A unique capsular polysaccharide structure from the psychrophilic marine bacterium Colwellia psychrerythraea 34H that mimics antifreeze (glyco)proteins

Journal of the American Chemical Society

Volumn 137, Issue 1, 2015, Pages 179-189

  Carillo, Sara ^a   Casillo, Angela ^a   Pieretti, Giuseppina ^a   Parrilli, Ermenegilda ^a   Sannino, Filomena ^a,b   Bayer Giraldi, Maddalena ^d   Cosconati, Sandro ^e   Novellino, Ettore ^a   Ewert, Marcela ^c   Deming, Jody W ^c   Lanzetta, Rosa ^a   Marino, Gennaro ^a   Parrilli, Michelangelo ^a   Randazzo, Antonio ^a   Tutino, Maria L ^a   Corsaro, M Michela ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

^c UNIVERSITY OF WASHINGTON   (United States)

^d ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^e SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIA; CHEMICAL ANALYSIS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SUBMARINE GEOLOGY;

ANTIFREEZE PROTEIN; CAPSULAR POLYSACCHARIDES; COLWELLIA PSYCHRERYTHRAEA; DYNAMICS CALCULATIONS; MARINE ENVIRONMENT; ONE-AND TWO-DIMENSIONAL NMR; SECONDARY STRUCTURES; SUB-FREEZING CONDITION;

PROTEINS;

AMINOSUGAR; ANTIFREEZE PROTEIN; GLYCOPROTEIN; PHENOL; POLYMER; POLYSACCHARIDE; THREONINE; URONIC ACID; WATER;

ARTICLE; BACTERIAL COLONIZATION; CELL GROWTH; CHEMICAL ANALYSIS; CHEMICAL COMPOSITION; CHEMICAL STRUCTURE; COLWELLIA PSYCHRERYTHRAEA; CONTROLLED STUDY; CRYSTALLIZATION; FREEZING; MARINE ENVIRONMENT; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PSYCHROPHILIC BACTERIUM; ALTEROMONADACEAE; CARBOHYDRATE ANALYSIS; CHEMISTRY; CONFORMATION; CYTOLOGY; ISOLATION AND PURIFICATION; MOLECULAR GENETICS;

ALTEROMONADACEAE; ANTIFREEZE PROTEINS; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES;

EID: 84921033477     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja5075954     Document Type: Article

References (67)

