechniques 34: 374-378.
27. Blumenthal HJ, Huettner CF, Montiel FA (1974) Comparative aspects of glucose catabolism in Staphylococcus aureus and S. epidermidis. Ann N Y Acad Sci 236: 105-114.
28. Gardner JF, Lascelles J (1962) The requirement for acetate of a streptomycin-resistant strain of Staphylococcus aureus. J Gen Microbiol 29: 157-164.
29. Liebeke M, Dörries K, Zühlke D, Bernhardt J, Fuchs S, et al. (2011) A metabolomics and proteomics study of the adaptation of Staphylococcus aureus to glucose starvation. Mol Biosyst 7: 1241-1253.
30. Lopez de Felipe F, Kleerebezem M, de Vos WM, Hugenholtz J (1998) Cofactor engineering: a novel approach to metabolic engineering in Lactococcus lactis by controlled expression of NADH oxidase. J Bacteriol 180: 3804-3808.
31. Hugenholtz J, Kleerebezem M, Starrenburg M, Delcour J, de Vos W, et al. (2000) Lactococcus lactis as a cell factory for high-level diacetyl production. Appl Environ Microbiol 66: 4112-4114.
32. Le Bars D, Yvon M (2008) Formation of diacetyl and acetoin by Lactococcus lactis via aspartate catabolism. J Appl Microbiol 104: 171-177.
33. Strasters KC, Winkler KC (1963) Carbohydrate Metabolism of Staphylococcus aureus. J Gen Microbiol 33: 213-229.
34. Seidl K, Müller S, Francois P, Kriebitzsch C, Schrenzel J, et al. (2009) Effect of a glucose impulse on the CcpA regulon in Staphylococcus aureus. BMC Microbiol 9: 95.
35. Zhu Y, Xiong YQ, Sadykov MR, Fey PD, Lei MG, et al. (2009) Tricarboxylic acid cycle-dependent attenuation of Staphylococcus aureus in vivo virulence by selective inhibition of amino acid transport. Infect Immun 77: 4256-4264.
36. Sadykov MR, Hartmann T, Mattes TA, Hiatt M, Jann NJ, et al. (2011) CcpA coordinates central metabolism and biofilm formation in Staphylococcus epidermidis. Microbiology 157: 3458-3468.
37. Patton TG, Rice KC, Foster MK, Bayles KW (2005) The Staphylococcus aureus cidC gene encodes a pyruvate oxidase that affects acetate metabolism and cell death in stationary phase. Mol Microbiol 56: 1664-1674.
38. Seidl K, Stucki M, Ruegg M, Goerke C, Wolz C, et al. (2006) Staphylococcus aureus CcpA affects virulence determinant production and antibiotic resistance. Antimicrob Agents Chemother 50: 1183-1194.
39. Kohler C, Wolff S, Albrecht D, Fuchs S, Becher D, et al. (2005) Proteome analyses of Staphylococcus aureus in growing and non-growing cells: A physiological approach. Int J Med Microbiol 295: 547-565.
40. Sonenshein AL (2005) CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr Opin Microbiol 8: 203-207.
41. Chambellon E, Yvon M (2003) CodY-regulated aminotransferases AraT and BcaT play a major role in the growth of Lactococcus lactis in milk by regulating the intracellular pool of amino acids. Appl Environ Microbiol 69: 3061-3068.
42. 13C nuclear magnetic resonance investigation of the metabolism of leucine to isoamyl alcohol in Saccharomyces cerevisiae. J Biol Chem 272: 26871-26878.
43. Dickinson JR, Harrison SJ, Hewlins MJ (1998) An investigation of the metabolism of valine to isobutyl alcohol in Saccharomyces cerevisiae. J Biol Chem 273: 25751-25756.
44. Dickinson JR, Harrison SJ, Dickinson JA, Hewlins MJ (2000) An investigation of the metabolism of isoleucine to active amyl alcohol in Saccharomyces cerevisiae. J Biol Chem 275: 10937-10942.
45. Lam H, Oh DC, Cava F, Takacs CN, Clardy J, et al. (2009) D-amino acids govern stationary phase cell wall remodeling in bacteria. Science 325: 1552-1555.
46. Horcajo P, de Pedro MA, Cava F (2012) Peptidoglycan plasticity in bacteria: stress-induced peptidoglycan editing by noncanonical D-amino acids. Microb Drug Resist 18: 306-313.
47. Cava F, de Pedro MA, Lam H, Davis BM, Waldor MK (2011) Distinct pathways for modification of the bacterial cell wall by non-canonical D-amino acids. EMBO J 30: 3442-3453.
48. Lupoli TJ, Tsukamoto H, Doud EH, Wang TS, Walker S, et al. (2011) Transpeptidase-mediated incorporation of D-amino acids into bacterial peptidoglycan. J Am Chem Soc 133: 10748-10751.
49. Kolodkin-Gal I, Romero D, Cao S, Clardy J, Kolter R, et al. (2010) D-amino acids trigger biofilm disassembly. Science 328: 627-629.
50. Hochbaum AI, Kolodkin-Gal I, Foulston L, Kolter R, Aizenberg J, et al. (2011) Inhibitory effects of D-amino acids on Staphylococcus aureus biofilm development. J Bacteriol 193: 5616-5622.
51. Lavermicocca P, Valerio F, Evidente A, Lazzaroni S, Corsetti A, et al. (2000) Purification and characterization of novel antifungal compounds from the sourdough Lactobacillus plantarum strain 21B. Appl Environ Microbiol 66: 4084-4090.
52. Valerio F, Lavermicocca P, Pascale M, Visconti A (2004) Production of phenyllactic acid by lactic acid bacteria: an approach to the selection of strains contributing to food quality and preservation. FEMS Microbiol Lett 233: 289-295.
53. Abrahamse SL, Pool-Zobel BL, Rechkemmer G (1999) Potential of short chain fatty acids to modulate the induction of DNA damage and changes in the intracellular calcium concentration by oxidative stress in isolated rat distal colon cells. Carcinogenesis 20: 629-634.
54. Jan G, Belzacq AS, Haouzi D, Rouault A, Métivier D, et al. (2002) Propionibacteria induce apoptosis of colorectal carcinoma cells via short-chain fatty acids acting on mitochondria. Cell Death Differ 9: 179-188.
55. Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ (2006) Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 40: 235-243.