Structural flexibility of the heme cavity in the cold-adapted truncated hemoglobin from the Antarctic marine bacterium Pseudoalteromonas haloplanktis TAC125

FEBS Journal

Volumn 282, Issue 15, 2015, Pages 2948-2965

  Giordano, Daniela ^a   Pesce, Alessandra ^b   Boechi, Leonardo ^c   Bustamante, Juan Pablo ^c   Caldelli, Elena ^d   Howes, Barry D ^d   Riccio, Alessia ^a   Di Prisco, Guido ^a   Nardini, Marco ^e   Estrin, Dario ^c   Smulevich, Giulietta ^d   Bolognesi, Martino ^e   Verde, Cinzia ^a,f  

^a CNR   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^d UNIVERSITY OF FLORENCE   (Italy)

^e UNIVERSITY OF MILAN   (Italy)

^f ROMA TRE UNIVERSITY   (Italy)

Author keywords

adaptation; bacterial hemoglobin; molecular dynamics; resonance Raman; X ray structure

Indexed keywords

HISTIDINE; ISOLEUCINE; LEUCINE; METHIONINE; PHENYLALANINE; TRUNCATED HEMOGLOBIN; TRYPTOPHAN; TYROSINE; HEME; HEMOGLOBIN;

ABSORPTION SPECTROSCOPY; ARTICLE; COMPARATIVE STUDY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON SPIN RESONANCE; HEME CAVITY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE, FUNCTION AND VARIABILITY; PSEUDOALTEROMONAS HALOPLANKTIS; RAMAN SPECTROMETRY; STRUCTURE ANALYSIS; STRUCTURE FLEXIBILITY; AMINO ACID SEQUENCE; ANTARCTICA; CHEMISTRY; MARINE BIOLOGY; MOLECULAR GENETICS; PROTEIN CONFORMATION; PSEUDOALTEROMONAS; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

BACTERIA (MICROORGANISMS); CYANOBACTERIA; PROTOZOA; PSEUDOALTEROMONAS HALOPLANKTIS;

AMINO ACID SEQUENCE; ANTARCTIC REGIONS; CRYSTALLOGRAPHY, X-RAY; HEME; HEMOGLOBINS; MARINE BIOLOGY; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PSEUDOALTEROMONAS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84938211607     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13335     Document Type: Article

References (70)