1. Cavicchioli, R. Nat. Rev. Microbiol. 2006, 4, 331-43
2. Cavicchioli, R.; Siddiqui, K. S.; Andrews, D.; Sowers, K. R. Curr. Opin. Biotechnol. 2002, 13, 253-261
3. DAmico, S.; Collins, T.; Marx, J. C.; Feller, G.; Gerday, C. EMBO Rep. 2006, 7, 385-389
4. Casanueva, A.; Tuffin, M.; Cary, C.; Cowan, D. A. Trends Microbiol. 2010, 18, 374-381
5. Chattopadhyay, M. K. J. Biosci. 2006, 31, 157-165
6. Ummarino, S.; Corsaro, M. M.; Lanzetta, R.; Parrilli, M.; Peter-Katalinić, J. Rapid Commun. Mass Spectrom. 2003, 17, 2226-2232
7. Corsaro, M. M.; Lanzetta, R.; Parrilli, E.; Parrilli, M.; Tutino, M. L.; Ummarino, S. J. Bacteriol. 2004, 186, 29-34
8. Corsaro, M. M.; Pieretti, G.; Lindner, B.; Lanzetta, R.; Parrilli, E.; Tutino, M. L.; Parrilli, M. Chemistry 2008, 14, 9368-76
9. Carillo, S.; Pieretti, G.; Parrilli, E.; Tutino, M. L.; Gemma, S.; Molteni, M.; Lanzetta, R.; Parrilli, M.; Corsaro, M. M. Chemistry 2011, 17, 7053-7060
10. Ray, M. K.; Kumar, G. S.; Shivaji, S. Microbiology 1994, 140, 3217-3223
11. Ray, M. K.; Kumar, G. S.; Shivaji, S. J. Bacteriol. 1994, 176, 4243-4249
12. Huston, A. L.; Methé, B. A.; Deming, J. W. Appl. Environ. Microbiol. 2004, 70, 3321-3328
13. Deming, J. W. Extremophiles: cold environments. In Encyclopedia of microbiology, 3 rd ed.; Lederberg, J.; Schaechter, M., Eds.; Elsevier: Oxford, 2009.
14. Krembs, C.; Deming, J. W.; Junge, K.; Eicken, H. Deep Sea Res. Part I, Oceanogr. Res. Pap. 2002, 49, 2163-2181
15. Krembs, C.; Deming, J. W. The role of exopolymers in microbial adaptation to sea ice. In Psychrophiles: from biodiversity to biotechnology; Margesin, R.; Schinner, F.; Marx, J.-C.; Gerday, C., Eds.; Springer-Verlag: Berlin, 2008; pp 247-264.
16. Guézennec, J. J. Ind. Microbiol. Biotech. 2002, 29, 204-208
17. Krembs, C.; Eicken, H.; Deming, J. W. Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 3653-3658
18. Ewert, M.; Deming, J. W. Biology 2013, 2, 603-628
19. Nichols, C. M.; Lardière, S. G.; Bowman, J. P.; Nichols, P. D.; Gibson, J. A. E.; Guézennec, J. Microb. Ecol. 2005, 49, 578-589
20. Baker, M. G.; Lalonde, S. V.; Konhauser, K. O.; Foght, J. M. Appl. Environ. Microbiol. 2010, 76, 102-109
21. Sheng-Bo, L.; Xiu-Lan, C.; Hai-Lun, H.; Xi-Ying, Z.; Bin-Bin, X.; Yong, Y.; Bo, C.; Bai-Cheng, Z.; Yu-Zhong, Z. Appl. Environ. Microbiol. 2013, 79, 224
22. Methé, B. A.; Nelson, K. E.; Deming, J. W.; Momen, B.; Melamud, E.; Zhang, X.; Moult, J.; Madupu, R.; Nelson, W. C.; Dodson, R. J.; Brinkac, L. M.; Daugherty, S. C.; Durkin, A. S.; DeBoy, R. T.; Kolonay, J. F.; Sullivan, S. A.; Zhou, L.; Davidsen, T. M.; Wu, M.; Huston, A. L.; Lewis, M.; Weaver, B.; Weidman, J. F.; Khouri, H.; Utterback, T. R.; Feldblyum, T. V.; Fraser, C. M. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 10913-10918
23. Marx, J. G.; Carpenter, S. D.; Deming, J. W. Can. J. Microbiol. 2009, 55, 63-72
24. Ewert, M.; Deming, J. W. Ann. Glaciol. 2011, 52, 111-117
25. Basile, A.; Cafiero, G.; Spagnuolo, V.; Castaldo Cobianchi, R. J. Bryol. 1994, 18, 69-81
26. Carillo, S.; Pieretti, G.; Lindner, B.; Parrilli, E.; Sannino, F.; Tutino, M. L.; Lanzetta, R.; Parrilli, M.; Corsaro, M. M. Eur. J. Org. Chem. 2013, 3771-3779
27. Galanos, C.; Lüderitz, O.; Westphal, O. Eur. J. Biochem. 1969, 9, 245-249
28. Westphal, O.; Jann, K. Methods Carbohydr. Chem. 1965, 5, 83-91
29. Laemmli, U. K. Nature 1970, 227, 680-685
30. Tsai, C. M.; Frasch, C. E. Anal. Biochem. 1982, 119, 115-119
31. Al-Hakim, A.; Linhardt, R. J. Electrophoresis 1990, 11, 23-28
32. Simeone, L.; Mangiapia, G.; Vitiello, G.; Irace, C.; Colonna, A.; Ortona, O.; Montesarchio, D.; Paduano, L. Bioconjugate Chem. 2012, 23, 758-770
33. Ciucanu, I.; Kerek, F. Carbohydr. Res. 1984, 131, 209-217
34. Forsberg, L. S.; Ramadas Bhat, U.; Carlson, R. W. J. Biol. Chem. 2000, 275, 18851-18863
35. Leontein, K.; Lindberg, B.; Lönngren, J. Carbohydr. Res. 1978, 62, 359-362
