The EutQ and EutP proteins are novel acetate kinases involved in ethanolamine catabolism: Physiological implications for the function of the ethanolamine metabolosome in Salmonella enterica

Molecular Microbiology

Volumn 99, Issue 3, 2016, Pages 497-511

  Moore, Theodore C ^a,b   Escalante Semerena, Jorge C ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETALDEHYDE; ACETATE KINASE; ACETIC ACID; ACETYLPHOSPHATE; ADENOSINE DIPHOSPHATE; ETHANOLAMINE; EUTP PROTEIN; EUTQ PROTEIN; MAGNESIUM ION; PANTOTHENIC ACID; PHOSPHATE; PHOSPHATE ACETYLTRANSFERASE; TETRATHIONIC ACID; UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CATABOLISM; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SUBSTRATE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA; CHEMISTRY; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; KINETICS; METABOLISM; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM;

ACETATE KINASE; BACTERIAL PROTEINS; ETHANOLAMINE; KINETICS; SALMONELLA TYPHIMURIUM;

EID: 84956572661     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13243     Document Type: Article

References (67)

1. Aaron, M., Charbon, G., Lam, H., Schwarz, H., Vollmer, W., and Jacobs-Wagner, C. (2007) The tubulin homologue FtsZ contributes to cell elongation by guiding cell wall precursor synthesis in Caulobacter crescentus. Mol Microbiol 64: 938-952.
2. Balch, W.E., and Wolfe, R.S. (1976) New approach to the cultivation of methanogenic bacteria: 2-mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressurized atmosphere. Appl Environ Microbiol 32: 781-791.
3. Barrett, E.L., and Clark, M.A. (1987) Tetrathionate reduction and production of hydrogen sulfide from thiosulfate. Microbiol Rev 51: 192-205.
4. Baumler, A.J., Winter, S.E., Thiennimitr, P., and Casadesus, J. (2011) Intestinal and chronic infections: Salmonella lifestyles in hostile environments. Environ Microbiol Rep 3: 508-517.
5. Bergmeyer, J., Grassl, M., and Berger, R. (1984) Principles of enzymatic analysis. In Methods of Enzymatic Analysis. Bergmeyer, H.U. (ed.). Weinheim/Bergstrasse: Verlag Chemie, pp. 139-141.
6. Berkowitz, D., Hushon, J.M., Whitfield, H.J., Jr, Roth, J., and Ames, B.N. (1968) Procedure for identifying nonsense mutations. J Bacteriol 96: 215-220.
7. Blommel, P.G., and Fox, B.G. (2007) A combined approach to improving large-scale production of tobacco etch virus protease. Protein Expr Purif 55: 53-68.
8. Bobik, T.A. (2006) Polyhedral organelles compartmenting bacterial metabolic processes. Appl Microbiol Biotechnol 70: 517-525.
9. 12-dependent 1, 2-propanediol degradation. J Bacteriol 181: 5967-5975.
10. Bock, J.L. (1980) The binding of metal ions to ATP: a proton and phosphorus nmr investigation of diamagnetic metal-ATP complexes. J Inorg Biochem 12: 119-310.
11. Brinsmade, S.R., and Escalante-Semerena, J.C. (2004) The eutD gene of Salmonella enterica encodes a protein with phosphotransacetylase enzyme activity. J Bacteriol 186: 1890-1892.
12. Brinsmade, S.R., Paldon, T., and Escalante-Semerena, J.C. (2005) Minimal functions and physiological conditions required for growth of Salmonella enterica on ethanolamine in the absence of the metabolosome. J Bacteriol 187: 8039-8046.
