A phasin with extra talents: A polyhydroxyalkanoate granule-associated protein has chaperone activity

Environmental Microbiology

Volumn 17, Issue 5, 2015, Pages 1765-1776

  Mezzina, Mariela P ^a   Wetzler, Diana E ^a   de Almeida, Alejandra ^a   Dinjaski, Nina ^b   Prieto, M Auxiliadora ^b   Pettinari, Maria Julia ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AZOTOBACTER; ESCHERICHIA COLI;

BACTERIAL PROTEIN; CHAPERONE; PHASIN; PLANT LECTIN; POLYHYDROXYALKANOIC ACID;

AZOTOBACTER; CELL INCLUSION; CHEMISTRY; ESCHERICHIA COLI; GENETICS; METABOLISM; PROTEIN FOLDING;

AZOTOBACTER; BACTERIAL PROTEINS; ESCHERICHIA COLI; INCLUSION BODIES; MOLECULAR CHAPERONES; PLANT LECTINS; POLYHYDROXYALKANOATES; PROTEIN FOLDING;

EID: 84928298441     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12636     Document Type: Article

References (45)

1. de Almeida, A., Nikel, P.I., Giordano, A.M., and Pettinari, M.J. (2007) Effects of granule-associated protein PhaP on glycerol-dependent growth and polymer production in poly(3-hydroxybutyrate)-producing Escherichia coli. Appl Environ Microbiol 73: 7912-7916.
2. de Almeida, A., Catone, M.V., Rhodius, V.A., Gross, C.A., and Pettinari, M.J. (2011) Unexpected stress-reducing effect of PhaP, a poly(3-hydroxybutyrate) granule-associated protein, in Escherichia coli. Appl Environ Microbiol 77: 6622-6629.
3. Alonso, L.G., Smal, C., Garcia-Alai, M.M., Chemes, L., Salame, M., and de Prat-Gay, G. (2006) Chaperone holdase activity of human papillomavirus E7 oncoprotein. Biochemistry 45: 657-667.
4. Ayub, N.D., Tribelli, P.M., and López, N.I. (2009) Polyhydroxyalkanoates are essential for maintenance of redox state in the Antarctic bacterium Pseudomonas sp. 14-3 during low temperature adaptation. Extremophiles 13: 59-66.
5. Banki, M.R., Gerngross, T.U., and Wood, D.W. (2005) Novel and economical purification of recombinant proteins: intein-mediated protein purification using in vivo polyhydroxybutyrate ( PHB ) matrix association. Protein Sci 14: 1387-1395.
6. Bolte, S., and Cordelières, F.P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224: 213-232.
7. Buchner, J., Grallert, H., and Jakob, U. (1998) Analysis of chaperone function using citrate synthase as nonnative substrate protein. Methods Enzymol 290: 323-338.
8. Carrió, M.M., and Villaverde, A. (2003) Role of molecular chaperones in inclusion body formation. FEBS Lett 537: 215-221.
9. Carrió, M.M., and Villaverde, A. (2005) Localization of chaperones DnaK and GroEL in bacterial inclusion bodies. J Bacteriol 187: 3599-3601.
10. Dennis, D., Sein, V., Martinez, E., and Augustine, B. (2008) PhaP is involved in the formation of a network on the surface of polyhydroxyalkanoate inclusions in Cupriavidus necator H16. J Bacteriol 190: 555-563.
11. Galán, B., Dinjaski, N., Maestro, B., de Eugenio, L.I., Escapa, I.F., Sanz, J.M., etal. (2011) Nucleoid-associated PhaF phasin drives intracellular location and segregation of polyhydroxyalkanoate granules in Pseudomonas putida KT2442. Mol Microbiol 79: 402-418.
12. Gill, R.T., Valdes, J.J., and Bentley, W.E. (2000) A comparative study of global stress gene regulation in response to overexpression of recombinant proteins in Escherichia coli. Metab Eng 2: 178-189.
13. Guisbert, E., Yura, T., Rhodius, V.A., and Gross, C.A. (2008) Convergence of molecular, modeling, and systems approaches for an understanding of the Escherichia coli heat shock response. Microbiol Mol Biol Rev 72: 545-554.
