Alanine scanning mutagenesis identifies an asparagine-arginine-lysine triad essential to assembly of the shell of the Pdu microcompartment

Journal of Molecular Biology

Volumn 426, Issue 12, 2014, Pages 2328-2345

  Sinha, Sharmistha ^a   Cheng, Shouqiang ^a   Sung, Yea Won ^a   McNamara, Dan E ^b   Sawaya, Michael R ^b   Yeates, Todd O ^b   Bobik, Thomas A ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

1,2 propanediol; carboxysome; microcompartment; Salmonella

Indexed keywords

ALANINE; ARGININE; ASPARAGINE; CYANOCOBALAMIN; LYSINE; PROPIONALDEHYDE; STRUCTURAL PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL MICROCOMPARTMENT; BACTERIAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; CRYSTAL STRUCTURE; DELETION MUTANT; DNA DAMAGE; DNA SEQUENCE; ENZYME SUBSTRATE; GENE DELETION; GROWTH CURVE; GROWTH INHIBITION; GROWTH RATE; MUTAGENESIS; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN INTERACTION; PROTEIN PURIFICATION;

BACTERIA (MICROORGANISMS); SALMONELLA;

1,2-PROPANEDIOL; B(12); CARBOXYSOME; MICROCOMPARTMENT; SALMONELLA;

ALANINE; AMINO ACID SEQUENCE; ASPARAGINE; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; DIPEPTIDES; DNA MUTATIONAL ANALYSIS; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; MUTATION, MISSENSE; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SALMONELLA TYPHIMURIUM;

EID: 84901239311     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.04.012     Document Type: Article

References (50)