1. Vinogradov S, Tinajero-Trejo M, Poole RK, &, Hoogewijs D, (2013) Bacterial and archaeal globins-a revised perspective. Biochim Biophys Acta 1834, 1789-1800.
2. Vuletich DA, &, Lecomte JT, (2006) A phylogenetic and structural analysis of truncated hemoglobins. J Mol Evol 62, 196-210.
3. Pesce A, Bolognesi M, &, Nardini M, (2013) The diversity of 2/2 (truncated) globins. Adv Microb Physiol 63, 49-78.
4. Milani M, Savard PY, Ouellet H, Ascenzi P, Guertin M, &, Bolognesi M, (2003) A TyrCD1/TrpG8 hydrogen bond network and a TyrB10TyrCD1 covalent link shape the heme distal site of Mycobacterium tuberculosis hemoglobin O. Proc Natl Acad Sci USA 100, 5766-5771.
5. Bonamore A, Ilari A, Giangiacomo L, Bellelli A, Morea V, &, Boffi A, (2005) A novel thermostable hemoglobin from the actinobacterium Thermobifida fusca. FEBS J 272, 4189-4201.
6. Giangiacomo A, Ilari L, Boffi A, Morea V, &, Chiancone E, (2005) The truncated oxygen-avid hemoglobin from Bacillus subtilis: X-ray structure and ligand binding properties. J Biol Chem 280, 9192-9202.
7. Ilari A, Kjelgaard P, von Wachenfeldt C, Catacchio B, Chiancone E, &, Boffi A, (2007) Crystal structure and ligand binding properties of the truncated hemoglobin from Geobacillus stearothermophilus. Arch Biochem Biophys 457, 85-94.
8. Pesce A, Nardini M, Labarre M, Richard C, Wittenberg JB, Wittenberg BA, Guertin M, &, Bolognesi M, (2011) Structural characterization of a group II 2/2 hemoglobin from the plant pathogen Agrobacterium tumefaciens. Biochim Biophys Acta 1814, 810-816.
9. Reeder BJ, &, Hough MA, (2014) The structure of a class 3 nonsymbiotic plant haemoglobin from Arabidopsis thaliana reveals a novel N-terminal helical extension. Acta Crystallogr D Biol Crystallogr 70, 1411-1418.
10. Giordano D, Parrilli E, Dettaï A, Russo R, Barbiero G, Marino G, Lecointre G, di Prisco G, Tutino L, &, Verde C, (2007) The truncated hemoglobins in the Antarctic psychrophilic bacterium Pseudoalteromonas haloplanktis TAC125. Gene 398, 69-77.
11. Giordano D, Coppola D, Russo R, Tinajero-Trejo M, di Prisco G, Lauro F, Ascenzi P, &, Verde C, (2013) The globins of cold-adapted Pseudoalteromonas haloplanktis TAC125: from the structure to the physiological functions. Adv Microb Physiol 63, 329-389.
12. Parrilli E, Giuliani M, Giordano D, Russo R, Marino G, Verde C, &, Tutino ML, (2010) The role of a 2-on-2 haemoglobin in oxidative and nitrosative stress resistance of Antarctic Pseudoalteromonas haloplanktis TAC125. Biochimie 92, 1003-1009.
13. Howes BD, Giordano D, Boechi L, Russo R, Mucciacciaro S, Ciaccio C, Sinibaldi F, Fittipaldi M, Martbox drawings light down and left MA, Estrin DA, et al,. (2011) The peculiar heme pocket of the 2/2 hemoglobin of cold-adapted Pseudoalteromonas haloplanktis TAC125. J Biol Inorg Chem 16, 299-311.
14. Giordano D, Russo R, Ciaccio C, Howes BD, di Prisco G, Smulevich G, Coletta M, &, Verde C, (2011) Ligand- and proton-linked conformational changes of the ferrous 2/2 hemoglobin of Pseudoalteromonas haloplanktis TAC125. IUBMB Life 63, 566-573.
15. Russo R, Giordano D, di Prisco G, Hui Bon Hoa G, Marden MC, Verde C, &, Kiger L, (2013) Ligand-rebinding kinetics of 2/2 hemoglobin from the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Biochim Biophys Acta 1834, 1932-1938.
16. Coppola D, Giordano D, Tinajero-Trejo M, di Prisco G, Ascenzi P, Poole RK, &, Verde C, (2013) Antarctic bacterial hemoglobin and its role in the protection against nitrogen reactive species. Biochim Biophys Acta 1834, 1923-1931.
17. Laskowski RA, MacArthur MW, Moss DS, &, Thornton JM, (1993) PROCHECK, a program to check the stereochemical quality of protein structure. J Appl Crystallogr 26, 283-291.
