Quantitative NMR metabolite profiling of methicillin-resistant and methicillin-susceptible staphylococcus aureus discriminates between biofilm and planktonic phenotypes

Journal of Proteome Research

Volumn 13, Issue 6, 2014, Pages 2973-2985

  Ammons, Mary Cloud B ^a   Tripet, Brian P ^a   Carlson, Ross P ^b   Kirker, Kelly R ^b   Gross, Michael A ^a   Stanisich, Jessica J ^a   Copié, Valérie ^a  

^a MONTANA STATE UNIVERSITY   (United States)

^b Montana State University   (United States)

Author keywords

biofilm; NMR metabolomics; Staphylococcus aureus

Indexed keywords

BUTANEDIOL;

AMINO ACID TRANSPORT; ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BIOFILM; CONTROLLED STUDY; ENERGY YIELD; FERMENTATION; LIPOLYSIS; METABOLOMICS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN SUSCEPTIBLE STAPHYLOCOCCUS AUREUS; NONHUMAN; PHENOTYPIC VARIATION; PLANKTON; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS; COMPARATIVE STUDY; METABOLISM; METABOLOME; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PENICILLIN RESISTANCE; PH; PHENOTYPE; PRINCIPAL COMPONENT ANALYSIS; PROTEOMICS;

BIOFILMS; HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE SPECTROSCOPY; METABOLOME; METHICILLIN RESISTANCE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; PHENOTYPE; PLANKTON; PRINCIPAL COMPONENT ANALYSIS; PROTEOMICS;

EID: 84902108692     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr500120c     Document Type: Article

References (63)

