Search for novel targets of the PII signal transduction protein in Bacteria identifies the BCCP component of acetyl-CoA carboxylase as a PII binding partner

Molecular Microbiology

Volumn 91, Issue 4, 2014, Pages 751-761

  Rodrigues, Thiago E ^a   Gerhardt, Edileusa C M ^a   Oliveira, Marco A ^a   Chubatsu, Leda S ^a   Pedrosa, Fabio O ^a   Souza, Emanuel M ^a   Souza, Gustavo A ^b   Müller Santos, Marcelo ^a   Huergo, Luciano F ^a  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOGLUTARIC ACID; ACETYL COENZYME A CARBOXYLASE; ADENOSINE TRIPHOSPHATE; ALPHA-KETOGLUTARIC ACID; BACTERIAL PROTEIN; BIOTIN CARBOXYL CARRIER PROTEIN; FATTY ACID SYNTHASE; NITROGEN REGULATORY PROTEIN; PIID REGULATORY PROTEIN, BACTERIA; PROTEIN BINDING;

ARABIDOPSIS; AZOSPIRILLUM BRASILENSE; ENZYMOLOGY; ESCHERICHIA COLI; METABOLISM; PROTEIN ANALYSIS;

ACETYL-COA CARBOXYLASE; ADENOSINE TRIPHOSPHATE; ARABIDOPSIS; AZOSPIRILLUM BRASILENSE; BACTERIAL PROTEINS; ESCHERICHIA COLI; FATTY ACID SYNTHASE, TYPE II; KETOGLUTARIC ACIDS; PII NITROGEN REGULATORY PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING;

EID: 84893801140     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12493     Document Type: Article

References (64)

