Localization of proteins to the 1,2-propanediol utilization microcompartment by non-native signal sequences is mediated by a common hydrophobic motif

Journal of Biological Chemistry

Volumn 290, Issue 40, 2015, Pages 24519-24533

  Jakobson, Christopher M ^a   Kim, Edward Y ^a   Slininger, Marilyn F ^a   Chien, Alex ^a   Tullman Ercek, Danielle ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EQUIPMENT TESTING; HYDROPHOBICITY; METABOLIC ENGINEERING; METABOLISM; SALMONELLA;

ENGINEERING APPLICATIONS; HETEROLOGOUS PROTEINS; HYDROPHOBIC MOTIFS; HYDROPHOBIC RESIDUES; METABOLIC PATHWAYS; N-TERMINAL SEQUENCES; SALMONELLA ENTERICA; SOLE CARBON SOURCE;

PROTEINS;

BACTERIAL PROTEIN; CYANOCOBALAMIN; ETHANOLAMINE; PROPYLENE GLYCOL; PROTEIN EUT; PROTEIN PDU; UNCLASSIFIED DRUG; CARBON; PROTEIN BINDING; SIGNAL PEPTIDE;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL MICROCOMPARTMENT; BACTERIAL STRUCTURES; CARBON SOURCE; CONTROLLED STUDY; ENCAPSULATION; ESCHERICHIA COLI; HYDROPHOBICITY; IN VIVO STUDY; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN TARGETING; SALMONELLA ENTERICA; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; BACTERIAL GENOME; BINDING COMPETITION; CELL FRACTIONATION; CHEMICAL PHENOMENA; CHEMISTRY; CLOSTRIDIUM; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; MOLECULAR GENETICS; PROCEDURES; PROTEIN ENGINEERING; PROTEIN TERTIARY STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING, COMPETITIVE; CARBON; CLOSTRIDIUM; ETHANOLAMINE; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; OPERON; PROPYLENE GLYCOL; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; SALMONELLA ENTERICA; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS; TRANSCRIPTION, GENETIC;

EID: 84943339595     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.651919     Document Type: Article

References (45)

