Engineering bacterial microcompartment shells: Chimeric shell proteins and chimeric carboxysome shells

ACS Synthetic Biology

Volumn 4, Issue 4, 2015, Pages 444-453

  Cai, Fei ^a,c   Sutter, Markus ^c,d   Bernstein, Susan L ^c   Kinney, James N ^b   Kerfeld, Cheryl A ^a,b,c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

bacterial microcompartment; chimeric protein shell; cyanobacteria; metabolosome; self assembly; synthetic shell

Indexed keywords

ALPHA CARBOXYSOME; BACTERIAL MICROCOMPARTMENT SHELL PROTEIN; BACTERIAL PROTEIN; BETA CARBOXYSOME; CARBOXYSOME SHELL PROTEIN; CCMK2 PROTEIN; CCMK4 PROTEIN; CHIMERIC PROTEIN; CSOS1 PROTEIN; UNCLASSIFIED DRUG; HYBRID PROTEIN; MULTIPROTEIN COMPLEX;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; IN VIVO STUDY; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN ENGINEERING; BACTERIUM; BIOSYNTHESIS; CHEMISTRY; GENETICS; METABOLISM;

BACTERIA (MICROORGANISMS); CYANOBACTERIA;

BACTERIA; BACTERIAL PROTEINS; MULTIPROTEIN COMPLEXES; RECOMBINANT FUSION PROTEINS;

EID: 84928138623     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/sb500226j     Document Type: Article

References (49)