1. Alves, J., Westling, L., Peters, E.C., Harris, J.L., and Trauger, J.W. (2011) Cloning, expression, and enzymatic activity of Acinetobacter baumannii and Klebsiella pneumoniae acetyl-coenzyme A carboxylases. Anal Biochem 417: 103-111.
2. Araujo, L.M., Huergo, L.F., Invitti, A.L., Gimenes, C.I., Bonatto, A.C., Monteiro, R.A., etal. (2008) Different responses of the GlnB and GlnZ proteins upon in vitro uridylylation by the Azospirillum brasilense GlnD protein. Braz J Med Biol Res 41: 289-294.
3. Araujo, M.S., Baura, V.A., Souza, E.M., Benelli, E.M., Rigo, L.U., Steffens, M.B., etal. (2004) In vitro uridylylation of the Azospirillum brasilense N-signal transducing GlnZ protein. Protein Expr Purif 33: 19-24.
4. Athappilly, F.K., and Hendrickson, W.A. (1995) Structure of the biotinyl domain of acetyl-coenzyme A carboxylase determined by MAD phasing. Structure 3: 1407-1419.
5. Bokinsky, G., Peralta-Yahya, P.P., George, A., Holmes, B.M., Steen, E.J., Dietrich, J., etal. (2011) Synthesis of three advanced biofuels from ionic liquid-pretreated switchgrass using engineered Escherichia coli. Proc Natl Acad Sci U S A 108: 19949-19954.
6. Bonatto, A.C., Couto, G.H., Souza, E.M., Araujo, L.M., Pedrosa, F.O., Noindorf, L., and Benelli, E.M. (2007) Purification and characterization of the bifunctional uridylyltransferase and the signal transducing proteins GlnB and GlnK from Herbaspirillum seropedicae. Protein Expr Purif 55: 293-299.
7. Broussard, T.C., Kobe, M.J., Pakhomova, S., Neau, D.B., Price, A.E., Champion, T.S., and Waldrop, G.L. (2013) The three-dimensional structure of the biotin carboxylase-biotin carboxyl carrier protein complex of E.coli acetyl-CoA carboxylase. Structure 21: 650-657.
8. Burillo, S., Luque, I., Fuentes, I., and Contreras, A. (2004) Interactions between the nitrogen signal transduction protein PII and N-acetyl glutamate kinase in organisms that perform oxygenic photosynthesis. J Bacteriol 186: 3346-3354.
9. Castellen, P., Rego, F.G., Portugal, M.E., and Benelli, E.M. (2011) The Streptococcus mutans GlnR protein exhibits an increased affinity for the glnRA operon promoter when bound to GlnK. Braz J Med Biol Res 44: 1202-1208.
10. Chapman-Smith, A., Turner, D.L., Cronan, J.E., Jr, Morris, T.W., and Wallace, J.C. (1994) Expression, biotinylation and purification of a biotin-domain peptide from the biotin carboxy carrier protein of Escherichia coli acetyl-CoA carboxylase. Biochem J 302 (Part 3): 881-887.
11. Choi-Rhee, E., and Cronan, J.E. (2003) The biotin carboxylase-biotin carboxyl carrier protein complex of Escherichia coli acetyl-CoA carboxylase. J Biol Chem 278: 30806-30812.
12. Conroy, M.J., Durand, A., Lupo, D., Li, X.D., Bullough, P.A., Winkler, F.K., and Merrick, M. (2007) The crystal structure of the Escherichia coli AmtB-GlnK complex reveals how GlnK regulates the ammonia channel. Proc Natl Acad Sci U S A 104: 1213-1218.
13. Cronan, J.E., Jr, and Waldrop, G.L. (2002) Multi-subunit acetyl-CoA carboxylases. Prog Lipid Res 41: 407-435.
14. Davis, M.S., and Cronan, J.E., Jr (2001) Inhibition of Escherichia coli acetyl coenzyme A carboxylase by acyl-acyl carrier protein. J Bacteriol 183: 1499-1503.
15. Dixon, R., and Kahn, D. (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2: 621-631.
16. Dodsworth, J.A., and Leigh, J.A. (2006) Regulation of nitrogenase by 2-oxoglutarate-reversible, direct binding of a PII-like nitrogen sensor protein to dinitrogenase. Proc Natl Acad Sci U S A 103: 9779-9784.
17. Dodsworth, J.A., Cady, N.C., and Leigh, J.A. (2005) 2-Oxoglutarate and the PII homologues NifI1 and NifI2 regulate nitrogenase activity in cell extracts of Methanococcus maripaludis. Mol Microbiol 56: 1527-1538.
18. Ehlers, C., Weidenbach, K., Veit, K., Forchhammer, K., and Schmitz, R.A. (2005) Unique mechanistic features of post-translational regulation of glutamine synthetase activity in Methanosarcina mazei strain Go1 in response to nitrogen availability. Mol Microbiol 55: 1841-1854.
19. Feria Bourrellier, A.B., Valot, B., Guillot, A., Ambard-Bretteville, F., Vidal, J., and Hodges, M. (2010a) Chloroplast acetyl-CoA carboxylase activity is 2-oxoglutarate-regulated by interaction of PII with the biotin carboxyl carrier subunit. Proc Natl Acad Sci U S A 107: 502-507.
20. Feria Bourrellier, A.B., Valot, B., Guillot, A., Ambard-Bretteville, F., Vidal, J., and Hodges, M. (2010b) Chloroplast acetyl-CoA carboxylase activity is 2-oxoglutarate-regulated by interaction of PII with the biotin carboxyl carrier subunit. Proc Natl Acad Sci U S A 107: 502-507.
