Production and characterization of synthetic carboxysome shells with incorporated luminal proteins

Plant Physiology

Volumn 170, Issue 3, 2016, Pages 1868-1877

  Cai, Fei ^a,b   Bernstein, Susan L ^a,b   Wilson, Steven C ^a,b   Kerfeld, Cheryl A ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN;

AMINO ACID SEQUENCE; CELL GRANULE; CHEMISTRY; CYANOBACTERIUM; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOBLOTTING; METABOLISM; MOLECULAR MODEL; OPERON; PROCEDURES; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY; SYNTHETIC BIOLOGY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CYANOBACTERIA; CYTOPLASMIC GRANULES; ESCHERICHIA COLI; GREEN FLUORESCENT PROTEINS; IMMUNOBLOTTING; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; OPERON; PROTEIN CONFORMATION; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SYNTHETIC BIOLOGY;

EID: 84959274767     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.01822     Document Type: Article

References (54)

1. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201
2. Aussignargues C, Paasch BC, Gonzalez-Esquer R, Erbilgin O, Kerfeld CA (2015) Bacterial microcompartment assembly: the key role of encapsulation peptides. Commun Integr Biol 8: e1039755
3. Axen SD, Erbilgin O, Kerfeld CA (2014) A taxonomy of bacterial microcompartment loci constructed by a novel scoring method. PLOS Comput Biol 10: e1003898
4. Billis K, Billini M, Tripp HJ, Kyrpides NC, Mavromatis K (2014) Comparative transcriptomics between Synechococcus PCC 7942 and Synechocystis PCC 6803 provide insights into mechanisms of stress acclimation. PLoS One 9: e109738
5. Bobik TA, Havemann GD, Busch RJ, Williams DS, Aldrich HC (1999) The propanediol utilization (pdu) operon of Salmonella enterica serovar Typhimurium LT2 includes genes necessary for formation of polyhedral organelles involved in coenzyme B(12)-dependent 1, 2-propanediol degradation. J Bacteriol 181: 5967-5975
6. Cai F, Sutter M, Bernstein SL, Kinney JN, Kerfeld CA (2015) Engineering bacterial microcompartment shells: chimeric shell proteins and chimeric carboxysome shells. ACS Synth Biol 4: 444-453
7. Cameron JC, Wilson SC, Bernstein SL, Kerfeld CA (2013) Biogenesis of a bacterial organelle: the carboxysome assembly pathway. Cell 155: 1131-1140
8. Chessher A, Breitling R, Takano E (2015) Bacterial microcompartments: biomaterials for synthetic biology-based compartmentalization strategies. ACS Biomater Sci Eng. 1: 345-351
9. Choudhary S, Quin MB, Sanders MA, Johnson ET, Schmidt-Dannert C (2012) Engineered protein nano-compartments for targeted enzyme localization. PLoS One 7: e33342
10. Chowdhury C, Sinha S, Chun S, Yeates TO, Bobik TA (2014) Diverse bacterial microcompartment organelles. Microbiol Mol Biol Rev 78: 438-468
11. Erbilgin O, McDonald KL, Kerfeld CA (2014) Characterization of a planctomycetal organelle: a novel bacterial microcompartment for the aerobic degradation of plant saccharides. Appl Environ Microbiol 80: 2193-2205
12. Fan C, Bobik TA (2011) The N-terminal region of the medium subunit (PduD) packages adenosylcobalamin-dependent diol dehydratase (PduCDE) into the Pdu microcompartment. J Bacteriol 193: 5623-5628
13. Fan C, Cheng S, Sinha S, Bobik TA (2012) Interactions between the termini of lumen enzymes and shell proteins mediate enzyme encapsulation into bacterial microcompartments. Proc Natl Acad Sci USA 109: 14995-15000
14. Frank S, Lawrence AD, Prentice MB, Warren MJ (2013) Bacterial microcompartments moving into a synthetic biological world. J Biotechnol 163: 273-279