14. Han, M., Yoon, S.S., and Lee, S.Y. (2001) Proteome analysis of metabolically engineered Escherichia coli producing poly ( 3-hydroxybutyrate ). J Bacteriol 183: 301-308.
15. Handrick, R., Reinhardt, S., Schultheiss, D., Reichart, T., Jendrossek, V., and Jendrossek, D. (2004) Unraveling the function of the Rhodospirillum rubrum activator ofPolyhydroxybutyrate (PHB) degradation: the activator is a PHB-granule-bound protein (Phasin). J Bacteriol 186: 2466-2475.
16. Hoffmann, F., and Rinas, U. (2004) Stress induced by recombinant protein production in Escherichia coli. Adv Biochem Eng Biotechnol 89: 73-92.
17. Jürgen, B., Lin, H.Y., Riemschneider, S., Scharf, C., Neubauer, P., Schmid, R., etal. (2000) Monitoring of genes that respond to overproduction of an insoluble recombinant protein in Escherichia coli glucose-limited fed-batch fermentations. Biotechnol Bioeng 70: 217-224.
18. Kadouri, D., Jurkevitch, E., Okon, Y., and Castro-Sowinski, S. (2005) Ecological and agricultural significance of bacterial polyhydroxyalkanoates. Crit Rev Microbiol 31: 55-67.
19. Keshavarz, T., and Roy, I. (2010) Polyhydroxyalkanoates: bioplastics with a green agenda. Curr Opin Microbiol 13: 321-326.
20. Kitagawa, M., Matsumura, Y., and Tsuchido, T. (2000) Small heat shock proteins, IbpA and IbpB, are involved in resistances to heat and superoxide stresses in Escherichia coli. FEMS Microbiol Lett 184: 165-171.
21. Kuchta, K., Chi, L., Fuchs, H., Pötter, M., and Steinbüchel, A. (2007) Studies on the influence of phasins on accumulation and degradation of PHB and nanostructure of PHB granules in Ralstonia eutropha H16. Biomacromolecules 8: 657-662.
22. Laskowskaa, E., Wawrzynow, A., and Taylor, A. (1996) lbpA and IbpB, the new heat-shock proteins bind to endogenous Escherichia coli proteins aggregated intracellularly by heat shock. Biochimie 78: 117-122.
23. Lindner, A.B., Madden, R., Demarez, A., Stewart, E.J., and Taddei, F. (2008) Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc Natl Acad Sci USA 105: 3076-3081.
24. López, N.I., Floccari, M., Steinbüchel, A., García, A.F., and Méndez, B. (1995) Effect of poly(3-hydroxybutyrate) (PHB) content on the starvation-survival of bacteria in natural waters. FEMS Microbiol Ecol 16: 95-101.
25. Maestro, B., Galán, B., Alfonso, C., Rivas, G., Prieto, M.A., and Sanz, J.M. (2013) A new family of intrinsically disordered proteins: structural characterization of the major phasin PhaF from Pseudomonas putida KT2440. PLoS ONE 8: e56904.
26. Mezzina, M.P., Wetzler, D.E., Catone, M., V, Bucci, H., Di Paola, M., and Pettinari, M.J. (2014) A phasin with many faces: structural insights on PhaP from Azotobacter sp. FA8. PLoS ONE 9: e103012.
27. Moldes, C., García, P., García, L., and Prieto, M.A. (2004) In vivo immobilization of fusion proteins on bioplastics by the novel tag BioF. Appl Environ Microbiol 70: 3205-3212.
28. Pais, J., Farinha, I., Freitas, F., Serafim, L.S., Martínez, V., Martínez, J.C., etal. (2014) Improvement on the yield of polyhydroxyalkanotes production from cheese whey by a recombinant Escherichia coli strain using the proton suicide methodology. Enzyme Microb Technol 55: 151-158.
29. Pettinari, M., Chaneton, L., Vazquez, G., Steinbüchel, A., and Méndez, B.S. (2003) Insertion sequence-like elements associated with putative polyhydroxybutyrate regulatory genes in Azotobacter sp. FA8. Plasmid 50: 36-44.