18. Krissinel E, &, Henrick K, (2005) Detection of Protein Assemblies in Crystals. In Computational Life Science (, Berthold MR, Glen RC, Diederichs K, Kohlbacher O, &, Fischer I, eds), pp. 163-174. Springer, Berlin Heidelberg.
19. Nardini M, Pesce A, Milani M, &, Bolognesi M, (2007) Protein fold and structure in the truncated (2/2) globin family. Gene 398, 2-11.
20. Milani M, Pesce A, Nardini M, Ouellet H, Ouellet Y, Dewilde S, Bocedi A, Ascenzi P, Guertin M, Moens L, et al,. (2005) Structural bases for heme binding and diatomic ligand recognition in truncated hemoglobins. J Inorg Biochemistry 99, 97-109.
21. Milani M, Pesce A, Ouellet H, Guertin M, &, Bolognesi M, (2003) Truncated hemoglobins and nitric oxide action. IUBMB Life 55, 623-627.
22. Egawa T, &, Yeh SR, (2005) Structural and functional properties of hemoglobins from unicellular organisms as revealed by resonance Raman spectroscopy. J Inorg Biochem 99, 72-96.
23. Das TK, Couture M, Lee HC, Peisach J, Rousseau DL, Wittenberg BA, Wittenberg JB, &, Guertin M, (1999) Identification of the ligands to the ferric heme of Chlamydomonas chloroplast hemoglobin: evidence for ligation of tyrosine-63 (B10) to the heme. Biochemistry 38, 15360-15368.
24. Caillet-Saguy C, Turano P, Piccioli M, Lukat-Rodgers GS, Czjzek M, Guigliarelli B, Izadi-Pruneyre N, Rodgers KR, Delepierre M, &, Lecroisey A, (2008) Deciphering the structural role of histidine 83 for heme binding in hemophore HasA. J Biol Chem 283, 5960-5970.
25. Alontaga AY, Rodriguez JC, Schonbrunn E, Becker A, Funke T, Yukl ET, Hayashi T, Stobaugh J, Moenne-Loccoz P, &, Rivera M, (2009) Structural characterization of the hemophore HasAp from Pseudomonas aeruginosa: NMR spectroscopy reveals protein-protein interactions between Holo-HasAp and hemoglobin. Biochemistry 48, 96-109.
26. Smulevich G, Miller MA, Kraut J, &, Spiro TG, (1991) Conformational change and histidine control of heme chemistry in cytochrome c peroxidase: resonance Raman evidence from Leu-52 and Gly-181 mutants of cytochrome c peroxidase. Biochemistry 30, 9546-9558.
27. Que L, (1988) Metal-tyrosinate proteins. In Biological Applications of Raman Spectroscopy (, Spiro TG, ed), pp. 491-521. Wiley, NY.
28. Nagai M, Yoneyama Y, &, Kitagawa T, (1989) Characteristics in tyrosine coordinations of four hemoglobins M probed by resonance Raman spectroscopy. Biochemistry 28, 2418-2422.
29. Aki Y, Nagai M, Nagai Y, Imai K, Aki M, Sato A, Kubo M, Nagatomo S, &, Kitagawa T, (2010) Differences in coordination states of substituted tyrosine residues and quaternary structures among hemoglobin M probed by resonance Raman spectroscopy. J Biol Inorg Chem 15, 147-158.
30. Sharma KD, Andersson LA, Loehr TM, Terner J, &, Goff HM, (1989) Comparative spectral analysis of mammalian, fungal, and bacterial catalases. Resonance Raman evidence for iron-tyrosinate coordination. J Biol Chem 264, 12772-12779.
31. Eakanunkul S, Lukat-Rodgers GS, Sumithran S, Ghosh A, Rodgers KR, Dawson JH, &, Wilks A, (2005) Characterization of the periplasmic heme-binding protein shut from the heme uptake system of Shigella dysenteriae. Biochemistry 44, 13179-13191.
32. Nicoletti FP, Howes BD, Fittipaldi M, Fanali G, Fasano M, Ascenzi P, &, Smulevich G, (2008) Ibuprofen induces an allosteric conformational transition in the heme complex of human serum albumin with significant effects on heme ligation. J Am Chem Soc 130, 11677-11688.
33. Reeder BJ, Svistunenko DA, &, Wilson MT, (2011) Lipid binding to cytoglobin leads to a change in haem co-ordination: a role for cytoglobin in lipid signalling of oxidative stress. Biochemistry 434, 483-492.
