IpsA, a novel LacI-type regulator, is required for inositol-derived lipid formation in Corynebacteria and Mycobacteria

BMC Biology

Volumn 11, Issue , 2013, Pages

  Baumgart, Meike ^a   Luder, Kerstin ^a   Grover, Shipra ^b   Gätgens, Cornelia ^a   Besra, Gurdyal S ^b   Frunzke, Julia ^a  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Cell wall synthesis; Corynebacterium diphtheriae; Corynebacterium glutamicum; Inositol; LAM; LM; Mycobacterium tuberculosis; Mycolic acids; Mycothiol; Transcriptional regulator

Indexed keywords

CORYNEBACTERIACEAE; CORYNEBACTERINEAE; CORYNEBACTERIUM; CORYNEBACTERIUM DIPHTHERIAE; CORYNEBACTERIUM GLUTAMICUM; IPSA; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS;

BACTERIAL DNA; INOSITOL; LAC REPRESSOR; LIPID;

ARTICLE; BACTERIAL GENE; BIOSYNTHESIS; CELL WALL; CORYNEBACTERIUM GLUTAMICUM; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; LIPID METABOLISM; METABOLISM; MYCOBACTERIUM TUBERCULOSIS; PHENOTYPE; PROMOTER REGION;

CELL WALL; CORYNEBACTERIUM GLUTAMICUM; DNA, BACTERIAL; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; INOSITOL; LAC REPRESSORS; LIPID METABOLISM; LIPIDS; MYCOBACTERIUM TUBERCULOSIS; PHENOTYPE; PROMOTER REGIONS, GENETIC;

EID: 84891350474     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-11-122     Document Type: Article

References (50)