15. Garcia-Pichel F, Nübel U, Muyzer G (1998) The phylogeny of unicellular, extremely halotolerant cyanobacteria. Arch Microbiol 169: 469-482
16. Gonzalez-Esquer CR, Shubitowski TB, Kerfeld CA (2015) Streamlined construction of the cyanobacterial CO2-fixing organelle via protein domain fusions for use in plant synthetic biology. Plant Cell 27: 2637-2644
17. Hibberd JM, Sheehy JE, Langdale JA (2008) Using C4 photosynthesis to increase the yield of rice-rationale and feasibility. Curr Opin Plant Biol 11: 228-231
18. Iancu CV, Ding HJ, Morris DM, Dias DP, Gonzales AD, Martino A, Jensen GJ (2007) The structure of isolated Synechococcus strain WH8102 carboxysomes as revealed by electron cryotomography. J Mol Biol 372: 764-773
19. Iancu CV, Morris DM, Dou Z, Heinhorst S, Cannon GC, Jensen GJ (2010) Organization, structure, and assembly of alpha-carboxysomes determined by electron cryotomography of intact cells. J Mol Biol 396: 105-117
20. Jaenicke R, Böhm G (1998) The stability of proteins in extreme environments. Curr Opin Struct Biol 8: 738-748
21. Jakobson CM, Kim EY, Slininger MF, Chien A, Tullman-Ercek D (2015) Localization of proteins to the propanediol utilization microcompartment by non-native signal sequences is mediated by a common hydrophobic motif. J Biol Chem 1: 2
22. Jones DT (1999) Protein secondary structure prediction based on positionspecific scoring matrices. J Mol Biol 292: 195-202
23. Kerfeld CA, Erbilgin O (2015) Bacterial microcompartments and the modular construction of microbial metabolism. Trends Microbiol 23: 22-34
24. Kerfeld CA, Sawaya MR, Tanaka S, Nguyen CV, Phillips M, Beeby M, Yeates TO (2005) Protein structures forming the shell of primitive bacterial organelles. Science 309: 936-938
25. Kinney JN, Salmeen A, Cai F, Kerfeld CA (2012) Elucidating essential role of conserved carboxysomal protein CcmN reveals common feature of bacterial microcompartment assembly. J Biol Chem 287: 17729-17736
26. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948
27. Lassila JK, Bernstein SL, Kinney JN, Axen SD, Kerfeld CA (2014) Assembly of robust bacterial microcompartment shells using building blocks from an organelle of unknown function. J Mol Biol 426: 2217-2228
28. Lawrence AD, Frank S, Newnham S, Lee MJ, Brown IR, Xue WF, Rowe ML, Mulvihill DP, Prentice MB, Howard MJ, Warren MJ (2014) Solution structure of a bacterial microcompartment targeting peptide and its application in the construction of an ethanol bioreactor. ACS Synth Biol 3: 454-465
29. Li W, Cowley A, Uludag M, Gur T, McWilliam H, Squizzato S, Park YM, Buso N, Lopez R (2015) The EMBL-EBI bioinformatics web and programmatic tools framework. Nucleic Acids Res 43 (W1): W580-W584
30. Lin MT, Occhialini A, Andralojc PJ, Devonshire J, Hines KM, Parry MA, Hanson MR (2014) b-Carboxysomal proteins assemble into highly organized structures in Nicotiana chloroplasts. Plant J 79: 1-12
31. Long BM, Badger MR, Whitney SM, Price GD (2007) Analysis of carboxysomes from Synechococcus PCC7942 reveals multiple Rubisco complexes with carboxysomal proteins CcmM and CcaA. J Biol Chem 282: 29323-29335
32. Long BM, Tucker L, Badger MR, Price GD (2010) Functional cyanobacterial beta-carboxysomes have an absolute requirement for both long and short forms of the CcmM protein. Plant Physiol 153: 285-293
33. Marco E, Martinez I, Ronen-Tarazi M, Orus MI, Kaplan A (1994) Inactivation of ccmO in Synechococcus sp. strain PCC 7942 results in a mutant requiring high levels of CO2. Appl Environ Microbiol 60: 1018-1020
34. Margesin R, Schinner F (2001) Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 5: 73-83
