Deciphering the response of Mycobacterium smegmatis to nitrogen stress using bipartite active modules

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Williams, Kerstin J ^a   Bryant, William A ^b   Jenkins, Victoria A ^a   Barton, Geraint R ^b   Witney, Adam A ^c   Pinney, John W ^b   Robertson, Brian D ^a,b  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Gene Expression; Metabolic Network; Mycobacteria; Nitrogen Stress

Indexed keywords

CARBON; HYDROGEN PEROXIDE; NITROGEN;

AMT1 GENE; AMTA GENE; AMTB GENE; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL SURVIVAL; CELL METABOLISM; COMPUTER PROGRAM; DOWN REGULATION; ENERGY YIELD; GENE EXPRESSION; GENE MAPPING; GENETIC TRANSCRIPTION; GLNA GENE; GLND GENE; GLNK GENE; GLTD GENE; GROWTH RATE; MYCOBACTERIUM SMEGMATIS; NITROGEN AVAILABILITY; NITROGEN FIXATION; NITROGEN UPTAKE; NITROSATIVE STRESS; NONHUMAN; SCAVENGING SYSTEM; UPREGULATION;

ALGORITHMS; GENE EXPRESSION PROFILING; GENOME, BACTERIAL; GENOMICS; HYDROGEN PEROXIDE; MYCOBACTERIUM SMEGMATIS; NITROGEN; STRESS, PHYSIOLOGICAL;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MYCOBACTERIUM SMEGMATIS;

EID: 84879821892     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-436     Document Type: Article

References (38)