1. Mishra AK, Driessen NN, Appelmelk BJ, Besra GS. Lipoarabinomannan and related glycoconjugates: structure, biogenesis and role in Mycobacterium tuberculosis physiology and host-pathogen interaction. FEMS Microbiol Rev 2011, 35:1126-1157. 10.1111/j.1574-6976.2011.00276.x, 3229680, 21521247.
2. Eggeling L, Besra GS, Alderwick L. Structure and synthesis of the cell wall. Corynebacteria: genomics and molecular biology 2008, 267-294. Wymondham, UK: Caister Academic Press, Burkovski A.
3. Fahey RC. Glutathione analogs in prokaryotes. Biochim Biophys Acta 1830, 2013:3182-3198.
4. Morita YS, Fukuda T, Sena CBC, Yamaryo-Botte Y, McConville MJ, Kinoshita T. Inositol lipid metabolism in mycobacteria: biosynthesis and regulatory mechanisms. Biochim Biophys Acta 1810, 2011:630-641.
5. http://www.microbesonline.org.
6. Alm EJ, Huang KH, Price MN, Koche RP, Keller K, Dubchak IL, Arkin AP. The MicrobesOnline web site for comparative genomics. Genome Res 2005, 15:1015-1022. 10.1101/gr.3844805, 1172046, 15998914.
7. Bachhawat N, Mande SC. Identification of the INO1 gene of Mycobacterium tuberculosis H37Rv reveals a novel class of inositol-1-phosphate synthase enzyme. J Mol Biol 1999, 291:531-536. 10.1006/jmbi.1999.2980, 10448034.
8. Nigou J, Besra GS. Characterization and regulation of inositol monophosphatase activity in Mycobacterium smegmatis. Biochem J 2002, 361:385-390. 1222319, 11772411.
9. Movahedzadeh F, Wheeler PR, Dinadayala P, Av-Gay Y, Parish T, Daffe M, Stoker NG. Inositol monophosphate phosphatase genes of Mycobacterium tuberculosis. BMC Microbiol 2010, 10:50. 10.1186/1471-2180-10-50, 2834668, 20167072.
10. Movahedzadeh F, Smith DA, Norman RA, Dinadayala P, Murray-Rust J, Russell DG, Kendall SL, Rison SC, McAlister MS, Bancroft GJ, McDonald NQ, Daffe M, Av-Gay Y, Stoker NG. The Mycobacterium tuberculosis ino1 gene is essential for growth and virulence. Mol Microbiol 2004, 51:1003-1014. 10.1046/j.1365-2958.2003.03900.x, 14763976.
11. Jackson M, Crick DC, Brennan PJ. Phosphatidylinositol is an essential phospholipid of mycobacteria. J Biol Chem 2000, 275:30092-30099.
12. Haites RE, Morita YS, McConville MJ, Jacobe HB. Function of phosphatidylinositol in mycobacteria. J Biol Chem 2005, 280:10981-10987. 10.1074/jbc.M413443200, 15634688.
13. Hernick M. Mycothiol: a target for potentiation of rifampin and other antibiotics against Mycobacterium tuberculosis. Expert Rev Anti Infect Ther 2013, 11:49-67. 10.1586/eri.12.152, 23428102.
14. Krings E, Krumbach K, Bathe B, Kelle R, Wendisch VF, Sahm H, Eggeling L. Characterization of myo-inositol utilization by Corynebacterium glutamicum: the stimulon, identification of transporters, and influence on L-lysine formation. J Bacteriol 2006, 188:8054-8061. 10.1128/JB.00935-06, 1698185, 16997948.
15. Klaffl S, Brocker M, Kalinowski J, Eikmanns B, Bott M. Complex regulation of the PEP carboxykinase gene pck and characterization of its GntR-type regulator IolR as a repressor of myo-inositol utilization genes in Corynebacterium glutamicum. J Bacteriol 2013, 195:4283-4296. 10.1128/JB.00265-13, 23873914.
16. Swint-Kruse L, Matthews KS. Allostery in the Lacl/GaIR family: variations on a theme. Curr Opin Microbiol 2009, 12:129-137. 10.1016/j.mib.2009.01.009, 2688824, 19269243.
17. http://www.ncbi.nlm.nih.gov/geo.
18. Wennerhold J, Bott M. The DtxR regulon of Corynebacterium glutamicum. J Bacteriol 2006, 188:2907-2918. 10.1128/JB.188.8.2907-2918.2006, 1446976, 16585752.
19. Wennerhold J, Krug A, Bott M. The AraC-type regulator RipA represses aconitase and other iron proteins from Corynebacterium under iron limitation and is itself repressed by DtxR. J Biol Chem 2005, 280:40500-40508. 10.1074/jbc.M508693200, 16179344.