1. 12-dependent 1, 2-propanediol degradation. J. Bacteriol. 181, 5967-5975
2. Sampson, E. M., and Bobik, T. A. (2008) Microcompartments for B12-dependent 1,2-propanediol degradation provide protection from DNA and cellular damage by a reactive metabolic intermediate. J. Bacteriol. 190, 2966-2971
3. Lawrence, A. D., Frank, S., Newnham, S., Lee, M. J., Brown, I. R., Xue, W.-F., and 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. 3, 454-465
4. Fan, C., Cheng, S., Liu, Y., Escobar, C. M., Crowley, C. S., Jefferson, R. E., Yeates, T. O., and Bobik, T. A. (2010) Short N-terminal sequences package proteins into bacterial microcompartments. Proc. Natl. Acad. Sci. 107, 7509-7514
5. Fan, C., and Bobik, T. A. (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
6. Fan, C., Cheng, S., Sinha, S., and Bobik, T. A. (2012) Interactions between the termini of lumen enzymes and shell proteins mediate enzyme encapsulation into bacterial microcompartments. Proc. Natl. Acad. Sci. 109, 14995-15000
7. Jorda, J., Liu, Y., Bobik, T. A., and Yeates, T. O. (2015) Exploring bacterial organelle interactomes: a model of the protein-protein interaction network in the Pdu microcompartment. PLoS Comput. Biol. 11, e1004067
8. Choudhary, S., and Quin., M. B., Sanders, M. A., Johnson, E. T., and Schmidt-Dannert, C. (2012) Engineered protein nano-compartments for targeted enzyme localization. PLoS One 7, e33342
9. Lassila, J. K., and 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, 2217-2228
10. Datsenko, K. A., and Wanner, B. L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A. 97, 6640-6645
11. Datta, S., Costantino, N., and Court, D. L. (2006) A set of recombineering plasmids for Gram-negative bacteria. Gene. 379, 109-115
12. 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
13. Cheng, S., Sinha, S., Fan, C., Liu, Y., and Bobik, T. A. (2011) Genetic analysis of the protein shell of the microcompartments involved in coen-zyme B12-dependent 1, 2-propanediol degradation by Salmonella. J. Bacteriol. 193, 1385-1392
14. Sinha, S., Cheng, S., Fan, C., and Bobik, T. A. (2012) The PduM protein is a structural component of the microcompartments involved in coenzyme B12-dependent 1,2-propanediol degradation by Salmonella enterica. J. Bacteriol. 194, 1912-1918
15. 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
16. Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J. D., and Higgins, D. G. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539
17. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
18. Engler, C., Gruetzner, R., Kandzia, R., and Marillonnet, S. (2009) Golden gate shuffling: a one-pot DNA shuffling method based on type IIs restriction enzymes. PLoS One 4, e5553
19. Kim, E. Y., and Jakobson., C. M., and Tullman-Ercek, D. (2014) Engineering transcriptional regulation to control Pdu microcompartment formation. PLoS One 9, e113814
20. Temme, K., Salis, H., Tullman-Ercek, D., Levskaya, A., Hong, S.-H., and Voigt, C. A. (2008) Induction and relaxation dynamics of the regulatory network controlling the type III secretion system encoded within Salmonella pathogenicity island 1. J. Mol. Biol. 377, 47-61
21. Bobik, T. A., Ailion, M., and Roth, J. R. (1992) A single regulatory gene integrates control of vitamin B12 synthesis and propanediol degradation. J. Bacteriol. 174, 2253-2266
22. Chen, P., Ailion, M., Bobik, T., Stormo, G., and Roth, J. (1995) Five promoters integrate control of the cob/pdu regulon in Salmonella typhimurium. J. Bacteriol. 177, 5401-5410
23. Rondon, M.R., and Escalante-Semerena, J. C. (1996) In vitro analysis of the interactions between the PocR regulatory protein and the promoter region of the cobalamin biosynthetic (cob) operon of Salmonella typhimurium LT2. J. Bacteriol. 178, 2196-2203
24. Roof, D. M., and Roth, J. R. (1992) Autogenous regulation of ethanolamine utilization by a transcriptional activator of the eut operon in Salmonella typhimurium. J. Bacteriol. 174, 6634-6643
25. Sheppard, D. E., and Roth, J. R. (1994) A rationale for autoinduction of a transcriptional activator: ethanolamine ammonia-lyase (EutBC) and the operon activator (EutR) compete for adenosyl-cobalamin in Salmonella typhimurium. J. Bacteriol. 176, 1287-1296