35. 2 for growth. Plant Physiol Biochem 35: 137-146
36. McGrath JM, Long SP (2014) Can the cyanobacterial carbon-concentrating mechanism increase photosynthesis in crop species? A theoretical analysis. Plant Physiol 164: 2247-2261
37. Parry MAJ, Reynolds M, Salvucci ME, Raines C, Andralojc PJ, Zhu XG, Price GD, Condon AG, Furbank RT (2011) Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency. J Exp Bot 62: 453-467
38. Parsons JB, Frank S, Bhella D, Liang M, Prentice MB, Mulvihill DP, Warren MJ (2010) Synthesis of empty bacterial microcompartments, directed organelle protein incorporation, and evidence of filamentassociated organelle movement. Mol Cell 38: 305-315
39. Petit E, LaTouf WG, Coppi MV, Warnick TA, Currie D, Romashko I, Deshpande S, Haas K, Alvelo-Maurosa JG, Wardman C, Schnell DJ, Leschine SB, et al (2013) Involvement of a bacterial microcompartment in the metabolism of fucose and rhamnose by Clostridium phytofermentans. PLoS One 8: e54337
40. 2-concentrating mechanism. Can J Bot Revue Can Bot 69: 963-973
41. Price GD, Pengelly JJL, Forster B, Du J, Whitney SM, von Caemmerer S, Badger MR, Howitt SM, Evans JR (2013) The cyanobacterial CCM as a source of genes for improving photosynthetic CO2 fixation in crop species. J Exp Bot 64: 753-768
42. Rae BD, Long BM, Badger MR, Price GD (2012) Structural determinants of the outer shell of b-carboxysomes in Synechococcus elongatus PCC 7942: roles for CcmK2, K3-K4, CcmO, and CcmL. PLoS One 7: e43871
43. Samborska B, Kimber MS (2012) A dodecameric CcmK2 structure suggests b-carboxysomal shell facets have a double-layered organization. Structure 20: 1353-1362
44. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to Image J: 25 years of image analysis. Nat Methods 9: 671-675
45. Schwarz D, Nodop A, Hüge J, Purfürst S, Forchhammer K, Michel KP, Bauwe H, Kopka J, Hagemann M (2011) Metabolic and transcriptomic phenotyping of inorganic carbon acclimation in the Cyanobacterium Synechococcus elongatus PCC 7942. Plant Physiol 155: 1640-1655
46. Shively JM, Ball F, Brown DH, Saunders RE (1973a) Functional organelles in prokaryotes: polyhedral inclusions (carboxysomes) of Thiobacillus neapolitanus. Science 182: 584-586
47. Shively JM, Ball FL, Kline BW (1973b) Electron microscopy of the carboxysomes (polyhedral bodies) of Thiobacillus neapolitanus. J Bacteriol 116: 1405-1411
48. Shively JM, Bradburne CE, Aldrich HC, Bobik TA, Mehlman JL, Jin S, Baker SH (1998) Sequence homologs of the carboxysomal polypeptide CsoS1 of the thiobacilli are present in cyanobacteria and enteric bacteria that form carboxysomes-polyhedral bodies. Can J Bot Revue Can Bot 76: 906-916
49. Tanaka S, Kerfeld CA, Sawaya MR, Cai F, Heinhorst S, Cannon GC, Yeates TO (2008) Atomic-level models of the bacterial carboxysome shell. Science 319: 1083-1086
50. Vijayan V, Jain IH, O’Shea EK (2011) A high resolution map of a cyanobacterial transcriptome. Genome Biol 12: R47
51. Xu D, Zhang Y (2012) Ab initio protein structure assembly using continuous structure fragments and optimized knowledge-based force field. Proteins 80: 1715-1735
52. Xu D, Zhang Y (2013) Toward optimal fragment generations for ab initio protein structure assembly. Proteins 81: 229-239
53. Zarzycki J, Axen SD, Kinney JN, Kerfeld CA (2013) Cyanobacterial-based approaches to improving photosynthesis in plants. J Exp Bot 64: 787-798
54. Zarzycki J, Erbilgin O, Kerfeld CA (2015) Bioinformatic characterization of glycyl radical enzyme-associated bacterial microcompartments. Appl Environ Microbiol 81: 8315-8329