Bacterial microcompartments moving into a synthetic biological world

Journal of Biotechnology

Volumn 163, Issue 2, 2013, Pages 273-279

  Frank, Stefanie ^a   Lawrence, Andrew D ^a   Prentice, Michael B ^b   Warren, Martin J ^a  

^a UNIVERSITY OF KENT   (United Kingdom)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Bacterial microcompartment; Carboxysome; Metabolism; Organelle; Propanediol utilisation

Indexed keywords

BACTERIAL MICROCOMPARTMENT; BIOTECHNOLOGICAL APPLICATIONS; CARBON FIXATION; CARBOXYSOMES; METABOLIC PROCESS; MICRO-COMPARTMENTS; ORGANELLE; PROPANEDIOLS; PROPIONIC ACIDS;

ENZYMES;

METABOLISM;

ALCOHOL; BACTERIAL ENZYME; BACTERIAL PROTEIN; BIODIESEL; ETHANOLAMINE; PROPYLENE GLYCOL; PROTEIN PDUU; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL MICROCOMPARTMENT; BACTERIUM TRANSFORMATION; BIOFUEL PRODUCTION; BIOTECHNOLOGICAL PROCEDURES; CARBON FIXATION; CARBOXY TERMINAL SEQUENCE; CARBOXYSOME; CATABOLISM; CELL COMPARTMENTALIZATION; CELL ENGINEERING; CELL ORGANELLE; CITROBACTER FREUNDII; ENCAPSULATION; ESCHERICHIA COLI; GENETIC RECOMBINATION; HALOTHIOBACILLUS NEAPOLITANUS; HETEROLOGOUS EXPRESSION; METABOLOSOME; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; SALMONELLA; STRUCTURE ANALYSIS;

BACTERIA; BACTERIAL PROTEINS; BACTERIAL STRUCTURES; BACTERIOLOGICAL TECHNIQUES; BIOTECHNOLOGY; ORGANELLES;

BACTERIA (MICROORGANISMS);

EID: 84872197140     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2012.09.002     Document Type: Article

References (56)

