Free glucosylglycerate is a novel marker of nitrogen stress in Mycobacterium smegmatis

Journal of Proteome Research

Volumn 11, Issue 7, 2012, Pages 3888-3896

  Behrends, Volker ^a   Williams, Kerstin J ^b   Jenkins, Victoria A ^b   Robertson, Brian D ^b   Bundy, Jacob G ^a  

^a Department of Surgery and Cancer ^*  (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

carbon metabolism; glucosylglycerate; glucosylglyceric acid; metabolic footprinting; Mycobacteria; nitrogen stress; NMR; nutrient limitation

Indexed keywords

2 OXOGLUTARIC ACID; AMMONIA; GLUCOSYLGLYCERATE; GLUTAMIC ACID; GLUTAMINE; GLYCERIC ACID; NITROGEN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; METABOLITE; METABOLOMICS; MYCOBACTERIUM SMEGMATIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OSMOTIC STRESS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

BIOLOGICAL MARKERS; GLUCOSIDES; GLUTAMIC ACID; GLYCERIC ACIDS; KETOGLUTARIC ACIDS; MYCOBACTERIUM SMEGMATIS; NITROGEN; STRESS, PHYSIOLOGICAL; TREHALOSE;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MYCOBACTERIUM SMEGMATIS;

EID: 84863630973     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300371b     Document Type: Article

References (39)