20. Bailey TL, Elkan C. " Fitting a mixture model by expectation maximization to discover motifs in biopolymers" , Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology 1994, 28-36. Menlo Park, Ca: AAAI Press.
21. Feng J, Che YS, Milse J, Yin YJ, Liu L, Rückert C, Shen XH, Qi SW, Kalinowski J, Liu SJ. The gene ncgl2918 encodes a novel maleylpyruvate isomerase that needs mycothiol as cofactor and links mycothiol biosynthesis and gentisate assimilation in Corynebacterium glutamicum. J Biol Chem 2006, 281:10778-10785. 10.1074/jbc.M513192200, 16481315.
22. Tatituri RV, Illarionov PA, Dover LG, Nigou J, Gilleron M, Hitchen P, Krumbach K, Morris HR, Spencer N, Dell A, Eggeling L, Besra GS. Inactivation of Corynebacterium glutamicum NCgl0452 and the role of MgtA in the biosynthesis of a novel mannosylated glycolipid involved in lipomannan biosynthesis. J Biol Chem 2007, 282:4561-4572.
23. Mishra AK, Klein C, Gurcha SS, Alderwick LJ, Babu P, Hitchen PG, Morris HR, Dell A, Besra GS, Eggeling L. Structural characterization and functional properties of a novel lipomannan variant isolated from a Corynebacterium glutamicum pimB′ mutant. Antonie Van Leeuwenhoek 2008, 94:277-287. 10.1007/s10482-008-9243-1, 2480597, 18421567.
24. Mishra AK, Batt S, Krumbach K, Eggeling L, Besra GS. Characterization of the Corynebacterium glutamicum ΔpimB′ ΔmgtA double deletion mutant and the role of Mycobacterium tuberculosis orthologues Rv2188c and Rv0557 in glycolipid biosynthesis. J Bacteriol 2009, 191:4465-4472. 10.1128/JB.01729-08, 2698491, 19395496.
25. Vilchèze C, Av-Gay Y, Attarian R, Liu Z, Hazbón MH, Colangeli R, Chen B, Liu W, Alland D, Sacchettini JC, Jacobs WR. Mycothiol biosynthesis is essential for ethionamide susceptibility in Mycobacterium tuberculosis. Mol Microbiol 2008, 69:1316-1329. 10.1111/j.1365-2958.2008.06365.x, 2628429, 18651841.
26. Turner BL, Paphazy MJ, Haygarth PM, McKelvie ID. Inositol phosphates in the environment. Philos T Roy Soc B 2002, 357:449-469.
27. Schröder J, Jochmann N, Rodionov DA, Tauch A. The Zur regulon of Corynebacterium glutamicum ATCC 13032. BMC Genomics 2010, 11:12. 10.1186/1471-2164-11-12, 2823685, 20055984.
28. Tropis M, Meniche X, Wolf A, Gebhardt H, Strelkov S, Chami M, Schomburg D, Kramer R, Morbach S, Daffe M. The crucial role of trehalose and structurally related oligosaccharides in the biosynthesis and transfer of mycolic acids in corynebacterineae. J Biol Chem 2005, 280:26573-26585. 10.1074/jbc.M502104200, 15901732.
29. Murphy HN, Stewart GR, Mischenko VV, Apt AS, Harris R, McAlister MSB, Driscoll PC, Young DB, Robertson BD. The OtsAB pathway is essential for trehalose biosynthesis in Mycobacterium tuberculosis. J Biol Chem 2005, 280:14524-14529. 10.1074/jbc.M414232200, 15703182.
30. Norman RA, McAlister MSB, Murray-Rust J, Movahedzadeh F, Stoker NG, McDonald NQ. Crystal structure of inositol 1-phosphate synthase from Mycobacterium tuberculosis, a key enzyme in phosphatidylinositol synthesis. Structure 2002, 10:393-402. 10.1016/S0969-2126(02)00718-9, 12005437.
31. Roback P, Beard J, Baumann D, Gille C, Henry K, Krohn S, Wiste H, Voskuil MI, Rainville C, Rutherford R. A predicted operon map for Mycobacterium tuberculosis. Nucleic Acids Res 2007, 35:5085-5095. 10.1093/nar/gkm518, 1976454, 17652327.
32. Bell CE, Lewis M. The Lac repressor: a second generation of structural and functional studies. Curr Opin Struct Biol 2001, 11:19-25. 10.1016/S0959-440X(00)00180-9, 11179887.
33. Camas FM, Alm EJ, Poyatos JF. Local gene regulation details a recognition code within the LacI transcriptional factor family. PLoS Comput Biol 2010, 6:11.
34. Belisle JT, Vissa VD, Sievert T, Takayama K, Brennan PJ, Besra GS. Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis. Science 1997, 276:1420-1422. 10.1126/science.276.5317.1420, 9162010.