1. Leigh JA, Dodsworth JA. Nitrogen regulation in bacteria and archaea. Annu Rev Microbiol 2007, 61:349-377. 10.1146/annurev.micro.61.080706.093409, 17506680.
2. Merrick MJ, Edwards RA. Nitrogen control in bacteria. Microbiol Rev 1995, 59:604-622. 239390, 8531888.
3. Reitzer L. Nitrogen assimilation and global regulation in Escherichia coli. Annu Rev Microbiol 2003, 57:155-176. 10.1146/annurev.micro.57.030502.090820, 12730324.
4. Reuther J, Wohlleben W. Nitrogen metabolism in Streptomyces coelicolor: transcriptional and post-translational regulation. J Mol Microbiol Biotechnol 2007, 12:139-146. 10.1159/000096469, 17183221.
5. Amon J, Titgemeyer F, Burkovski A. Common patterns - unique features: nitrogen metabolism and regulation in Gram-positive bacteria. FEMS Microbiol Rev 2010, 34:588-605.
6. Hesketh A, Fink D, Gust B, Rexer H-U, Scheel B, Chater K, Wohlleben W, Engels A. The GlnD and GlnK homologues of Streptomyces coelicolor A3(2) are functionally dissimilar to their nitrogen regulatory system counterparts from enteric bacteria. Mol Microbiol 2002, 46:319-330. 10.1046/j.1365-2958.2002.03149.x, 12406211.
7. Harper C, Hayward D, Wiid I, van Helden P. Regulation of nitrogen metabolism in Mycobacterium tuberculosis: a comparison with mechanisms in Corynebacterium glutamicum and Streptomyces coelicolor. IUBMB Life 2008, 60:643-650. 10.1002/iub.100, 18493948.
8. Burkovski A. Nitrogen control in Corynebacterium glutamicum: proteins, mechanisms, signals. J Microbiol Biotechnol 2007, 17:187-194.
9. Walter B, Hänssler E, Kalinowski J, Burkovski A. Nitrogen metabolism and nitrogen control in corynebacteria: variations of a common theme. J Mol Microbiol Biotechnol 2007, 12:131-138. 10.1159/000096468, 17183220.
10. Amon J, Titgemeyer F, Burkovski A. A genomic view on nitrogen metabolism and nitrogen control in mycobacteria. J Mol Microbiol Biotechnol 2009, 17:20-29. 10.1159/000159195, 18824837.
11. Betts JC, Lukey PT, Robb LC, McAdam RA, Duncan K. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol Microbiol 2002, 43:717-731. 10.1046/j.1365-2958.2002.02779.x, 11929527.
12. Hampshire T, Soneji S, Bacon J, James BW, Hinds J, Laing K, Stabler RA, Marsh PD, Butcher PD. Stationary phase gene expression of Mycobacterium tuberculosis following a progressive nutrient depletion: a model for persistent organisms?. Tuberculosis 2004, 84:228-238. 10.1016/j.tube.2003.12.010, 3195342, 15207492.
13. Voskuil MI, Visconti KC, Schoolnik GK. Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy. Tuberculosis 2004, 84:218-227. 10.1016/j.tube.2004.02.003, 15207491.
14. Beste DJV, Laing E, Bonde B, Avignone-Rossa C, Bushell ME, McFadden JJ. Transcriptomic analysis identifies growth rate modulation as a component of the adaptation of mycobacteria to survival inside the macrophage. J Bacteriol 2007, 189:3969-3976. 10.1128/JB.01787-06, 1913408, 17384194.
15. Bacon J, James BW, Wernisch L, Williams A, Morley KA, Hatch GJ, Mangan JA, Hinds J, Stoker NG, Butcher PD, Marsh PD. The influence of reduced oxygen availability on pathogenicity and gene expression in Mycobacterium tuberculosis. Tuberculosis 2004, 84:205-217. 10.1016/j.tube.2003.12.011, 15207490.
16. Berney M, Cook GM. Unique flexibility in energy metabolism allows mycobacteria to combat starvation and hypoxia. PLoS One 2010, 5:e8614. 10.1371/journal.pone.0008614, 2799521, 20062806.
17. Zimmer DP, Soupene E, Lee HL, Wendisch VF, Khodursky AB, Peter BJ, Bender RA, Kustu S. Nitrogen regulatory protein C-controlled genes of Escherichia coli: scavenging as a defense against nitrogen limitation. Proc Natl Acad Sci USA 2000, 97:14674-14679. 10.1073/pnas.97.26.14674, 18977, 11121068.
18. Tiffert Y, Franz-Wachtel M, Fladerer C, Nordheim A, Reuther J, Wohlleben W, Mast Y. Proteomic analysis of the GlnR-mediated response to nitrogen limitation in Streptomyces coelicolor M145. Applied Microbiol Biotechnol 2011, 89:1149-1159.
19. Tiffert Y, Supra P, Wurm R, Wohlleben W, Wagner R, Reuther J. The Streptomyces coelicolor GlnR regulon: identification of new GlnR targets and evidence for a central role of GlnR in nitrogen metabolism in actinomycetes. Mol Microbiol 2008, 67:861-880. 10.1111/j.1365-2958.2007.06092.x, 18179599.
20. Pullan ST, Chandra G, Bibb MJ, Merrick M. Genome-wide analysis of the role of GlnR in Streptomyces venezuelae provides new insights into global nitrogen regulation in actinomycetes. BMC Genomics 2011, 12:175. 10.1186/1471-2164-12-175, 3087709, 21463507.
21. Amon J, Bräu T, Grimrath A, Hänssler E, Hasselt K, Höller M, Jessberger N, Ott L, Szököl J, Titgemeyer F, Burkovski A. Nitrogen control in Mycobacterium smegmatis: nitrogen-dependent expression of ammonium transport and assimilation proteins depends on the OmpR-type regulator GlnR. J Bacteriol 2008, 190:7108-7116. 10.1128/JB.00855-08, 2580704, 18689485.
22. Jenkins VA, Robertson BD, Williams KJ. Aspartate D48 is essential for the GlnR-mediated transcriptional response to nitrogen limitation in Mycobacterium smegmatis. FEMS Microbiol Lett 2012, 330:38-45. 10.1111/j.1574-6968.2012.02530.x, 22356601.
23. Jenkins VA, Barton GR, Robertson BD, Williams KJ. Genome wide analysis of the complete GlnR nitrogen-response regulon in Mycobacterium smegmatis. BMC Genomics 2013, 14:301. 10.1186/1471-2164-14-301, 3662644, 23642041.
24. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 2012, 40:D109-D114. 10.1093/nar/gkr988, 3245020, 22080510.
25. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005, 102:15545-15550. 10.1073/pnas.0506580102, 1239896, 16199517.
26. Bonde BK, Beste DJV, Laing E, Kierzek AM, McFadden J. Differential Producibility Analysis (DPA) of transcriptomic data with metabolic networks: deconstructing the metabolic response of m. tuberculosis. PLoS Comp Biol 2011, 7:e1002060.
27. Colijn C, Brandes A, Zucker J, Lun DS, Weiner B, Farhat MR, Cheng T-Y, Moody DB, Murray M, Galagan JE. Interpreting expression data with metabolic flux models: predicting Mycobacterium tuberculosis mycolic acid production. PLoS Comp Biol 2009, 5:e1000489.
28. Bonarius HPJ, Schmid G, Tramper J. Flux analysis of underdetermined metabolic networks: the quest for the missing constraints. Trends Biotechnol 1997, 15:308-314.
29. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang H-Y, Cohoon M, de Crécy-Lagard V, Diaz N, Disz T, Edwards R, Fonstein M, Frank ED, Gerdes S, Glass EM, Goesmann A, Hanson A, Iwata-Reuyl D, Jensen R, Jamshidi N, Krause L, Kubal M, Larsen N, Linke B, McHardy AC, Meyer F, Neuweger H, Olsen G, Olson R, Osterman A, Portnoy V, et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 2005, 33:5691-5702. 10.1093/nar/gki866, 1251668, 16214803.
30. Bryant WA, Sternberg MJ, Pinney JW. AMBIENT: active modules for bipartite networks - using high-throughput transcriptomic data to dissect metabolic response. BMC Syst Biol 2013, 7:26. 10.1186/1752-0509-7-26, 3656802, 23531303.
31. Henry CS, DeJongh M, Best AA, Frybarger PM, Linsay B, Stevens RL. High-throughput generation, optimization and analysis of genome-scale metabolic models. Nat Biotechnol 2010, 28:977-982. 10.1038/nbt.1672, 20802497.
32. Guest JR. Anaerobic growth of Escherichia coli K12 with fumarate as terminal electron acceptor. Genetic studies with menaquinone and fluoroacetate-resistant mutants. J Gen Microbiol 1979, 115:259-271. 10.1099/00221287-115-2-259, 393800.
33. Hayaishi O, Kornberg A. Metabolism of cytosine, thymine, uracil, and barbituric acid by bacterial enzymes. J Biol Chem 1952, 197:717-732.
34. Castañeda-García A, Do TT, Blazquez J. The K + uptake regulator TrkA controls membrane potential, pH homeostasis and multidrug susceptibility in Mycobacterium smegmatis. J Antimicrob Chemother 2011, 66:1489-1498. 10.1093/jac/dkr165, 21613307.
35. Mycobacterial Protocols 1998, New Jersey: Humana Press, Parish T, Stoker NG.
36. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article3.
37. Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci USA 2003, 100:9440-9445. 10.1073/pnas.1530509100, 170937, 12883005.
38. Ideker T, Ozier O, Schwikowski B, Siegel AF. Discovering regulatory and signalling circuits in molecular interaction networks. Bioinformatics 2002, 18(Suppl 1):S233-S240. 10.1093/bioinformatics/18.suppl_1.S233, 12169552.