13. Buan, N.R., and Escalante-Semerena, J.C. (2006) Purification and initial biochemical characterization of ATP:Cob(I)alamin adenosyltransferase (EutT) enzyme of Salmonella enterica. J Biol Chem 281: 16971-16977.
14. Buan, N.R., Suh, S.J., and Escalante-Semerena, J.C. (2004) The eutT gene of Salmonella enterica encodes an oxygen-labile, metal-containing ATP:corrinoid adenosyltransferase enzyme. J Bacteriol 186: 5708-5714.
15. Burton, R.M., and Stadtman, E.R. (1953) The oxidation of acetaldehyde to acetyl coenzyme A. J Biol Chem 202: 873-890.
16. Chang, G.W., and Chang, J.T. (1975) Evidence for the B12-dependent enzyme ethanolamine deaminase in Salmonella. Nature 254: 150-151.
17. Cheng, S., Liu, Y., Crowley, C.S., Yeates, T.O., and Bobik, T.A. (2008) Bacterial microcompartments: their properties and paradoxes. Bioessays 30: 1084-1095.
18. Cheng, S., Fan, C., Sinha, S., and Bobik, T.A. (2012) The PduQ enzyme is an alcohol dehydrogenase used to recycle NAD+ internally within the Pdu microcompartment of Salmonella enterica. PLoS ONE 7: e47144.
19. Chittori, S., Savithri, H.S., and Murthy, M.R. (2012) Structural and mechanistic investigations on Salmonella typhimurium acetate kinase (AckA): identification of a putative ligand binding pocket at the dimeric interface. BMC Struct Biol 12: 24.
20. Chowdhury, C., Chun, S., Pang, A., Sawaya, M.R., Sinha, S., Yeates, T.O., and Bobik, T.A. (2015) Selective molecular transport through the protein shell of a bacterial microcompartment organelle. Proc Natl Acad Sci USA 112: 2990-2995.
21. Cotton, P.B. (1972) Non-dietary lipid in the intestinal lumen. Gut 13: 675-681.
22. Dunwell, J.M., Purvis, A., and Khuri, S. (2004) Cupins: the most functionally diverse protein superfamily? Phytochemistry 65: 7-17.
23. Escalante-Semerena, J.C., and Roth, J.R. (1987) Regulation of cobalamin biosynthetic operons in Salmonella typhimurium. J Bacteriol 169: 2251-2258.
24. Fahey, R.C., Brown, W.C., Adams, W.B., and Worsham, M.B. (1978) Occurrence of glutathione in bacteria. J Bacteriol 133: 1126-1129.
25. Fung, C.K., and Proulx, P. (1969) Metabolism of phosphoglycerides in E. coli. 3. The presence of phospholipase A. Can J Biochem 47: 371-373.
26. Gorrell, A., and Ferry, J.G. (2007) Investigation of the Methanosarcina thermophila acetate kinase mechanism by fluorescence quenching. Biochemistry 46: 14170-14176.
27. Gorrell, A., Lawrence, S.H., and Ferry, J.G. (2005) Structural and kinetic analyses of arginine residues in the active site of the acetate kinase from Methanosarcina thermophila. J Biol Chem 280: 10731-10742.
28. Guzman, L.M., Belin, D., Carson, M.J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
29. Held, M., Quin, M.B., and Schmidt-Dannert, C. (2013) Eut bacterial microcompartments: insights into their function, structure, and bioengineering applications. J Mol Microbiol Biotechnol 23: 308-320.
30. Hesslinger, C., Fairhurst, S.A., and Sawers, G. (1998) Novel keto acid formate-lyase and propionate kinase enzymes are components of an anaerobic pathway in Escherichia coli that degrades L- threonine to propionate. Mol Microbiol 27: 477-492.
31. Huseby, D.L., and Roth, J.R. (2013) Evidence that a metabolic microcompartment contains and recycles private cofactor pools. J Bacteriol 195: 2864-2879.
32. Ingram-Smith, C., Gorrell, A., Lawrence, S.H., Iyer, P., Smith, K., and Ferry, J.G. (2005) Characterization of the acetate binding pocket in the Methanosarcina thermophila acetate kinase. J Bacteriol 187: 2386-2394.