1. Reitzer, L. Nitrogen assimilation and global regulation in Escherichia coli Annu. Rev. Microbiol. 2003, 57, 155-76 (Pubitemid 37392939)
2. Truan, D.; Huergo, L. F.; Chubatsu, L. S.; Merrick, M.; Li, X. D.; Winkler, F. K. A new P(II) protein structure identifies the 2-oxoglutarate binding site J. Mol. Biol. 2010, 400, 531-9
3. Doucette, C. D.; Schwab, D. J.; Wingreen, N. S.; Rabinowitz, J. D. alpha-Ketoglutarate coordinates carbon and nitrogen utilization via enzyme I inhibition Nat. Chem. Biol. 2011, 7, 894-901
4. Lienhardt, C.; Espinal, M.; Pai, M.; Maher, D.; Raviglione, M. C. What research is needed to stop TB? Introducing the TB Research Movement PLoS Med. 2011, 8, e1001135
5. Amon, J.; Titgemeyer, F.; Burkovski, A. A genomic view on nitrogen metabolism and nitrogen control in mycobacteria J. Mol. Microbiol. Biotechnol. 2009, 17, 20-9
6. Mashego, M. R.; Rumbold, K.; De Mey, M.; Vandamme, E.; Soetaert, W.; Heijnen, J. J. Microbial metabolomics: past, present and future methodologies Biotechnol. Lett. 2007, 29, 1-16 (Pubitemid 44950152)
7. Oldiges, M.; Lutz, S.; Pflug, S.; Schroer, K.; Stein, N.; Wiendahl, C. Metabolomics: current state and evolving methodologies and tools Appl. Microbiol. Biotechnol. 2007, 76, 495-511 (Pubitemid 47283107)
8. Behrends, V.; Bundy, J. G.; Williams, H. D. Differences in strategies to combat osmotic stress in Burkholderia cenocepacia elucidated by NMR-based metabolic profiling Lett. Appl. Microbiol. 2011, 52, 619-25
9. Jozefczuk, S.; Klie, S.; Catchpole, G.; Szymanski, J.; Cuadros-Inostroza, A.; Steinhauser, D.; Selbig, J.; Willmitzer, L. Metabolomic and transcriptomic stress response of Escherichia coli Mol. Syst. Biol. 2010, 6, 364
10. Tremaroli, V.; Workentine, M. L.; Weljie, A. M.; Vogel, H. J.; Ceri, H.; Viti, C.; Tatti, E.; Zhang, P.; Hynes, A. P.; Turner, R. J.; Zannoni, D. Metabolomic investigation of the bacterial response to a metal challenge Appl. Environ. Microbiol. 2009, 75, 719-728
11. Snapper, S. B.; Melton, R. E.; Mustafa, S.; Kieser, T.; Jacobs, W. R. J. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis Mol. Microbiol. 1990, 4, 1911-9
12. Parish, T.; Wheeler, P. R. Mycobacteria Protocols; Humana Press: Totowa, 1998.
13. Saikolappan, S.; Das, K.; Sasindran, S. J.; Jagannath, C.; Dhandayuthapani, S. OsmC proteins of Mycobacterium tuberculosis and Mycobacterium smegmatis protect against organic hydroperoxide stress Tuberculosis 2011, 91 (Suppl 1) S119-27
14. Bolten, C. J.; Kiefer, P.; Letisse, F.; Portais, J. C.; Wittmann, C. Sampling for metabolome analysis of microorganisms Anal. Chem. 2007, 79, 3843-9 (Pubitemid 46799081)
15. Kind, T.; Wohlgemuth, G.; Lee do, Y.; Lu, Y.; Palazoglu, M.; Shahbaz, S.; Fiehn, O. FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry Anal. Chem. 2009, 81, 10038-48
16. Beckonert, O.; Keun, H. C.; Ebbels, T. M.; Bundy, J.; Holmes, E.; Lindon, J. C.; Nicholson, J. K. Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts Nat. Protoc. 2007, 2, 2692-703
17. Ulrich, E. L.; Akutsu, H.; Doreleijers, J. F.; Harano, Y.; Ioannidis, Y. E.; Lin, J.; Livny, M.; Mading, S.; Maziuk, D.; Miller, Z.; Nakatani, E.; Schulte, C. F.; Tolmie, D. E.; Kent Wenger, R.; Yao, H.; Markley, J. L. BioMagResBank Nucleic Acids Res. 2008, 36, D402-8
18. Wishart, D. S.; Knox, C.; Guo, A. C.; Eisner, R.; Young, N.; Gautam, B.; Hau, D. D.; Psychogios, N.; Dong, E.; Bouatra, S.; Mandal, R.; Sinelnikov, I.; Xia, J.; Jia, L.; Cruz, J. A.; Lim, E.; Sobsey, C. A.; Shrivastava, S.; Huang, P.; Liu, P.; Fang, L.; Peng, J.; Fradette, R.; Cheng, D.; Tzur, D.; Clements, M.; Lewis, A.; De Souza, A.; Zuniga, A.; Dawe, M.; Xiong, Y.; Clive, D.; Greiner, R.; Nazyrova, A.; Shaykhutdinov, R.; Li, L.; Vogel, H. J.; Forsythe, I. HMDB: a knowledgebase for the human metabolome Nucleic Acids Res. 2009, 37, D603-10
19. Stein, S. E. An integrated method for spectrum extraction and compound identification from gas chromatography/mass spectrometry data J. Am. Soc. Mass Spectrom. 1999, 10, 770-81 (Pubitemid 34506228)
20. Behrends, V.; Tredwell, G. D.; Bundy, J. G. A software complement to AMDIS for processing GC-MS metabolomic data Anal. Biochem. 2011, 415, 206-208
21. Jenkins, V. A.; Robertson, B. D.; Williams, K. J. Aspartate D48 is essential for the GlnR-mediated transcriptional response to nitrogen limitation in Mycobacterium smegmatis FEMS Microbiol. Lett. 2012, 330, 38-45
22. Behrends, V.; Ebbels, T. M. D.; Williams, H. D.; Bundy, J. G. Time-resolved metabolic footprinting for non-linear modelling of bacterial substrate utilization Appl. Environ. Microbiol. 2009, 75, 2453-63
23. Hunter, B. K.; Mowbray, S. L.; Walton, D. J. A compound representing the D-glycerate terminus of the methylglucose-containing polysaccharide of Mycobacterium smegmatis Biochemistry 1979, 18, 4458-65 (Pubitemid 10209034)
24. Kamisango, K.; Dell, A.; Ballou, C. E. Biosynthesis of the mycobacterial O-methylglucose lipopolysaccharide. Characterization of putative intermediates in the initiation, elongation, and termination reactions J. Biol. Chem. 1987, 262, 4580-6 (Pubitemid 17102822)
25. Takenaka, F.; Uchiyama, H.; Imamura, T. Identification of alpha-D-glucosylglycerol in sake Biosci. Biotechnol. Biochem. 2000, 64, 378-85
26. Kaur, D.; Pham, H.; Larrouy-Maumus, G.; Riviere, M.; Vissa, V.; Guerin, M. E.; Puzo, G.; Brennan, P. J.; Jackson, M. Initiation of methylglucose lipopolysaccharide biosynthesis in mycobacteria PLoS One 2009, 4, e5447
27. Kramer, R. Bacterial stimulus perception and signal transduction: response to osmotic stress Chem. Rec. 2010, 10, 217-29
28. Klahn, S.; Steglich, C.; Hess, W. R.; Hagemann, M. Glucosylglycerate: a secondary compatible solute common to marine cyanobacteria from nitrogen-poor environments Environ. Microbiol. 2010, 12, 83-94
29. Elbein, A. D.; Pan, Y. T.; Pastuszak, I.; Carroll, D. New insights on trehalose: a multifunctional molecule Glycobiology. 2003, 13, 17R-27R (Pubitemid 36592310)
30. Empadinhas, N.; da Costa, M. S. Diversity, biological roles and biosynthetic pathways for sugar-glycerate containing compatible solutes in bacteria and archaea Environ. Microbiol. 2011, 13, 2056-77
31. Cox, R. A.; Cook, G. M. Growth regulation in the mycobacterial cell Curr. Mol. Med. 2007, 7, 231-45 (Pubitemid 46767784)
32. Smeulders, M. J.; Keer, J.; Speight, R. A.; Williams, H. D. Adaptation of Mycobacterium smegmatis to stationary phase J. Bacteriol. 1999, 181, 270-283 (Pubitemid 29013681)
33. Wietzerbin-Falszpan, J.; Das, B. C.; Gros, C.; Petit, J. F.; Lederer, E. The amino acids of the cell wall of Mycobacterium tuberculosis var. bovis, strain BCG. Presence of a poly(L-glutamic acid) Eur. J. Biochem. 1973, 32, 525-32
34. Raunio, R. Accumulation of keto acids during the growth cycle of Escherichia coli Acta Chem. Scand. 1966, 20, 11-6
35. Van Elsas, J. D.; Van Overbeek, L. S. Starvation in Bacteria.; Plenum Press: New York, 1993.
36. Pope, C. F.; McHugh, T. D.; Gillespie, S. H. Methods to determine fitness in bacteria Methods Mol. Biol. 2010, 642, 113-21
37. Forsberg, L. S.; Dell, A.; Walton, D. J.; Ballou, C. E. Revised structure for the 6-O-methylglucose polysaccharide of Mycobacterium smegmatis J. Biol. Chem. 1982, 257, 3555-63 (Pubitemid 12077137)
38. Griffin, J. E.; Gawronski, J. D.; Dejesus, M. A.; Ioerger, T. R.; Akerley, B. J.; Sassetti, C. M. High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism PLoS Pathog. 2011, 7, e1002251
39. Sassetti, C. M.; Boyd, D. H.; Rubin, E. J. Genes required for mycobacterial growth defined by high density mutagenesis Mol. Microbiol. 2003, 48, 77-84 (Pubitemid 36411469)