1. Kerfeld, C. A., Sawaya, M. R., Tanaka, S., Nguyen, C. V., Phillips, M., Beeby, M., and Yeates, T. O. (2005) Protein structures forming the shell of primitive bacterial organelles Science 309, 936-938
2. Cai, F., Sutter, M., Cameron, J. C., Stanley, D. N., Kinney, J. N., and Kerfeld, C. A. (2013) The structure of CcmP, a tandem bacterial microcompartment domain protein from the β-carboxysome, forms a subcompartment within a microcompartment J. Biol. Chem. 288, 16055-16063
3. Takenoya, M., Nikolakakis, K., and Sagermann, M. (2010) Crystallographic insights into the pore structures and mechanisms of the EutL and EutM shell proteins of the ethanolamine-utilizing microcompartment of Escherichia coli J. Bacteriol. 192, 6056-6063
4. Klein, M. G., Zwart, P., Bagby, S. C., Cai, F., Chisholm, S. W., Heinhorst, S., Cannon, G. C., and Kerfeld, C. A. (2009) Identification and structural analysis of a novel carboxysome shell protein with implications for metabolite transport J. Mol. Biol. 392, 319-333
5. Tanaka, S., Kerfeld, C. A., Sawaya, M. R., Cai, F., Heinhorst, S., Cannon, G. C., and Yeates, T. O. (2008) Atomic-level models of the bacterial carboxysome shell Science 319, 1083-1086
6. Tsai, Y., Sawaya, M. R., Cannon, G. C., Cai, F., Williams, E. B., Heinhorst, S., Kerfeld, C. A., and Yeates, T. O. (2007) Structural analysis of CsoS1A and the protein shell of the Halothiobacillus neapolitanus carboxysome PLoS Biol. 5, e144
7. 2 leakage barrier PLoS One 4, e7521
8. Jorda, J., Lopez, D., Wheatley, N. M., and Yeates, T. O. (2013) Using comparative genomics to uncover new kinds of protein-based metabolic organelles in bacteria Protein Sci. 22, 179-195
9. Kerfeld, C. A., Heinhorst, S., and Cannon, G. C. (2010) Bacterial microcompartments Annu. Rev. Microbiol. 64, 391-408
10. Beeby, M., Bobik, T. A., and Yeates, T. O. (2009) Exploiting genomic patterns to discover new supramolecular protein assemblies Protein Sci. 18, 69-79
11. Erbilgin, O., McDonald, K. L., and Kerfeld, C. A. (2014) Characterization of a planctomycetal organelle: A novel bacterial microcompartment for the aerobic degradation of plant saccharides Appl. Environ. Microbiol. 80, 2193-2205
12. Petit, E., LaTouf, W. G., Coppi, M. V., Warnick, T. A., Currie, D., Romashko, I., Deshpande, S., Haas, K., Alvelo-Maurosa, J. G., Wardman, C., Schnell, D. J., Leschine, S. B., and Blanchard, J. L. (2013) Involvement of a bacterial microcompartment in the metabolism of fucose and rhamnose by Clostridium phytofermentans PLoS One 8, e54337
13. Kinney, J. N., Axen, S. D., and Kerfeld, C. A. (2011) Comparative analysis of carboxysome shell proteins Photosynth Res. 109, 21-32
14. Yeates, T. O., Jorda, J., and Bobik, T. A. (2013) The shells of BMC-type microcompartment organelles in bacteria J. Mol. Microbiol. Biotechnol. 23, 290-299
15. Frank, S., Lawrence, A. D., Prentice, M. B., and Warren, M. J. (2013) Bacterial microcompartments moving into a synthetic biological world J. Biotechnol. 163, 273-279
16. Kim, E. Y. and Tullman-Ercek, D. (2013) Engineering nanoscale protein compartments for synthetic organelles Curr. Opin. Biotechnol. 24, 627-632
17. Zarzycki, J., Axen, S. D., Kinney, J. N., and Kerfeld, C. A. (2013) Cyanobacterial-based approaches to improving photosynthesis in plants J. Exp. Bot. 64, 787-798
18. Lassila, J. K., Bernstein, S. L., Kinney, J. N., Axen, S. D., and Kerfeld, C. A. (2014) Assembly of robust bacterial microcompartment shells using building blocks from an organelle of unknown function J. Mol. Biol. 426, 2217
19. Howorka, S. (2011) Rationally engineering natural protein assemblies in nanobiotechnology Curr. Opin. Biotechnol 22, 485-491
20. Doll, T. A., Raman, S., Dey, R., and Burkhard, P. (2013) Nanoscale assemblies and their biomedical applications J. R. Soc. Interface 10, 20120740
21. Agapakis, C. M., Boyle, P. M., and Silver, P. A. (2012) Natural strategies for the spatial optimization of metabolism in synthetic biology Nat. Chem. Biol. 8, 527-535
22. Chen, A. H. and Silver, P. A. (2012) Designing biological compartmentalization Trends Cell Biol. 22, 662-670
23. 2 fixation in crop species J. Exp Bot 64, 753-768
24. Lawrence, A. D., Frank, S., Newnham, S., Lee, M. J., Brown, I. R., Xue, W., Rowe, M. L., Mulvihill, D. P., Prentice, M. B., Howard, M. J., and Warren, M. J. (2014) Solution structure of a bacterial microcompartment targeting peptide and its application in the construction of an ethanol bioreactor ACS Synth. Biol. 30, 2014 10.1021/sb4001118
25. Roberts, E. W., Cai, F., Kerfeld, C. A., Cannon, G. C., and Heinhorst, S. (2012) Isolation and characterization of the Prochlorococcus carboxysome reveal the presence of the novel shell protein CsoS1D J. Bacteriol. 194, 787-795
26. Cai, F., Kerfeld, C. A., and Sandh, G. (2012) Bioinformatic identification and structural characterization of a new carboxysome shell protein Adv. Photosynth. Respir. 33, 12
27. Schwarz, D., Nodop, A., Huge, J., Purfurst, S., Forchhammer, K., Michel, K. P., Bauwe, H., Kopka, J., and Hagemann, M. (2011) Metabolic and transcriptomic phenotyping of inorganic carbon acclimation in the cyanobacterium Synechococcus elongatus PCC 7942 Plant Physiol. 155, 1640-1655
28. Vijayan, V., Jain, I. H., and O'Shea, E. K. (2011) A high resolution map of a cyanobacterial transcriptome Genome Biol. 12, R47
29. Rae, B. D., Long, B. M., Badger, M. R., and Price, G. D. (2012) Structural determinants of the outer shell of β-carboxysomes in Synechococcus elongatus PCC 7942: Roles for CcmK2, K3-K4, CcmO, and CcmL PLoS One 7, e43871
30. Cameron, J. C., Wilson, S. C., Bernstein, S. L., and Kerfeld, C. A. (2013) Biogenesis of a bacterial organelle: The carboxysome assembly pathway Cell 155, 1131-1140
31. Tanaka, S., Sawaya, M. R., and Yeates, T. O. (2010) Structure and mechanisms of a protein-based organelle in Escherichia coli Science 327, 81-84
32. 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
33. Crowley, C. S., Cascio, D., Sawaya, M. R., Kopstein, J. S., Bobik, T. A., and Yeates, T. O. (2010) Structural insight into the mechanisms of transport across the Salmonella enterica Pdu microcompartment shell J. Biol. Chem. 285, 37838-37846
34. Sinha, S., Cheng, S., Sung, Y. W., McNamara, D. E., Sawaya, M. R., Yeates, T. O., and Bobik, T. A. (2014) Alanine scanning mutagenesis identifies an asparagine-arginine-lysine triad essential to assembly of the shell of the pdu microcompartment J. Mol. Biol. 426, 2328-2345
35. Pang, A., Frank, S., Brown, I., Warren, M. J., and Pickersgill, R. W. (2014) Structural insights into higher-order assembly and function of the bacterial microcompartment protein PduA J. Biol. Chem. 289, 22377
36. Savage, D. F., Afonso, B., Chen, A. H., and Silver, P. A. (2010) Spatially ordered dynamics of the bacterial carbon fixation machinery Science 327, 1258-1261
37. Samborska, B. and Kimber, M. S. (2012) A dodecameric CcmK2 structure suggests β-carboxysomal shell facets have a double-layered organization Structure 20, 1353-1362
38. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372, 774-797
39. Kinney, J. N., Salmeen, A., Cai, F., and Kerfeld, C. A. (2012) Elucidating essential role of conserved carboxysomal protein CcmN reveals common feature of bacterial microcompartment assembly J. Biol. Chem. 287, 17729-17736
40. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
41. Afonine, P. V., Grosse-Kunstleve, R. W., Echols, N., Headd, J. J., Moriarty, N. W., Mustyakimov, M., Terwilliger, T. C., Urzhumtsev, A., Zwart, P. H., and Adams, P. D. (2012) Towards automated crystallographic structure refinement with phenix.refine Acta Crystallogr., Sect. D: Biol. Crystallogr. 68, 352-367
42. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments Acta Crystallogr., Sect. D: Biol. Crystallogr. 67, 235-242
43. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041
44. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0 Bioinformatics 23, 2947-2948
45. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M., Claverie, J. M., and Gascuel, O. (2008) Phylogeny.fr: Robust phylogenetic analysis for the non-specialist Nucleic Acids Res. 36, W465-469
46. Huson, D. H., Richter, D. C., Rausch, C., Dezulian, T., Franz, M., and Rupp, R. (2007) Dendroscope: An interactive viewer for large phylogenetic trees BMC Bioinformatics 8, 460
47. Edgar, R. C. (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res. 32, 1792-1797
48. Eddy, S. R. (1998) Profile hidden Markov models Bioinformatics 14, 755-763
49. Schuster-Bockler, B., Schultz, J., and Rahmann, S. (2004) HMM Logos for visualization of protein families BMC Bioinformatics 5, 7