33. Johnson, C.L., Buszko, M.L., and Bobik, T.A. (2004) Purification and initial characterization of the Salmonella enterica PduO ATP:Cob(I)alamin adenosyltransferase. J Bacteriol 186: 7881-7887.
34. Kapralek, F. (1972) The physiological role of tetrathionate respiration in growing Citrobacter. J Gen Microbiol 71: 133-139.
35. Kofoid, E., Rappleye, C., Stojiljkovic, I., and Roth, J. (1999) The 17-gene ethanolamine (eut) operon of Salmonella typhimurium encodes five homologues of carboxysome shell proteins. J Bacteriol 181: 5317-5329.
36. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
37. Larson, T.J., Ehrmann, M., and Boos, W. (1983) Periplasmic glycerophosphodiester phosphodiesterase of Escherichia coli, a new enzyme of the glp regulon. J Biol Chem 258: 5428-5432.
38. Leal, N.A., Havemann, G.D., and Bobik, T.A. (2003) PduP is a coenzyme-A-acylating propionaldehyde dehydrogenase associated with the polyhedral bodies involved in B12-dependent 1, 2-propanediol degradation by Salmonella enterica serovar Typhimurium LT2. Arch Microbiol 180: 353-361.
39. Liu, Y., Jorda, J., Yeates, T.O., and Bobik, T.A. (2015) The PduL phosphotransacylase is used to recycle coenzyme A within the Pdu microcompartment. J Bacteriol 197: 2392-2399.
40. Maniatis, T., Fritsch, E.F., and Sambrook, J. (1982) Introduction of plasmid and bacteriophage lambda into Escherichia coli. In Molecular Cloning: A Laboratory Manual. Maniatis, T., Fritsch, E.F., and Sambrook, J. (eds). Cold Spring Harbor, New York.: Cold Spring Harbor Laboratory, pp. 250-251.
41. Mera, P.E., Maurice, M.S., Rayment, I., and Escalante-Semerena, J.C. (2007) Structural and functional analyses of the human-type corrinoid adenosyltransferase (PduO) from Lactobacillus reuteri. Biochemistry 46: 13829-13836.
42. Miles, R.D., Gorrell, A., and Ferry, J.G. (2002) Evidence for a transition state analog, MgADP-aluminum fluoride-acetate, in acetate kinase from Methanosarcina thermophila. J Biol Chem 277: 22547-22552.
43. Moore, T.C., Mera, P.E., and Escalante-Semerena, J.C. (2014) the EutT enzyme of Salmonella enterica is a unique ATP:Cob(I)alamin adenosyltransferase metalloprotein that requires ferrous ions for maximal activity. J Bacteriol 196: 903-910.
44. Mori, K., Bando, R., Hieda, N., and Toraya, T. (2004) Identification of a reactivating factor for adenosylcobalamin-dependent ethanolamine ammonia lyase. J Bacteriol 186: 6845-6854.
45. Palacios, S., V., Starai, J., and Escalante-Semerena, J.C. (2003) Propionyl coenzyme A is a common intermediate in the 1, 2-propanediol and propionate catabolic pathways needed for expression of the prpBCDE operon during growth of Salmonella enterica on 1, 2-propanediol. J Bacteriol 185: 2802-2810.
46. Penrod, J.T., and Roth, J.R. (2006) Conserving a volatile metabolite: a role for carboxysome-like organelles in Salmonella enterica. J Bacteriol 188: 2865-2874.
47. Pitts, A.C., Tuck, L.R., Faulds-Pain, A., Lewis, R.J., and Marles-Wright, J. (2012) Structural insight into the Clostridium difficile ethanolamine utilisation microcompartment. PLoS ONE 7: e48360.