30. Pfeiffer, D., and Jendrossek, D. (2012) Localization of poly(3-hydroxybutyrate) (PHB) granule-associated proteins during PHB granule formation and identification of two new phasins, PhaP6 and PhaP7, in Ralstonia eutropha H16. J Bacteriol 194: 5909-5921.
31. Pfeiffer, D., Wahl, A., and Jendrossek, D. (2011) Identification of a multifunctional protein, PhaM, that determines number, surface to volume ratio, subcellular localization and distribution to daughter cells of poly(3-hydroxybutyrate), PHB, granules in Ralstonia eutropha H16. Mol Microbiol 82: 936-951.
32. Pötter, M., Müller, H., Reinecke, F., Wieczorek, R., Fricke, F., Bowien, B., etal. (2004) The complex structure of polyhydroxybutyrate (PHB) granules: four orthologous and paralogous phasins occur in Ralstonia eutropha. Microbiology 150: 2301-2311.
33. Qi, Q., Steinbuchel, A., and Rehm, B.H.A. (2000) In vitro synthesis of poly (3-hydroxydecanoate): purification and enzymatic characterization of type II polyhydroxyalkanoate synthases PhaC1 and PhaC2 from Pseudomonas aeruginosa. Appl Microbiol Biotechnol 54: 37-43.
34. Reddy, C.S., Ghai, R., Rashmi, and Kalia, V. (2003) Polyhydroxyalkanoates: an overview. Bioresour Technol 87: 137-146.
35. Ruiz, J., Lopez, N., Fernández, R.O., and Mendez, B. (2001) Polyhydroxyalkanoate degradation is associated with nucleotide accumulation and enhances stress resistance and survival of Pseudomonas oleovorans in natural water microcosms. Appl Environ Microbiol 67: 225-230.
36. Smock, R.G., Blackburn, M.E., and Gierasch, L.M. (2011) Conserved, disordered C terminus of DnaK enhances cellular survival upon stress and DnaK in vitro chaperone activity. J Biol Chem 286: 31821-31829.
37. Tal, S., and Okon, Y. (1985) Production of the reserve material poly-P-hydroxybutyrate and its function in Azospirillum brasilense Cd. Can J Microbiol 31: 608-613.
38. Tessmer, N., König, S., Malkus, U., Reichelt, R., Pötter, M., and Steinbüchel, A. (2007) Heat-shock protein HspA mimics the function of phasins sensu stricto in recombinant strains of Escherichia coli accumulating polythioesters or polyhydroxyalkanoates. Microbiology 153: 366-374.
39. Thomas, J., and Baneyx, F. (1998) Roles of the Escherichia coli small heat shock proteins IbpA and IbpB in thermal stress management: comparison with ClpA, ClpB, and HtpG in vivo. J Bacteriol 180: 5165-5172.
40. Tian, S.-J., Lai, W.-J., Zheng, Z., Wang, H.-X., and Chen, G.-Q. (2005) Effect of over-expression of phasin gene from Aeromonas hydrophila on biosynthesis of copolyesters of 3-hydroxybutyrate and 3-hydroxyhexanoate. FEMS Microbiol Lett 244: 19-25.
41. Wang, Y., Yin, J., and Chen, G.-Q. (2014) Polyhydroxyalkanoates, challenges and opportunities. Curr Opin Biotechnol 30C: 59-65.
42. Wei, D.-X., Chen, C.-B., Fang, G., Li, S.-Y., and Chen, G.-Q. (2011) Application of polyhydroxyalkanoate binding protein PhaP as a bio-surfactant. Appl Microbiol Biotechnol 91: 1037-1047.
43. Wieczorek, R., Pries, A., Steinbüchel, A., and Mayer, F. (1995) Analysis of a 24-kilodalton protein associated with the polyhydroxyalkanoic acid granules in Alcaligenes eutrophus. J Bacteriol 177: 2425-2435.
44. Yasukawa, T., Kanei-Ishii, C., Maekawa, T., Fujimoto, J., Yamamoto, T., and Ishii, S. (1995) Increase of solubility of foreign proteins in Escherichia coli by coproduction of the bacterial thioredoxin. J Biol Chem 270: 25328-25331.
45. York, G.M., Stubbe, J., and Sinskey, A.J. (2001) New insight into the role of the PhaP phasin of Ralstonia eutropha in promoting synthesis of polyhydroxybutyrate. J Bacteriol 183: 2394-2397.