1. Amichay D., Levitz R., Gurevitz M. Construction of a Synechocystis PCC6803 mutant suitable for the study of variant hexadecameric ribulose bisphosphate carboxylase/oxygenase enzymes. Plant Molecular Biology 1993, 23:465-476.
2. Beeby M., Bobik T.A., Yeates T.O. Exploiting genomic patterns to discover new supramolecular protein assemblies. Protein Science: A Publication of the Protein Society 2009, 18:69-79.
3. 12-dependent 1,2-propanediol degradation. Journal of Bacteriology 1999, 181:5967-5975.
4. Bobik T.A., Xu Y., Jeter R.M., Otto K.E., Roth J.R. Propanediol utilization genes (pdu) of Salmonella typhimurium: three genes for the propanediol dehydratase. Journal of Bacteriology 1997, 179:6633-6639.
5. Bonacci W., Teng P.K., Afonso B., Niederholtmeyer H., Grob P., Silver P.A., Savage D.F. Modularity of a carbon-fixing protein organelle. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:478-483.
6. Brinsmade S.R., Paldon T., Escalante-Semerena J.C. Minimal functions and physiological conditions required for growth of Salmonella enterica on ethanolamine in the absence of the metabolosome. Journal of Bacteriology 2005, 187:8039-8046.
7. Cannon G.C., Bradburne C.E., Aldrich H.C., Baker S.H., Heinhorst S., Shively J.M. Microcompartments in prokaryotes: carboxysomes and related polyhedra. Applied and Environmental Microbiology 2001, 67:5351-5361.
8. Chen P., Andersson D.I., Roth J.R. The control region of the pdu/cob regulon in Salmonella typhimurium. Journal of Bacteriology 1994, 176:5474-5482.
9. Cheng S., Bobik T.A. Characterization of the PduS cobalamin reductase of Salmonella enterica and its role in the Pdu microcompartment. Journal of Bacteriology 2010, 192:5071-5080.
10. Cheng S., Liu Y., Crowley C.S., Yeates T.O., Bobik T.A. Bacterial microcompartments: their properties and paradoxes. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 2008, 30:1084-1095.
11. 12 dependent 1,2-propanediol degradation by Salmonella. Journal of Bacteriology 2011, 193:1385-1392.
12. Choudhary S., Quin M.B., Sanders M.A., Johnson E.T., Schmidt-Dannert C. Engineered protein nano-compartments for targeted enzyme localization. PLoS One 2012, 7:e33342.
13. Crowley C.S., Cascio D., Sawaya M.R., Kopstein J.S., Bobik T.A., Yeates T.O. Structural insight into the mechanisms of transport across the Salmonella enterica Pdu microcompartment shell. Journal of Biological Chemistry 2010, 285:37838-37846.
14. Crowley C.S., Sawaya M.R., Bobik T.A., Yeates T.O. Structure of the PduU shell protein from the Pdu microcompartment of Salmonella. Structure 2008, 16:1324-1332.
15. 12 dependent glycerol and diol dehydratases and organization of the encoding genes. FEMS Microbiology Reviews 1998, 22:553-566.
16. Fan C., Bobik T.A. The N-terminal region of the medium subunit (PduD) packages adenosylcobalamin-dependent diol dehydratase (PduCDE) into the Pdu microcompartment. Journal of Bacteriology 2011, 193:5623-5628.
17. 12 synthesis. Journal of Biological Chemistry 2008, 283:11322-11329.
18. Fan C.G., Cheng S.Q., Liu Y., Escobar C.M., Crowley C.S., Jefferson R.E., Yeates T.O., Bobik T.A. Short N-terminal sequences package proteins into bacterial microcompartments. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:7509-7514.
19. Gibson D.G., Glass J.I., Lartigue C., Noskov V.N., Chuang R.Y., Algire M.A., Benders G.A., Montague M.G., Ma L., Moodie M.M., Merryman C., Vashee S., Krishnakumar R., Assad-Garcia N., Andrews-Pfannkoch C., Denisova E.A., Young L., Qi Z.Q., Segall-Shapiro T.H., Calvey C.H., Parmar P.P., Hutchison C.A., Smith H.O., Venter J.C. Creation of a bacterial cell controlled by a chemically synthesized genome. Science 2010, 329:52-56.
20. Hartman F.C., Harpel M.R. Structure, function, regulation, and assembly of d-ribulose-1,5-bisphosphate carboxylase/oxygenase. Annual Review of Biochemistry 1994, 63:197-234.
21. 12-dependent degradation of 1,2-propanediol in Salmonella enterica serovar Typhimurium LT2. Journal of Bacteriology 2003, 185:5086-5095.
22. Iancu C.V., Ding H.J., Morris D.M., Dias D.P., Gonzales A.D., Martino A., Jensen G.J. The structure of isolated Synechococcus strain WH8102 carboxysomes as revealed by electron cryotomography. Journal of Molecular Biology 2007, 372:764-773.
23. Iancu C.V., Morris D.M., Dou Z., Heinhorst S., Cannon G.C., Jensen G.J. Organization, structure, and assembly of alpha-carboxysomes determined by electron cryotomography of intact cells. Journal of Molecular Biology 2010, 396:105-117.
24. Johnson C.L., Pechonick E., Park S.D., Havemann G.D., Leal N.A., Bobik T.A. Functional genomic, biochemical, and genetic characterization of the Salmonella pduO gene, an ATP:cob(I)alamin adenosyltransferase gene. Journal of Bacteriology 2001, 183:1577-1584.
25. Kerfeld C.A., Heinhorst S., Cannon G.C. Bacterial microcompartments. Annual Review of Microbiology 2010, 64:391-408.
26. Kerfeld C.A., Sawaya M.R., Tanaka S., Nguyen C.V., Phillips M., Beeby M., Yeates T.O. Protein structures forming the shell of primitive bacterial organelles. Science 2005, 309:936-938.
27. Kinney J.N., Axen S.D., Kerfeld C.A. Comparative analysis of carboxysome shell proteins. Photosynthesis Research 2011, 109:21-32.
28. Kinney J.N., Salmeen A., Cai F., Kerfeld C.A. Elucidating essential role of conserved carboxysomal protein CcmN reveals common feature of bacterial microcompartment assembly. Journal of Biological Chemistry 2012, 287:17729-17736.