48. Price-Carter, M., Tingey, J., Bobik, T.A., and Roth, J.R. (2001) The alternative electron acceptor tetrathionate supports B12-dependent anaerobic growth of Salmonella enterica serovar Typhimurium on ethanolamine or 1, 2-propanediol. J Bacteriol 183: 2463-2475.
49. Price-Carter, M., Fazzio, T.G., Vallbona, E.I., and Roth, J.R. (2005) Polyphosphate kinase protects Salmonella enterica from weak organic acid stress. J Bacteriol 187: 3088-3099.
50. Rocco, C.J., Dennison, K.L., Klenchin, V.A., Rayment, I., and Escalante-Semerena, J.C. (2008) Construction and use of new cloning vectors for the rapid isolation of recombinant proteins from Escherichia coli. Plasmid 59: 231-237.
51. Rondon, M.R., Kazmierczak, R., and Escalante-Semerena, J.C. (1995) Glutathione is required for maximal transcription of the cobalamin biosynthetic and 1, 2-propanediol utilization (cob/pdu) regulon and for the catabolism of ethanolamine, 1, 2-propanediol, and propionate in Salmonella typhimurium LT2. J Bacteriol 177: 5434-5439.
52. Roof, D.M., and Roth, J.R. (1988a) Ethanolamine utilization in Salmonella typhimurium. J Bacteriol 170: 3855-3863.
53. Roof, D.M., and Roth, J.R. (1988b) Ethanolamine utilization in Salmonella typhimurium. J Bacteriol 170: 3855-3863.
54. Roof, D.M., and Roth, J.R. (1989) Functions required for vitamin B12-dependent ethanolamine utilization in Salmonella typhimurium. J Bacteriol 171: 3316-3323.
55. Ryu, J., and Hartin, R.J. (1990) Quick transformation in Salmonella typhimurium LT2. Biotechniques 8: 43-45.
56. Sasse, J. (1991) Detection of proteins. In Current Protocols in Molecular Biology. Ausubel, F.A., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (eds). New York: Wiley Interscience, pp. 10.16.11-10.16.18.
57. Sheppard, D.E., Penrod, J.T., Bobik, T., Kofoid, E., and Roth, J.R. (2004) Evidence that a B12-adenosyl transferase is encoded within the ethanolamine operon of Salmonella enterica. J Bacteriol 186: 7635-7644.
58. Stojiljkovic, I., Baumler, A.J., and Heffron, F. (1995) Ethanolamine utilization in Salmonella typhimurium: nucleotide sequence, protein expression, and mutational analysis of the cchA cchB eutE eutJ eutG eutH gene cluster. J Bacteriol 177: 1357-1366.
59. Szabo, Z. (2008) Multinuclear NMR studies of the interaction of metal ions with adenine-nucleotides. Coordin Chem Rev 252: 2362-2380.
60. Thauer, R.K., Jungermann, K., and Decker, K. (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41: 100-180.
61. Thiennimitr, P., Winter, S.E., and Baumler, A.J. (2012) Salmonella, the host and its microbiota. Curr Opin Microbiol 15: 108-114.
62. Tsoy, O., Ravcheev, D., and Mushegian, A. (2009) Comparative genomics of ethanolamine utilization. J Bacteriol 191: 7157-7164.
63. Vogel, H.J., and Bonner, D.M. (1956) Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem 218: 97-106.
64. Winter, S.E., Thiennimitr, P., Winter, M.G., Butler, B.P., Huseby, D.L., Crawford, R.W., etal. (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467: 426-4269.
65. Wolfe, A.J. (2005) The acetate switch. Microbiol Mol Biol Rev 69: 12-50.
66. Yeates, T.O., Thompson, M.C., and Bobik, T.A. (2011) The protein shells of bacterial microcompartment organelles. Curr Opin Struct Biol 21: 223-231.
67. Zhu, H., Gonzalez, R., and Bobik, T.A. (2011) Coproduction of acetaldehyde and hydrogen during glucose fermentation by Escherichia coli. Appl Environ Microbiol 77: 6441-6450.