1. American Diabetes Association. conomic costs of diabetes in the U.S In 2007 Diabetes Care 2008, 31 (3) 596-615
2. James, G. A.; Swogger, E.; Wolcott, R.; Pulcini, E.; Secor, P.; Sestrich, J.; Costerton, J. W.; Stewart, P. S. Biofilms in chronic wounds Wound Repair Regener. 2008, 16 (1) 37-44
3. Konturek, P. C.; Brzozowski, T.; Konturek, S. J.; Kwiecien, S.; Dembinski, A.; Hahn, E. G. Influence of bacterial lipopolysaccharide on healing of chronic experimental ulcer in rat Scand. J. Gastroenterol. 2001, 36 (12) 1239-1247
4. Power, C.; Wang, J. H.; Sookhai, S.; Street, J. T.; Redmond, H. P. Bacterial wall products induce downregulation of vascular endothelial growth factor receptors on endothelial cells via a CD14-dependent mechanism: implications for surgical wound healing J. Surg. Res. 2001, 101 (2) 138-145
5. Costerton, J. W.; Stewart, P. S.; Greenberg, E. P. Bacterial biofilms: a common cause of persistent infections Science 1999, 284 (5418) 1318-1322
6. Dowd, S. E.; Sun, Y.; Secor, P. R.; Rhoads, D. D.; Wolcott, B. M.; James, G. A.; Wolcott, R. D. Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing BMC Microbiol. 2008, 8, 43
7. Burke, K. A.; Lascelles, J. Nitrate reductase system in Staphylococcus aureus wild type and mutants J. Bacteriol. 1975, 123 (1) 308-316
8. Evans, J. B. Uracil and pyruvate requirements of anaerobic growth of staphylococci J. Clin. Microbiol. 1975, 2 (1) 14-17
9. Strasters, K. C.; Winkler, K. C. Carbohydrate Metabolism of Staphylococcus Aureus J. Gen. Microbiol. 1963, 33, 213-229
10. Leibig, M.; Liebeke, M.; Mader, D.; Lalk, M.; Peschel, A.; Gotz, F. Pyruvate formate lyase acts as a formate supplier for metabolic processes during anaerobiosis in Staphylococcus aureus J. Bacteriol. 2011, 193 (4) 952-962
11. Stewart, P. S.; Franklin, M. J. Physiological heterogeneity in biofilms Nat. Rev. Microbiol. 2008, 6 (3) 199-210
12. Rasmussen, K.; Lewandowski, Z. Microelectrode measurements of local mass transport rates in heterogeneous biofilms Biotechnol. Bioeng. 1998, 59 (3) 302-309
13. Fuchs, S.; Pane-Farre, J.; Kohler, C.; Hecker, M.; Engelmann, S. Anaerobic gene expression in Staphylococcus aureus J. Bacteriol. 2007, 189 (11) 4275-89
14. Bowden, G. H.; Li, Y. H. Nutritional influences on biofilm development Adv. Dental Res. 1997, 11 (1) 81-99
15. Stewart, P. S. Mechanisms of antibiotic resistance in bacterial biofilms Int. J. Med. Microbiol. 2002, 292 (2) 107-113
16. Gilbert, P.; Brown, M. R. Biofilms and beta-lactam activity J. Antimicrob. Chemother. 1998, 41 (5) 571-572
17. Resch, A.; Rosenstein, R.; Nerz, C.; Gotz, F. Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions Appl. Environ. Microbiol. 2005, 71 (5) 2663-2676
18. Resch, A.; Leicht, S.; Saric, M.; Pasztor, L.; Jakob, A.; Gotz, F.; Nordheim, A. Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling Proteomics 2006, 6 (6) 1867-1877
19. Beenken, K. E.; Dunman, P. M.; McAleese, F.; Macapagal, D.; Murphy, E.; Projan, S. J.; Blevins, J. S.; Smeltzer, M. S. Global gene expression in Staphylococcus aureus biofilms J. Bacteriol. 2004, 186 (14) 4665-4684
20. Hollywood, K.; Brison, D. R.; Goodacre, R. Metabolomics: current technologies and future trends Proteomics 2006, 6 (17) 4716-4723
21. Zhu, Y.; Weiss, E. C.; Otto, M.; Fey, P. D.; Smeltzer, M. S.; Somerville, G. A. Staphylococcus aureus biofilm metabolism and the influence of arginine on polysaccharide intercellular adhesin synthesis, biofilm formation, and pathogenesis Infect. Immun. 2007, 75 (9) 4219-4226
22. Becher, D.; Hempel, K.; Sievers, S.; Zuhlke, D.; Pane-Farre, J.; Otto, A.; Fuchs, S.; Albrecht, D.; Bernhardt, J.; Engelmann, S.; Volker, U.; van Dijl, J. M.; Hecker, M. A proteomic view of an important human pathogen - towards the quantification of the entire Staphylococcus aureus proteome PloS One 2009, 4 (12) e8176