29. Klein M.G., Zwart P., Bagby S.C., Cai F., Chisholm S.W., Heinhorst S., Cannon G.C., Kerfeld C.A. Identification and structural analysis of a novel carboxysome shell protein with implications for metabolite transport. Journal of Molecular Biology 2009, 392:319-333.
30. Kofoid E., Rappleye C., Stojiljkovic I., Roth J. The 17-gene ethanolamine (eut) operon of Salmonella typhimurium encodes five homologues of carboxysome shell proteins. Journal of Bacteriology 1999, 181:5317-5329.
31. Komeili A., Li Z., Newman D.K., Jensen G.J. Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 2006, 311:242-245.
32. 12-dependent 1,2-propanediol degradation by Salmonella enterica serovar Typhimurium LT2. Archives of Microbiology 2003, 180:353-361.
33. 12-dependent 1,2-propanediol degradation by Salmonella enterica serovar Typhimurium LT2. Journal of Bacteriology 2007, 189:1589-1596.
34. Marcus Y., Berry J.A., Pierce J. Photosynthesis and photorespiration in a mutant of the cyanobacterium Synechocystis PCC-6803 lacking carboxysomes. Planta 1992, 187:511-516.
35. Martin W., Koonin E.V. Introns and the origin of nucleus-cytosol compartmentalization. Nature 2006, 440:41-45.
36. Nakamura C.E., Whited G.M. Metabolic engineering for the microbial production of 1,3-propanediol. Current Opinions in Biotechnology 2003, 14:454-459.
37. Pang A., Warren M.J., Pickersgill R.W. Structure of PduT, a trimeric bacterial microcompartment protein with a 4Fe-4S cluster-binding site. Acta Crystallographica. Section D, Biological Crystallography 2011, 67:91-96.
38. Parsons J.B., Dinesh S.D., Deery E., Leech H.K., Brindley A.A., Heldt D., Frank S., Smales C.M., Lunsdorf H., Rambach A., Gass M.H., Bleloch A., McClean K.J., Munro A.W., Rigby S.E., Warren M.J., Prentice M.B. Biochemical and structural insights into bacterial organelle form and biogenesis. Journal of Biological Chemistry 2008, 283:14366-14375.
39. Parsons J.B., Frank S., Bhella D., Liang M., Prentice M.B., Mulvihill D.P., Warren M.J. Synthesis of empty bacterial microcompartments, directed organelle protein incorporation, and evidence of filament-associated organelle movement. Molecular Cell 2010, 38:305-315.
40. Parsons J.B., Lawrence A.D., McLean K.J., Munro A.W., Rigby S.E., Warren M.J. Characterisation of PduS, the pdu metabolosome corrin reductase, and evidence of substructural organisation within the bacterial microcompartment. PLoS One 2010, 5:e14009.
41. Penrod J.T., Roth J.R. Conserving a volatile metabolite: a role for carboxysome-like organelles in Salmonella enterica. Journal of Bacteriology 2006, 188:2865-2874.
42. Reinhold L., Kosloff R., Kaplan A. A model for inorganic carbon fluxes and photosynthesis in cyanobacterial carboxysomes. Canadian Journal of Botany - Revue Canadienne De Botanique 1991, 69:984-988.
43. Ro D.K., Paradise E.M., Ouellet M., Fisher K.J., Newman K.L., Ndungu J.M., Ho K.A., Eachus R.A., Ham T.S., Kirby J., Chang M.C., Withers S.T., Shiba Y., Sarpong R., Keasling J.D. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 2006, 440:940-943.
44. Rondon M.R., Kazmierczak R., Escalante-Semerena J.C. 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. Journal of Bacteriology 1995, 177:5434-5439.
45. 12-dependent 1,2-propanediol degradation provide protection from DNA and cellular damage by a reactive metabolic intermediate. Journal of Bacteriology 2008, 190:2966-2971.
46. Savage D.F., Afonso B., Chen A.H., Silver P.A. Spatially ordered dynamics of the bacterial carbon fixation machinery. Science 2010, 327:1258-1261.
47. Schmid M.F., Paredes A.M., Khant H.A., Soyer F., Aldrich H.C., Chiu W., Shively J.M. Structure of Halothiobacillus neapolitanus carboxysomes by cryo-electron tomography. Journal of Molecular Biology 2006, 364:526-535.
48. 12-dependent 1,2-propanediol degradation by Salmonella enterica. Journal of Bacteriology 2012, 194:1912-1918.
49. So A.K., Espie G.S., Williams E.B., Shively J.M., Heinhorst S., Cannon G.C. A novel evolutionary lineage of carbonic anhydrase (epsilon class) is a component of the carboxysome shell. Journal of Bacteriology 2004, 186:623-630.
50. Sriramulu D.D., Liang M., Hernandez-Romero D., Raux-Deery E., Lunsdorf H., Parsons J.B., Warren M.J., Prentice M.B. Lactobacillus reuteri DSM 20016 produces cobalamin-dependent diol dehydratase in metabolosomes and metabolizes 1,2-propanediol by disproportionation. Journal of Bacteriology 2008, 190:4559-4567.
51. Tanaka S., Kerfeld C.A., Sawaya M.R., Cai F., Heinhorst S., Cannon G.C., Yeates T.O. Atomic-level models of the bacterial carboxysome shell. Science 2008, 319:1083-1086.
52. Tanaka S., Sawaya M.R., Yeates T.O. Structure and mechanisms of a protein-based organelle in Escherichia coli. Science 2010, 327:81-84.
53. Tobimatsu T., Kawata M., Toraya T. The N-terminal regions of ss and gamma subunits lower the solubility of adenosylcobalamin-dependent diol dehydratase. Bioscience Biotechnology and Biochemistry 2005, 69:455-462.
54. Tsai S.J., Yeates T.O. Bacterial microcompartments: insights into the structure, mechanism, and engineering applications. Progress in Molecular Biology and Translational Science, vol 103: Molecular Assembly in Natural and Engineered Systems 2011, pp. 1-20.
55. Vernizzi G., Sknepnek R., Olvera de la Cruz M. Platonic and Archimedean geometries in multicomponent elastic membranes. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:4292-4296.
56. Yeates T.O., Kerfeld C.A., Heinhorst S., Cannon G.C., Shively J.M. Protein-based organelles in bacteria: carboxysomes and related microcompartments. Nature Reviews. Microbiology 2008, 6:681-691.