21. Fokina, O., Chellamuthu, V.R., Forchhammer, K., and Zeth, K. (2010) Mechanism of 2-oxoglutarate signaling by the Synechococcus elongatus PII signal transduction protein. Proc Natl Acad Sci U S A 107: 19760-19765.
22. Fokina, O., Herrmann, C., and Forchhammer, K. (2011) Signal-transduction protein PII from Synechococcus elongatus PCC 7942 senses low adenylate energy charge in vitro. Biochem J 440: 147-156.
23. Forchhammer, K. (2008) P(II) signal transducers: novel functional and structural insights. Trends Microbiol 16: 65-77.
24. Gerhardt, E.C., Araujo, L.M., Ribeiro, R.R., Chubatsu, L.S., Scarduelli, M., Rodrigues, T.E., etal. (2012) Influence of the ADP/ATP ratio, 2-oxoglutarate and divalent ions on Azospirillum brasilense PII protein signalling. Microbiology 158: 1656-1663.
25. Heinrich, A., Maheswaran, M., Ruppert, U., and Forchhammer, K. (2004) The Synechococcus elongatus PII signal transduction protein controls arginine synthesis by complex formation with N-acetyl-l-glutamate kinase. Mol Microbiol 52: 1303-1314.
26. Heinrich, A., Woyda, K., Brauburger, K., Meiss, G., Detsch, C., Stulke, J., and Forchhammer, K. (2006) Interaction of the membrane-bound GlnK-AmtB complex with the master regulator of nitrogen metabolism TnrA in Bacillus subtilis. J Biol Chem 281: 34909-34917.
27. Howard, T.P., Middelhaufe, S., Moore, K., Edner, C., Kolak, D.M., Taylor, G.N., etal. (2013) Synthesis of customized petroleum-replica fuel molecules by targeted modification of free fatty acid pools in Escherichia coli. Proc Natl Acad Sci U S A 110: 7636-7641.
28. Huergo, L.F., Souza, E.M., Araujo, M.S., Pedrosa, F.O., Chubatsu, L.S., Steffens, M.B., and Merrick, M. (2006) ADP-ribosylation of dinitrogenase reductase in Azospirillum brasilense is regulated by AmtB-dependent membrane sequestration of DraG. Mol Microbiol 59: 326-337.
29. Huergo, L.F., Merrick, M., Pedrosa, F.O., Chubatsu, L.S., Araujo, L.M., and Souza, E.M. (2007) Ternary complex formation between AmtB, GlnZ and the nitrogenase regulatory enzyme DraG reveals a novel facet of nitrogen regulation in bacteria. Mol Microbiol 66: 1523-1535.
30. Huergo, L.F., Noindorf, L., Gimenes, C., Lemgruber, R.S.P., Cordellini, D.F., Falarz, L.J., etal. (2010) Proteomic analysis of Herbaspirillum seropedicae reveals ammonium-induced AmtB-dependent membrane sequestration of PII proteins. FEMS Microbiol Lett 308: 40-47.
31. Huergo, L.F., Pedrosa, F.O., Muller-Santos, M., Chubatsu, L.S., Monteiro, R.A., Merrick, M., and Souza, E.M. (2012) PII signal transduction proteins: pivotal players in post-translational control of nitrogenase activity. Microbiology 158: 176-190.
32. Huergo, L.F., Chandra, G., and Merrick, M. (2013) P(II) signal transduction proteins: nitrogen regulation and beyond. FEMS Microbiol Rev 37: 251-283.
33. Huerlimann, R., and Heimann, K. (2013) Comprehensive guide to acetyl-carboxylases in algae. Crit Rev Biotechnol 33: 49-65.
34. James, E.S., and Cronan, J.E. (2004) Expression of two Escherichia coli acetyl-CoA carboxylase subunits is autoregulated. J Biol Chem 279: 2520-2527.
35. Javelle, A., Severi, E., Thornton, J., and Merrick, M. (2004) Ammonium sensing in Escherichia coli. Role of the ammonium transporter AmtB and AmtB-GlnK complex formation. J Biol Chem 279: 8530-8538.
36. Jiang, P., and Ninfa, A.J. (1999) Regulation of autophosphorylation of Escherichia coli nitrogen regulator II by the PII signal transduction protein. J Bacteriol 181: 1906-1911.
37. Jiang, P., and Ninfa, A.J. (2007) Escherichia coli PII signal transduction protein controlling nitrogen assimilation acts as a sensor of adenylate energy charge in vitro. Biochemistry 46: 12979-12996.
38. Jiang, P., and Ninfa, A.J. (2009) Sensation and signaling of alpha-ketoglutarate and adenylylate energy charge by the Escherichia coli PII signal transduction protein require cooperation of the three ligand-binding sites within the PII trimer. Biochemistry 48: 11522-11531.
39. Jiang, P., Peliska, J.A., and Ninfa, A.J. (1998) Enzymological characterization of the signal-transducing uridylyltransferase/uridylyl-removing enzyme (EC 2.7.7.59) of Escherichia coli and its interaction with the PII protein. Biochemistry 37: 12782-12794.
40. Jiang, P., Pioszak, A.A., and Ninfa, A.J. (2007) Structure-function analysis of glutamine synthetase adenylyltransferase (ATase, EC 2.7.7.49) of Escherichia coli. Biochemistry 46: 4117-4132.
41. Kamberov, E.S., Atkinson, M.R., and Ninfa, A.J. (1995) The Escherichia coli PII signal transduction protein is activated upon binding 2-ketoglutarate and ATP. J Biol Chem 270: 17797-17807.
42. Lennen, R.M., and Pfleger, B.F. (2012) Engineering Escherichia coli to synthesize free fatty acids. Trends Biotechnol 30: 659-667.