23. Beenken, K. E.; Blevins, J. S.; Smeltzer, M. S. Mutation of sarA in Staphylococcus aureus limits biofilm formation Infect. Immun. 2003, 71 (7) 4206-4211
24. Cramton, S. E.; Gerke, C.; Schnell, N. F.; Nichols, W. W.; Gotz, F. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation Infect. Immun. 1999, 67 (10) 5427-5433
25. Rohde, H.; Knobloch, J. K.; Horstkotte, M. A.; Mack, D. Correlation of biofilm expression types of Staphylococcus epidermidis with polysaccharide intercellular adhesin synthesis: evidence for involvement of icaADBC genotype-independent factors Med. Microbiol. Immunol. 2001, 190 (3) 105-112
26. Kirker, K. R.; Secor, P. R.; James, G. A.; Fleckman, P.; Olerud, J. E.; Stewart, P. S. Loss of viability and induction of apoptosis in human keratinocytes exposed to Staphylococcus aureus biofilms in vitro Wound Repair Regener. 2009, 17 (5) 690-699
27. Wishart, D. S. Quantitative metabolomics using NMR TrAC, Trends Anal. Chem. 2008, 27 (3) 228-237
28. Jackson, J. E. A User's Guide to Principal Components; Wiley-Interscience: Hoboken, NJ, 2003; p xvii, 569 p.
29. Lipp, C.; Kirker, K.; Agostinho, A.; James, G.; Stewart, P. Testing wound dressings using an in vitro wound model J. Wound Care 2010, 19 (6) 220-226
30. Secor, P. R.; Jennings, L. K.; James, G. A.; Kirker, K. R.; Pulcini, E. D.; McInnerney, K.; Gerlach, R.; Livinghouse, T.; Hilmer, J. K.; Bothner, B.; Fleckman, P.; Olerud, J. E.; Stewart, P. S. Phevalin (aureusimine B) production by Staphylococcus aureus biofilm and impacts on human keratinocyte gene expression PloS One 2012, 7 (7) e40973
31. Secor, P. R.; James, G. A.; Fleckman, P.; Olerud, J. E.; McInnerney, K.; Stewart, P. S. Staphylococcus aureus Biofilm and Planktonic cultures differentially impact gene expression, mapk phosphorylation, and cytokine production in human keratinocytes BMC Microbiol. 2011, 11, 143
32. Kirker, K. R.; James, G. A.; Fleckman, P.; Olerud, J. E.; Stewart, P. S. Differential effects of planktonic and biofilm MRSA on human fibroblasts Wound Repair Regener. 2012, 20 (2) 253-261
33. Wu, X. H.; Yu, H. L.; Ba, Z. Y.; Chen, J. Y.; Sun, H. G.; Han, B. Z. Sampling methods for NMR-based metabolomics of Staphylococcus aureus Biotechnol. J. 2010, 5 (1) 75-84
34. Sun, J. L.; Zhang, S. K.; Chen, J. Y.; Han, B. Z. Metabolic profiling of Staphylococcus aureus cultivated under aerobic and anaerobic conditions with (1)H NMR-based nontargeted analysis Can. J. Microbiol. 2012, 58 (6) 709-718
35. Faijes, M.; Mars, A. E.; Smid, E. J. Comparison of quenching and extraction methodologies for metabolome analysis of Lactobacillus plantarum Microb. Cell Fact. 2007, 6, 27
36. Hiller, J.; Franco-Lara, E.; Papaioannou, V.; Weuster-Botz, D. Fast sampling and quenching procedures for microbial metabolic profiling Biotechnol. Lett. 2007, 29 (8) 1161-1167
37. Taymaz-Nikerel, H.; de Mey, M.; Ras, C.; ten Pierick, A.; Seifar, R. M.; van Dam, J. C.; Heijnen, J. J.; van Gulik, W. M. Development and application of a differential method for reliable metabolome analysis in Escherichia coli Anal. Biochem. 2009, 386 (1) 9-19
38. Villas-Boas, S. G.; Bruheim, P. Cold glycerol-saline: the promising quenching solution for accurate intracellular metabolite analysis of microbial cells Anal. Biochem. 2007, 370 (1) 87-97
39. Villas-Boas, S. G.; Hojer-Pedersen, J.; Akesson, M.; Smedsgaard, J.; Nielsen, J. Global metabolite analysis of yeast: evaluation of sample preparation methods Yeast 2005, 22 (14) 1155-1169
40. Wittmann, C.; Kromer, J. O.; Kiefer, P.; Binz, T.; Heinzle, E. Impact of the cold shock phenomenon on quantification of intracellular metabolites in bacteria Anal. Biochem. 2004, 327 (1) 135-139
41. Weljie, A. M.; Newton, J.; Mercier, P.; Carlson, E.; Slupsky, C. M. Targeted profiling: quantitative analysis of 1H NMR metabolomics data Anal. Chem. 2006, 78 (13) 4430-4442
42. Tredwell, G. D.; Edwards-Jones, B.; Leak, D. J.; Bundy, J. G. The development of metabolomic sampling procedures for Pichia pastoris, and baseline metabolome data PloS One 2011, 6 (1) e16286