34. Cerda-Colon JF, Silfa E, &, Lopez-Garriga J, (1998) Unusual rocking freedom of the heme in the hydrogen sulfide-binding hemoglobin from Lucina pectinata. J Am Chem Soc 120, 9312-9317.
35. Kraus DW, Wittenberg JB, Lu JF, &, Peisach J, (1990) Hemoglobins of the Lucina pectinata bacteria symbiosis. II. An electron paramagnetic resonance and optical spectral study of the ferric proteins. J Biol Chem 265, 16054-16059.
36. Feis A, Marzocchi MP, Paoli M, &, Smulevich G, (1994) Spin state and axial ligand bonding in the hydroxide complexes of metmyoglobin, methemoglobin, and horseradish peroxidase at room and low temperatures. Biochemistry 33, 4577-4583.
37. Mukai M, Savard PY, Ouellet H, Guertin M, &, Yeh SR, (2002) Unique ligand-protein interactions in a new truncated hemoglobin from Mycobacterium tuberculosis. Biochemistry 41, 3897-3905.
38. Nicoletti FP, Bustamante JP, Droghetti E, Howes BD, Fittipaldi M, Bonamore A, Baiocco P, Feis A, Boffi A, Estrin DA, et al,. (2014) Interplay of the H-bond donor-acceptor role of the distal residues in hydroxyl ligand stabilization of Thermobifida fusca truncated hemoglobin. Biochemistry 53, 8021-8030.
39. Yeh SR, Couture M, Ouellet Y, Guertin M, &, Rousseau DL, (2000) A cooperative oxygen binding hemoglobin from Mycobacterium tuberculosis. Stabilization of heme ligands by a distal tyrosine residue. J Biol Chem 275, 1679-1684.
40. Couture M, Das TK, Savard P-Y, Ouellet Y, Wittenberg JB, Wittenberg BA, Rousseau DL, &, Guertin M, (2000) Structural investigations of the hemoglobin of the cyanobacterium Synechocystis PCC6803 reveal a unique distal heme pocket. Eur J Biochem 267, 4770-4780.
41. Das TK, Franzen S, Pond A, Dawson JH, &, Rousseau DL, (1999) Formation of a five-coordinate hydroxide-bound heme in the His93Gly mutant of sperm whale myoglobin. Inorg Chem 38, 1952-1953.
42. Das TK, Boffi A, Chiancone E, &, Rousseau DL, (1999) Hydroxide rather than histidine is coordinated to the heme in five-coordinate ferric Scapharca inaequivalvis hemoglobin. J Biol Chem 274, 2916-2919.
43. Howes BD, Rodriguez-Lopez JN, Smith AT, &, Smulevich G, (1997) Mutation of distal residues of horseradish peroxidase: influence on substrate binding and cavity properties. Biochemistry 36, 1532-1543.
44. Boechi L, Martí MA, Milani M, Bolognesi M, Luque FJ, &, Estrin DA, (2008) Structural determinants of ligand migration in Mycobacterium tuberculosis truncated hemoglobin O. Proteins 73, 372-379.
45. Boechi L, Mañez PA, Luque FJ, Marti MA, &, Estrin DA, (2010) Unraveling the molecular basis for ligand binding in truncated hemoglobins: the trHbO Bacillus subtilis case. Proteins 78, 962-970.
46. Droghetti E, Nicoletti FP, Bonamore A, Boechi L, Arroyo Manez P, Estrin DA, Boffi A, Smulevich G, &, Feis A, (2010) Heme pocket structural properties of a bacterial truncated hemoglobin from Thermobifida fusca. Biochemistry 49, 10394-10402.
47. Feis A, Lapini B, Catacchio B, Brogioni S, Foggi P, Chiancone E, Boffi A, &, Smulevich G, (2008) Unusually strong H-bonding to the heme ligand and fast geminate recombination dynamics of the carbon monoxide complex of Bacillus subtilis truncated hemoglobin. Biochemistry 47, 902-910.
48. Chen Z, Cheng CH, Zhang J, Cao L, Chen L, Zhou L, Jin Y, Ye H, Deng C, Dai Z, et al,. (2008) Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish. Proc Natl Acad Sci USA 105, 12944-12949.
49. Rodrigues DF, &, Tiedje JM, (2008) Coping with our cold planet. Appl Eviron Microbiol 74, 1677-1686.
50. D'Amico S, Collins T, Marx JC, Feller G, &, Gerday C, (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7, 385-389.
51. Siddiqui KS, &, Cavicchioli R, (2006) Cold-adapted enzymes. Annu Rev Biochem 75, 403-433.