26. Heldt, D., Frank, S., Seyedarabi, A., Ladikis, D., Parsons, J.B., Warren, M. J., and Pickersgill, R. W. (2009) Structure of a trimeric bacterial microcompartment shell protein, EtuB, associated with ethanol utilization in Clostridium kluyveri. Biochem. J. 423, 199-207
27. Kim, E. Y., and Tullman-Ercek, D. (2014) A rapid flow cytometry assay for the relative quantification of protein encapsulation into bacterial microcompartments. Biotechnol. J. 9, 348-354
28. Leal, N. A., and Havemann., G. D., and Bobik, T. A. (2003) PduP is a coenzymeA-acylating propionaldehyde dehydrogenase associated with the polyhedral bodies involved in B 12-dependent 1, 2-propanediol degradation by Salmonella enterica serovar Typhimurium LT2. Arch. Microbiol. 180, 353-361
29. Axen, S. D., Erbilgin, O., and Kerfeld, C. A. (2014) A taxonomy of bacterial microcompartment loci constructed by a novel scoring method. PLoS Comput. Biol. 10, e1003898
30. Kerfeld, C. A., and Erbilgin, O. (2015) Bacterial microcompartments and the modular construction of microbial metabolism. Trends Microbiol. 23, 22-34
31. Erbilgin, O., and McDonald., K. L., and Kerfeld, C. A. (2014) Characterization ofa planctomycetal organelle: anovel bacterial microcompartment for the aerobic degradation of plant saccharides. Appl. Environ. Microbiol. 80, 2193-2205
32. Drozdetskiy, A., Cole, C., Procter, J., and Barton, G. J. (2015) JPred4: a protein secondary structure prediction server. Nucleic Acids Res. 43, W389-W394
33. Aussignargues, C., and Paasch., B. C., Gonzalez-Esquer, R., Erbilgin, O., and Kerfeld, C. A. (2015) Bacterial microcompartment assembly: the key role of encapsulation peptides. Commun. Integr. Biol. 8, e1039755
34. Pang, A., Liang, M., Prentice, M. B., and Pickersgill, R. W. (2012) Substrate channels revealed in the trimeric Lactobacillus reuteri bacterial microcompartment shell protein PduB. Acta Crystallogr. D Biol. Crystallogr. 68, 1642-1652
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, 22377-22384
36. 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. U.S.A. 112, 2990-2995
37. Conrado, R. J., and Mansell., T. J., Varner, J. D., and DeLisa, M. P. (2007) Stochastic reaction-diffusion simulation of enzyme compartmentalization reveals improved catalytic efficiency for a synthetic metabolic pathway. Metab. Eng. 9, 355-363
38. Huseby, D. L., and Roth, J. R. (2013) Evidence that a metabolic microcompartment contains and recycles private cofactor pools. J. Bacteriol. 195, 2864-2879
39. Thompson, M. C., and Crowley., C. S., Kopstein, J., Bobik, T. A., and Yeates, T. O. (2014) Structure of a bacterial microcompartment shell protein bound to a cobalamin cofactor. Acta Crystallogr. F Struct. Biol. Commun. 70, 1584-1590
40. Dueber, J. E., and Wu., G. C., Malmirchegini, G. R., Moon, T. S., Petzold, C. J., Ullal, A. V., Prather, K. L., and Keasling, J. D. (2009) Synthetic protein scaffolds provide modular control over metabolic flux. Nat. Biotechnol. 27, 753-759
41. Conrado, R. J., and Wu., G. C., Boock, J. T., Xu, H., Chen, S. Y., Lebar, T., Turnšek, J., Tomšič, N., Avbelj, M., Gaber, R., Koprivnjak, T., Mori, J., Glavnik, V., Vovk, I., Benčina, M., Hodnik, V., Anderluh, G., Dueber, J. E., Jerala, R., and DeLisa, M. P. (2012) DNA-guided assembly of biosynthetic pathways promotes improved catalytic efficiency. Nucleic Acids Res. 40, 1879-1889
42. Lee, H., and DeLoache., W. C., and Dueber, J. E. (2012) Spatial organization of enzymes for metabolic engineering. Metab. Eng. 14, 242-251
43. Sachdeva, G., Garg, A., Godding, D., Way, J. C., and Silver, P. A. (2014) In vivo co-localization of enzymes on RNA scaffolds increases metabolic production in a geometrically dependent manner. Nucleic Acids Res. 42, 9493-9503
44. Srikumar, S., and Fuchs, T. M. (2011) Ethanolamine utilization contributes to proliferation of Salmonella enterica serovar Typhimurium in food and in nematodes. Appl. Environ. Microbiol. 77, 281-290
45. Bertin, Y., and Girardeau., J. P., Chaucheyras-Durand, F., Lyan, B., Pujos-Guillot, E., Harel, J., and Martin, C. (2011) Enterohaemorrhagic Escherichia coli gains a competitive advantage by using ethanolamine as a nitrogen source in the bovine intestinal content. Environ. Microbiol. 13, 365-377