43. Worley, B.; Powers, R. Multivariate Analysis in Metabolomics Curr. Metabolomics 2013, 1 (1) 92-107
44. Gillespie, J. J.; Wattam, A. R.; Cammer, S. A.; Gabbard, J. L.; Shukla, M. P.; Dalay, O.; Driscoll, T.; Hix, D.; Mane, S. P.; Mao, C.; Nordberg, E. K.; Scott, M.; Schulman, J. R.; Snyder, E. E.; Sullivan, D. E.; Wang, C.; Warren, A.; Williams, K. P.; Xue, T.; Yoo, H. S.; Zhang, C.; Zhang, Y.; Will, R.; Kenyon, R. W.; Sobral, B. W. PATRIC: the comprehensive bacterial bioinformatics resource with a focus on human pathogenic species Infect. Immun. 2011, 79 (11) 4286-4298
45. Liu, G. Y.; Essex, A.; Buchanan, J. T.; Datta, V.; Hoffman, H. M.; Bastian, J. F.; Fierer, J.; Nizet, V. Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity J. Exp. Med. 2005, 202 (2) 209-215
46. Kim, Y. S. Malonate metabolism: biochemistry, molecular biology, physiology, and industrial application J. Biochem. Mol. Biol. 2002, 35 (5) 443-451
47. Liebeke, M.; Dorries, K.; Zuhlke, D.; Bernhardt, J.; Fuchs, S.; Pane-Farre, J.; Engelmann, S.; Volker, U.; Bode, R.; Dandekar, T.; Lindequist, U.; Hecker, M.; Lalk, M. A metabolomics and proteomics study of the adaptation of Staphylococcus aureus to glucose starvation Mol. Biosyst. 2011, 7 (4) 1241-1253
48. Nisman, B. The Stickland reaction Bacteriol. Rev. 1954, 18 (1) 16-42
49. Dawes, E. A. Microbial Energetics; Blackie: New York, 1986; p viii, 187 p.
50. Khosravi-Darani, K.; Mokhtari, Z. B.; Amai, T.; Tanaka, K. Microbial production of poly(hydroxybutyrate) from C(1) carbon sources Appl. Microbiol. Biotechnol. 2013, 97 (4) 1407-1424
51. Liebeke, M.; Meyer, H.; Donat, S.; Ohlsen, K.; Lalk, M. A metabolomic view of Staphylococcus aureus and its ser/thr kinase and phosphatase deletion mutants: involvement in cell wall biosynthesis Chem. Biol. 2010, 17 (8) 820-830
52. Welman, A. D.; Maddox, I. S. Exopolysaccharides from lactic acid bacteria: perspectives and challenges Trends Biotechnol. 2003, 21 (6) 269-274
53. Navarre, W. W.; Schneewind, O. Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope Microbiol. Mol. Biol. Rev. 1999, 63 (1) 174-229
54. Ammons, M. C. Anti-biofilm strategies and the need for innovations in wound care Recent Pat. Anti-Infect. Drug Discovery 2010, 5 (1) 10-17
55. Mah, T. F. Biofilm-specific antibiotic resistance Future Microbiol. 2012, 7 (9) 1061-1072
56. Rohmer, L.; Hocquet, D.; Miller, S. I. Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis Trends Microbiol. 2011, 19 (7) 341-348
57. Davey, M. E.; O'Toole G, A. Microbial biofilms: from ecology to molecular genetics Microbiol Mol. Biol. Rev. 2000, 64 (4) 847-867
58. Ammons, M. C.; Ward, L. S.; Fisher, S. T.; Wolcott, R. D.; James, G. A. In vitro susceptibility of established biofilms composed of a clinical wound isolate of Pseudomonas aeruginosa treated with lactoferrin and xylitol Int. J. Antimicrob. Agents 2009, 33 (3) 230-236
59. Ivler, D. Comparative metabolism of virulent and avirulent staphylococci Ann. N.Y. Acad. Sci. 1965, 128, 62-80
60. Uhlemann, A. C.; Porcella, S. F.; Trivedi, S.; Sullivan, S. B.; Hafer, C.; Kennedy, A. D.; Barbian, K. D.; McCarthy, A. J.; Street, C.; Hirschberg, D. L.; Lipkin, W. I.; Lindsay, J. A.; DeLeo, F. R.; Lowy, F. D. Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties mBio 2012, 3, 2
61. Szewczyk, E.; Mikucki, J. Poly-beta-hydroxybutyric acid in staphylococci FEMS Microbiol. Lett. 1989, 52 (3) 279-284
62. Wozniak, D. J.; Wyckoff, T. J.; Starkey, M.; Keyser, R.; Azadi, P.; O'Toole, G. A.; Parsek, M. R. Alginate is not a significant component of the extracellular polysaccharide matrix of PA14 and PAO1 Pseudomonas aeruginosa biofilms Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (13) 7907-7912
63. Weidenmaier, C.; Peschel, A. Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions Nat. Rev. Microbiol. 2008, 6 (4) 276-287