35. Keilhauer C, Eggeling L, Sahm H. Isoleucine synthesis in Corynebacterium glutamicum - Molecular analysis of the Ilvb-Ilvn-Ilvc Operon. J Bacteriol 1993, 175:5595-5603. 206616, 8366043.
36. Sambrook J, Russell DW. Molecular cloning: A Laboratory Manual 2001, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 3.
37. Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol 1983, 166:557-580. 10.1016/S0022-2836(83)80284-8, 6345791.
38. van der Rest ME, Lange C, Molenaar D. A heat shock following electroporation induces highly efficient transformation of Corynebacterium glutamicum with xenogeneic plasmid DNA. Appl Microbiol Biotechnol 1999, 52:541-545. 10.1007/s002530051557, 10570802.
39. Niebisch A, Bott M. Molecular analysis of the cytochrome bc1-aa3 branch of the Corynebacterium glutamicum respiratory chain containing an unusual diheme cytochrome c1. Arch Microbiol 2001, 175:282-294. 10.1007/s002030100262, 11382224.
40. Möker N, Brocker M, Schaffer S, Krämer R, Morbach S, Bott M. Deletion of the genes encoding the MtrA-MtrB two-component system of Corynebacterium glutamicum has a strong influence on cell morphology, antibiotics susceptibility and expression of genes involved in osmoprotection. Mol Microbiol 2004, 54:420-438. 10.1111/j.1365-2958.2004.04249.x, 15469514.
41. Lange C, Rittmann D, Wendisch VF, Bott M, Sahm H. Global expression profiling and physiological characterization of Corynebacterium glutamicum grown in the presence of L-valine. Appl Environ Microbiol 2003, 69:2521-2532. 10.1128/AEM.69.5.2521-2532.2003, 154540, 12732517.
42. Smyth GK. Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions Using R and Bioconductor 2005, 397-420. New York, NY: Springer, Gentleman R, Carey VJ, Huber W, Irizarry RA, Dudoit S.
43. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30(1):207-210. 10.1093/nar/30.1.207, 99122, 11752295.
44. Garcia-Nafria J, Baumgart M, Bott M, Wilkinson AJ, Wilson KS. The Corynebacterium glutamicum aconitase repressor: scratching around for crystals. Acta Crystallogr Sect F Struct Biol Cryst Commun 2010, 66:1074-1077. 10.1107/S1744309110029015, 2935231, 20823530.
45. Niebisch A, Kabus A, Schultz C, Weil B, Bott M. Corynebacterial protein kinase G controls 2-oxoglutarate dehydrogenase activity via the phosphorylation status of the OdhI protein. J Biol Chem 2006, 281:12300-12307. 10.1074/jbc.M512515200, 16522631.
46. Heyer A, Gätgens C, Hentschel E, Kalinowski J, Bott M, Frunzke J. The two-component system ChrSA is crucial for haem tolerance and interferes with HrrSA in haem-dependent gene regulation in Corynebacterium glutamicum. Microbiology 2012, 158:3020-3031. 10.1099/mic.0.062638-0, 23038807.
47. Garcia-Nafria J, Baumgart M, Turkenburg JP, Wilkinson AJ, Bott M, Wilson KS. Crystal and solution studies reveal that the transcriptional regulator AcnR of Corynebacterium glutamicum is regulated by Citrate-Mg2+ binding to a non-canonical pocket. J Biol Chem 2013, 288:15800-15812. 10.1074/jbc.M113.462440, 23589369.
48. Anderberg SJ, Newton GL, Fahey RC. Mycothiol biosynthesis and metabolism - Cellular levels of potential intermediates in the biosynthesis and degradation of mycothiol in Mycobacterium smegmatis. J Biol Chem 1998, 273:30391-30397. 10.1074/jbc.273.46.30391, 9804803.
49. Dobson G, Minnikin DE, Minnikin SM, Parlett JH, Goodfellow M, Ridell M, Magnusson M. Systematic analysis of complex mycobacterial lipids. Chemical Methods in Bacterial Systematics, Volume 1 1985, 237-265. London, UK: Academic Press, M. G, E. MD.
50. Ludwiczak P, Brando T, Monsarrat B, Puzo G. Structural characterization of Mycobacterium tuberculosis lipoarabinomannans by the combination of capillary electrophoresis and matrix-assisted laser desorption/ionization time of-flight mass spectrometry. Anal Chem 2001, 73:2323-2330. 10.1021/ac001368h, 11393859.