1. S. Cheng, Y. Liu, C.S. Crowley, T.O. Yeates, and T.A. Bobik Bacterial microcompartments: their properties and paradoxes BioEssays 30 2008 1084 1095
2. 2 fixation in cyanobacteria and some proteobacteria Microbiol Mol Biol Rev 77 2013 357 379
3. T.O. Yeates, M.C. Thompson, and T.A. Bobik The protein shells of bacterial microcompartment organelles Curr Opin Struct Biol 21 2011 223 231
4. C.A. Kerfeld, S. Heinhorst, and G.C. Cannon Bacterial microcompartments Annu Rev Microbiol 64 2010 391 408
5. P. Thiennimitr, S.E. Winter, M.G. Winter, M.N. Xavier, V. Tolstikov, and D.L. Huseby et al. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota Proc Natl Acad Sci U S A 108 2011 17480 17485
6. T.A. Bobik Polyhedral organelles compartmenting bacterial metabolic processes Appl Microbiol Biotechnol 70 2006 517 525
7. F. Abdul-Rahman, E. Petit, and J.L. Blanchard The distribution of polyhedral bacterial microcompartments suggests frequent horizontal transfer and operon reassembly J Phylogenet Evol Biol 1 2013 10.4172/2329-9002.1000118
8. J. Jorda, D. Lopez, N.M. Wheatley, and T.O. Yeates Using comparative genomics to uncover new kinds of protein-based metabolic organelles in bacteria Protein Sci 22 2013 179 195
9. T.O. Yeates, C.A. Kerfeld, S. Heinhorst, G.C. Cannon, and J.M. Shively Protein-based organelles in bacteria: carboxysomes and related microcompartments Nat Rev Microbiol 6 2008 681 691
10. S.R. Brinsmade, T. Paldon, and J.C. Escalante-Semerena Minimal functions and physiological conditions required for growth of Salmonella enterica on ethanolamine in the absence of the metabolosome J Bacteriol 187 2005 8039 8046
11. 12-dependent degradation of 1,2-propanediol in Salmonella enterica serovar typhimurium LT2 J Bacteriol 184 2002 1253 1261
12. J.T. Penrod, and J.R. Roth Conserving a volatile metabolite: a role for carboxysome-like organelles in Salmonella enterica J Bacteriol 188 2006 2865 2874
13. C. Fan, and T.A. Bobik The N-terminal region of the medium subunit (PduD) packages adenosylcobalamin-dependent diol dehydratase (PduCDE) into the Pdu microcompartment J Bacteriol 193 2011 5623 5628
14. C. Fan, S. Cheng, Y. Liu, C.M. Escobar, C.S. Crowley, and R.E. Jefferson et al. Short N-terminal sequences package proteins into bacterial microcompartments Proc Natl Acad Sci U S A 107 2010 7509 7514
15. C. Fan, S. Cheng, S. Sinha, and T.A. Bobik Interactions between the termini of lumen enzymes and shell proteins mediate enzyme encapsulation into bacterial microcompartments Proc Natl Acad Sci U S A 109 2012 14995 15000
16. S. Tanaka, C.A. Kerfeld, M.R. Sawaya, F. Cai, S. Heinhorst, and G.C. Cannon et al. Atomic-level models of the bacterial carboxysome shell Science 319 2008 1083 1086
17. C.A. Kerfeld, M.R. Sawaya, S. Tanaka, C.V. Nguyen, M. Phillips, and M. Beeby et al. Protein structures forming the shell of primitive bacterial organelles Science 309 2005 936 938
18. J.N. Kinney, S.D. Axen, and C.A. Kerfeld Comparative analysis of carboxysome shell proteins Photosynth Res 109 2011 21 32
19. N.M. Wheatley, S.D. Gidaniyan, Y. Liu, D. Cascio, and T.O. Yeates Bacterial microcompartment shells of diverse functional types possess pentameric vertex proteins Protein Sci 22 2013 660 665
20. S. Tanaka, M.R. Sawaya, M. Phillips, and T.O. Yeates Insights from multiple structures of the shell proteins from the β-carboxysome Protein Sci 18 2009 108 120
21. K.A. Dryden, C.S. Crowley, S. Tanaka, T.O. Yeates, and M. Yeager Two-dimensional crystals of carboxysome shell proteins recapitulate the hexagonal packing of three-dimensional crystals Protein Sci 18 2009 2629 2635
22. 12-dependent 1, 2-propanediol degradation J Bacteriol 181 1999 5967 5975
23. 12-dependent degradation of 1,2-propanediol in Salmonella enterica serovar Typhimurium LT2 J Bacteriol 185 2003 5086 5095
24. 12-dependent 1,2-propanediol degradation by Salmonella J Bacteriol 193 2011 1385 1392
25. 12- dependent 1,2-propanediol degradation provide protection from DNA and cellular damage by a reactive metabolic intermediate J Bacteriol 190 2008 2966 2971
26. T.A. Bobik, Y. Xu, R.M. Jeter, K.E. Otto, and J.R. Roth Propanediol utilization genes (pdu) of Salmonella typhimurium: three genes for the propanediol dehydratase J Bacteriol 179 1997 6633 6639
27. 12-dependent 1,2-propanediol degradation by Salmonella enterica J Bacteriol 194 2012 1912 1918
28. C.S. Crowley, D. Cascio, M.R. Sawaya, J.S. Kopstein, T.A. Bobik, and T.O. Yeates Structural insight into the mechanisms of transport across the Salmonella enterica Pdu microcompartment shell J Biol Chem 285 2010 37838 37846
29. + internally within the Pdu microcompartment of Salmonella enterica PLoS One 7 2012 e47144
30. J.B. Parsons, S. Frank, D. Bhella, M. Liang, M.B. Prentice, and D.P. Mulvihill et al. Synthesis of empty bacterial microcompartments, directed organelle protein incorporation, and evidence of filament-associated organelle movement Mol Cell 38 2010 305 315
31. Y. Tsai, M.R. Sawaya, G.C. Cannon, F. Cai, E.B. Williams, and S. Heinhorst et al. Structural analysis of CsoS1A and the protein shell of the Halothiobacillus neapolitanus carboxysome PLoS Biol 5 2007 e144
32. D. Berkowitz, J.M. Hushon, H.J. Whitfield Jr., J. Roth, and B.N. Ames Procedure for identifying nonsense mutations J Bacteriol 96 1968 215 220
33. K.A. Datsenko, and B.L. Wanner One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Proc Natl Acad Sci U S A 97 2000 6640 6645
34. N. Philippe, J.P. Alcaraz, E. Coursange, J. Geiselmann, and D. Schneider Improvement of pCVD442, a suicide plasmid for gene allele exchange in bacteria Plasmid 51 2004 246 255
35. S.K. Sharan, L.C. Thomason, S.G. Kuznetsov, and D.L. Court Recombineering: a homologous recombination-based method of genetic engineering Nat Protoc 4 2009 206 223
36. J. Brosius, R.L. Cate, and A.P. Perlmutter Precise location of two promoters for the b-lactamase gene of pBR322. S1 mapping of ribonucleic acid isolated from Escherichia coli or synthesized in vitro J Biol Chem 257 1982 9205 9210
37. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 72 1976 248 254
38. C.L. Johnson, E. Pechonick, S.D. Park, G.D. Havemann, N.A. Leal, and T.A. Bobik Functional genomic, biochemical, and genetic characterization of the Salmonella pduO gene, an ATP:cob(I)alamin adenosyltransferase gene J Bacteriol 183 2001 1577 1584
39. W. Peti, and R. Page Strategies to maximize heterologous protein expression in Escherichia coli with minimal cost Protein Expr Purif 51 2007 1 10
40. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Macromol Crystallogr A 276 1997 307 326
41. W. Kabsch Xds Acta Crystallogr Sect D Biol Crystallogr 66 2010 125 132
42. P.A. Karplus, and K. Diederichs Linking crystallographic model and data quality Science 336 2012 1030 1033
43. M.S. Weiss Global indicators of X-ray data quality J Appl Crystallogr 34 2001 130 135
44. P.R. Evans, and G.N. Murshudov How good are my data and what is the resolution? Acta Crystallogr Sect D Biol Crystallogr 69 2013 1204 1214
45. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J Appl Crystallogr 40 2007 658 674
46. R.A. Laskowski, M.W. Macarthur, D.S. Moss, and J.M. Thornton Procheck - a program to check the stereochemical quality of protein structures J Appl Crystallogr 26 1993 283 291
47. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr Sect D Biol Crystallogr 60 2004 2126 2132
48. O.S. Smart, T.O. Womack, C. Flensburg, P. Keller, W. Paciorek, and A. Sharff et al. Exploiting structure similarity in refinement: automated NCS and target-structure restraints in BUSTER Acta Crystallogr Sect D Biol Crystallogr 68 2012 368 380
49. P.D. Adams, R.W. Grosse-Kunstleve, L.W. Hung, T.R. Ioerger, A.J. McCoy, and N.W. Moriarty et al. PHENIX: building new software for automated crystallographic structure determination Acta Crystallogr Sect D Biol Crystallogr 58 2002 1948 1954
50. J. Painter, and E.A. Merritt Optimal description of a protein structure in terms of multiple groups undergoing TLS motion Acta Crystallogr Sect D Biol Crystallogr 62 2006 439 450