36. Woods Group GLYCAM Web; Complex Carbohydrate Research Center, University of Georgia, Athens, GA, 2005-2014; http://www.glycam.com.
37. Case, D. A.; Babin, V.; Berryman, J. T.; Betz, R. M.; Cai, Q.; Cerutti, D. S.; Cheatham, T. E., III; Darden, T. A.; Duke, R. E.; Gohlke, H.; Goetz, A. W.; Gusarov, S.; Homeyer, N.; Janowski, P.; Kaus, J.; Kolossváry, I.; Kovalenko, A.; Lee, T. S.; LeGrand, S.; Luchko, T.; Luo, R.; Madej, B.; Merz, K. M.; Paesani, F.; Roe, D. R.; Roitberg, A.; Sagui, C.; Salomon-Ferrer, R.; Seabra, G.; Simmerling, C. L.; Smith, W.; Swails, J.; Walker, R. C.; Wang, J.; Wolf, R. M.; Wu, X.; Kollman, P. A. AMBER, 14 th ed.; University of California, San Francisco, 2014.
38. Kirschner, K. N.; Yongye, A. B.; Tschampel, S. M.; Daniels, C. R.; Foley, B. L.; Woods, R. J. J. Comput. Chem. 2008, 29, 622-655
39. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. J. Chem. Phys. 1983, 79, 926-935
40. Darden, T.; York, D.; Pedersen, L. J. Chem. Phys. 1993, 98, 10089-10092
41. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. J. Chem. Phys. 1995, 103, 8577-8593
42. van Gunsteren, W. F.; Berendsen, H. J. C. Mol. Phys. 1977, 34, 1311-1327
43. Shao, J.; Tanner, S. W.; Thompson, N.; Cheatham, T. E., III. J. Chem. Theory Comput. 2007, 3, 2312-2334
44. Pettersen, E. F.; Goddard, T. D.; Huang, C. C.; Couch, G. S.; Greenblatt, D. M.; Meng, E. C.; Ferrin, T. E. J. Comput. Chem. 2004, 25, 1605-1612
45. Bayer-Giraldi, M.; Weikusat, I.; Besir, H.; Dieckmann, G. Cryobiology 2011, 63, 210-219
46. Bayer-Giraldi, M.; Jin, E. S.; Wilson, P. W. Characterization of Ice Binding Proteins from Sea Ice Algae. In Plant Cold Acclimation; Hincha, D. K.; Zuther, E., Eds.; Methods in Molecular Biology; Springer: New York, 2014; 1166.
47. Cimini, D.; De Rosa, M.; Carlino, E.; Ruggiero, A.; Schiraldi, C. Microb. Cell. Fact. 2013, 12, 46-57
48. Taylor, W. H.; Juni, E. J. Bacteriol. 1960, 81, 688
49. Ramos, M. L. D.; Caldeira, M. M. M.; Gil, V. M. S. Carbohydr. Res. 1996, 286, 1-15
50. Sidorczyk, Z.; Swierzko, A.; Knirel, Y. A.; Vinogradov, E. V.; Chernyak, A. Y.; Kononov, L. O.; Cedzynski, M.; Rozalski, A.; Kaca, W.; Shashkov, A. S.; Kochetkov, N. K. Eur. J. Biochem. 1995, 230, 713-721
51. Bock, K.; Pedersen, C. Adv. Carbohydr. Chem. Biochem. 1983, 41, 27-66
52. Knight, C. A.; Duman, J. A. Cryobiology 1986, 23, 256-262
53. Sutherland, I. W. Biotechnology of microbial exopolysaccharides. In Cambridge Studies in Biotechnology; Baddiley, J.; Carey, N. H.; Higgins, I. J.; Potter, W. G., Eds.; Cambridge University Press: Cambridge, 1990; pp 1-11.
54. Komandrova, N. A.; Isakov, V. V.; Tomshich, S. V.; Romanenko, L. A.; Perepelov, A. V.; Shashkov, A. S. Biochemistry (Moscow) 2010, 75, 623-628
55. Palusiak, A. Carbohydr. Res. 2013, 380, 16-22
56. Nichols, C. M.; Guézennec, J.; Bowman, J. P. Mar. Biotechnol. 2005, 7, 253-271
57. Mancuso Nichols, C.; Lardière, S. G.; Bowman, J. P.; Nichols, P. D.; Gibson, J. A.; Guézennec, J. Microb. Ecol. 2005, 49, 578-589
58. Daley, M. E.; Sykes, B. D. Protein Sci. 2003, 12, 1323-1331
59. Ben, N. R. ChemBioChem 2001, 2, 161-166
60. Harding, M. M.; Anderberg, P. I.; Haymet, A. D. J. Eur. J. Biochem. 2003, 270, 1381-1392
61. Lin, F.; Davies, P. L.; Graham, L. A. Biochemistry 2011, 50, 4467-4478
62. Graether, S. P.; Kuiper, M. J.; Gagné, S. M.; Walker, V. K.; Jia, Z.; Sykes, B. D.; Davies, P. L. Nature 2000, 406, 325-328
63. Jia, Z.; Davies, P. L. Trends Biochem. Sci. 2002, 27, 101-110
64. Scotter, A. J.; Marshall, C. B.; Graham, L. A.; Gilbert, J. A.; Granham, C. P.; Davies, P. L. Cryobiology 2006, 53, 229-239
65. Pertaya, N.; Marshall, C. B.; Celik, Y.; Davies, P. L.; Braslavsky, I. Biophys. J. 2008, 95, 333-341
66. Raymond, J. A.; Fritsen, C.; Shen, K. FEMS Microbiol. Ecol. 2007, 61, 214-221
67. Walters, K. R.; Serianni, A. S.; Sformo, T.; Barnes, B. M.; Duman, J. G. Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 20210-20215