43. Llacer, J.L., Espinosa, J., Castells, M.A., Contreras, A., Forchhammer, K., and Rubio, V. (2010) Structural basis for the regulation of NtcA-dependent transcription by proteins PipX and PII. Proc Natl Acad Sci U S A 107: 15397-15402.
44. Machado, H.B., Funayama, S., Rigo, L.U., and Pedrosa, F.O. (1991) Excretion of ammonium by Azospirillum brasilense mutants resistant to ethylenediamine. Can J Microbiol 37: 549-553.
45. Maier, S., Schleberger, P., Lu, W., Wacker, T., Pfluger, T., Litz, C., and Andrade, S.L. (2011) Mechanism of disruption of the Amt-GlnK complex by P(II)-mediated sensing of 2-oxoglutarate. PLoS ONE 6: e26327.
46. Moure, V.R., Razzera, G., Araujo, L.M., Oliveira, M.A., Gerhardt, E.C., Muller-Santos, M., etal. (2012) Heat stability of proteobacterial PII protein facilitate purification using a single chromatography step. Protein Expr Purif 81: 83-88.
47. Nolden, L., Ngouoto-Nkili, C.E., Bendt, A.K., Kramer, R., and Burkovski, A. (2001) Sensing nitrogen limitation in Corynebacterium glutamicum: the role of glnK and glnD. Mol Microbiol 42: 1281-1295.
48. Pedrosa, F.O., and Yates, M.G. (1987) Regulation of nitrogen fixation (nif) genes of Azospirillum brasilense by nifA and ntrC (glnG) type genes. FEMS Microbiol Lett 55: 95-101.
49. Radchenko, M.V., Thornton, J., and Merrick, M. (2010) Control of AmtB-GlnK complex formation by intracellular levels of ATP, ADP, and 2-oxoglutarate. J Biol Chem 285: 31037-31045.
50. Radchenko, M.V., Thornton, J., and Merrick, M. (2013) PII signal transduction proteins are ATPases whose activity is regulated by 2-oxoglutarate. Proc Natl Acad Sci U S A 110: 12948-12953.
51. Roberts, E.L., Shu, N., Howard, M.J., Broadhurst, R.W., Chapman-Smith, A., Wallace, J.C., etal. (1999) Solution structures of apo and holo biotinyl domains from acetyl coenzyme A carboxylase of Escherichia coli determined by triple-resonance nuclear magnetic resonance spectroscopy. Biochemistry 38: 5045-5053.
52. da Rocha, R.A., Weschenfelder, T.A., de Castilhos, F., de Souza, E.M., Huergo, L.F., and Mitchell, D.A. (2013) Mathematical model of the binding of allosteric effectors to the Escherichia coli PII signal transduction protein GlnB. Biochemistry 52: 2683-2693.
53. Sarkar, A., Kohler, J., Hurek, T., and Reinhold-Hurek, B. (2012) A novel regulatory role of the Rnf complex of Azoarcus sp. strain BH72. Mol Microbiol 83: 408-422.
54. Schirmer, A., Rude, M.A., Li, X., Popova, E., and del Cardayre, S.B. (2010) Microbial biosynthesis of alkanes. Science 329: 559-562.
55. Smith, C.S., Weljie, A.M., and Moorhead, G.B. (2003) Molecular properties of the putative nitrogen sensor PII from Arabidopsis thaliana. Plant J 33: 353-360.
56. Soriano, A., Radice, A.D., Herbitter, A.H., Langsdorf, E.F., Stafford, J.M., Chan, S., etal. (2006) Escherichia coli acetyl-coenzyme A carboxylase: characterization and development of a high-throughput assay. Anal Biochem 349: 268-276.
57. Truan, D., Huergo, L.F., Chubatsu, L.S., Merrick, M., Li, X.D., and Winkler, F.K. (2010) A new P(II) protein structure identifies the 2-oxoglutarate binding site. J Mol Biol 400: 531-539.
58. Wisniewski-Dye, F., Borziak, K., Khalsa-Moyers, G., Alexandre, G., Sukharnikov, L.O., Wuichet, K., etal. (2011) Azospirillum genomes reveal transition of bacteria from aquatic to terrestrial environments. PLoS Genet 7: e1002430.
59. Xu, Y., Cheah, E., Carr, P.D., van Heeswijk, W.C., Westerhoff, H.V., Vasudevan, S.G., and Ollis, D.L. (1998) GlnK, a PII-homologue: structure reveals ATP binding site and indicates how the T-loops may be involved in molecular recognition. J Mol Biol 282: 149-165.
60. Yan, D., Lenz, P., and Hwa, T. (2011) Overcoming fluctuation and leakage problems in the quantification of intracellular 2-oxoglutarate levels in Escherichia coli. Appl Environ Microbiol 77: 6763-6771.
61. You, C., Okano, H., Hui, S., Zhang, Z., Kim, M., Gunderson, C.W., etal. (2013) Coordination of bacterial proteome with metabolism by cyclic AMP signalling. Nature 500: 301-306.
62. Yuan, J., Doucette, C.D., Fowler, W.U., Feng, X.J., Piazza, M., Rabitz, H.A., etal. (2009) Metabolomics-driven quantitative analysis of ammonia assimilation in E.coli. Mol Syst Biol 5: 302.
63. de Zamaroczy, M. (1998) Structural homologues PII and PZ of Azospirillum brasilense provide intracellular signalling for selective regulation of various nitrogen-dependent functions. Mol Microbiol 29: 449-463.
64. Zhang, C., Wei, Z.H., and Ye, B.C. (2013) Quantitative monitoring of 2-oxoglutarate in Escherichia coli cells by a fluorescence resonance energy transfer-based biosensor. Appl Microbiol Biotechnol 97: 8307-8316.