52. Riccio A, Vitagliano L, di Prisco G, Zagari A, &, Mazzarella L, (2002) The crystal structure of a tetrameric hemoglobin in a partial hemichrome state. Proc Natl Acad Sci USA 99, 9801-9806.
53. Giordano D, Boechi L, Vergara A, Martí MA, Samuni U, Dantsker D, Grassi L, Estrin DA, Friedman JM, Mazzarella L, et al,. (2009) The hemoglobins of the sub-Antarctic fish Cottoperca gobio, a phyletically basal species-oxygen-binding equilibria, kinetics and molecular dynamics. FEBS J 276, 2266-2277.
54. Boron I, Russo R, Boechi L, Cheng CH, di Prisco G, Estrin DA, Verde C, &, Nadra AD, (2011) Structure and dynamics of Antarctic fish neuroglobin assessed by computer simulations. IUBMB Life 63, 206-213.
55. Balsamo A, Sannino F, Merlino A, Parrilli E, Tutino ML, Mazzarella L, &, Vergara A, (2012) Role of the tertiary and quaternary structure in the formation of bis-histidyl adducts in cold-adapted hemoglobins. Biochimie 94, 953-960.
56. Smulevich G, Wang Y, Mauro JM, Wang JM, Fishel LA, Kraut J, &, Spiro TG, (1990) Single-crystal resonance Raman spectroscopy of site-directed mutants of cytochrome c peroxidase. Biochemistry 29, 7174-7180.
57. Indiani C, Santoni E, Becucci M, Boffi A, Fukuyama F, &, Smulevich G, (2003) New insight into the peroxidase-hydroxamic acid interaction revealed by the combination of spectroscopic and crystallographic studies. Biochemistry 42, 14066-14074.
58. Sezer M, Santos A, Kielb P, Pinto T, Martins LO, &, Todorovic S, (2013) Distinct structural and redox properties of the heme active site in bacterial dye decolorizing peroxidase-type peroxidases from two subfamilies: resonance Raman and electrochemical study. Biochemistry 52, 3074-3084.
59. Ouellet H, Juszczak L, Dantsker D, Samuni U, Ouellet YH, Savard PY, Wittenberg JB, Wittenberg BA, Friedman JM, &, Guertin M, (2003) Reactions of Mycobacterium tuberculosis truncated hemoglobin O with ligands reveal a novel ligand-inclusive hydrogen bond network. Biochemistry 42, 5764-5774.
60. Marcelli A, Abbruzzetti S, Bustamante JP, Feis A, Bonamore A, Boffi A, Gellini C, Salvi PR, Estrin DA, Bruno S, et al,. (2012) Following ligand migration pathways from picoseconds to milliseconds in type II truncated hemoglobin from Thermobifida fusca. PLoS One 7, e39884.
61. Leslie AGM, (2003) MOSFLM User Guide, Mosflm Version 6.2.3. MRC Laboratory of Molecular Biology, Cambridge, UK.
62. Evans P, (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62, 72-82.
63. Claude JB, Suhre K, Notredame C, Claverie JM, &, Abergel C, (2004) CaspR: a web-server for automated molecular replacement using homology modelling. Nucleic Acids Res 32, 606-609.
64. Emsley P, &, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-2132.
65. Murshudov GN, Vagin AA, &, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53, 240-255.
66. Laskowski RA, (1995) SURFNET: a program for visualizing molecular surfaces, cavities, and intermolecular interactions. J Mol Graph 13, 323-330.
67. Pearlman DA, Case DA, Caldwell JW, Ross WS, Cheatham TE III, DeBolt S, Ferguson D, Seibel G, &, Kollman P, (1995) AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comput Phys Commun 91, 1-41.
68. Ryckaert JP, Ciccotti G, &, Berendsen HJC, (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 23, 327-341.
69. Cohen J, Olsen KW, &, Schulten K, (2008) Finding gas migration pathways in proteins using implicit ligand sampling. Methods Enzymol 437, 439-457.
70. Forti F, Boechi L, Estrin DA, &, Marti MA, (2011) Comparing and combining implicit ligand sampling with multiple steered molecular dynamics to study ligand migration processes in heme proteins. J Comput Chem 32, 2219-2231.