Biochemical and structural analysis of the Bacillus subtilis ABC transporter OpuA and its isolated subunits

Journal of Molecular Microbiology and Biotechnology

Volumn 10, Issue 2-4, 2006, Pages 76-91

  Horn, Carsten ^a   Jenewein, Stefan ^a   Sohn Bösser, Linda ^b   Bremer, Erhard ^b   Schmitt, Lutz ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

B. subtilis, osmoprotection; B. subtilis, re association of intact OpuA transporter; OpuA, in vitro analysis; OpuA, in vivo studies; OpuAA, motor domain; SBP OpuAC, from specificity to recognition

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATE; BETAINE; BINDING PROTEIN; CYTOPLASM PROTEIN; MEMBRANE PROTEIN; PROLINE; PROTEIN OPUA; PROTEIN OPUAA; PROTEIN OPUAB; PROTEIN OPUAC; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

BACTERIAL GROWTH; BACTERIAL SURVIVAL; NONHUMAN; OSMOREGULATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN QUATERNARY STRUCTURE; SHORT SURVEY; SOIL MICROFLORA; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ATP-BINDING CASSETTE TRANSPORTERS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BINDING SITES; DIMERIZATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN SUBUNITS; SEQUENCE HOMOLOGY, AMINO ACID;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); OPUA; POSIBACTERIA;

EID: 33744484737     PISSN: 14641801     EISSN: None     Source Type: Journal    
DOI: 10.1159/000091556     Document Type: Short Survey

References (102)

1. Agre P, Kozono D: Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett 2003;555:72-78.
2. Ames GF: Bacterial periplasmic transport systems: structure, mechanism, and evolution. Annu Rev Biochem 1986;55:397-425.
3. Ames GF, Nikaido K, Wang IX, Liu PQ, Liu CE, Hu C: Purification and characterization of the membrane-bound complex of an ABC transporter, the histidine permease. J Bioenerg Biomembr 2001;33:79-92.
4. Arakawa T, Timasheff SN: The stabilization of proteins by osmolytes. Biochem J 1985;47:411-414.
5. Arechaga I, Miroux B, Karrasch S, Huijbregts R, de Kruijff B, Runswick MJ, Walker JE: Characterisation of new intracellular membranes in Escherichia coli accompanying large-scale over-production of the b subunit of F(1)F(o) ATP synthase. FEBS Lett 2000;482:215-219.
6. Banerjee R, Zou CG: Redox regulation and reaction mechanism of human cystathionine-β-synthase: a PLP-dependent hemesensor protein. Arch Biochem Biophys 2005;433:144-156.
7. Boch J, Kempf B, Bremer E: Osmoregulation in Bacillus subtilis; synthesis of the osmoprotectant glycine betaine from exogenously provided choline. J Bacteriol 1994;176:5364-5371.
8. Booth IR, Louis P: Managing hypoosmotic stress: aquaporins and mechanosensitive channels in Escherichia coli. Curr Opin Microbiol 1999;2:166-169.
9. Bremer E: Adaptation to changing osmolarity; in Sonenshein AL, Hoch JA, Losick R (eds): Bacillus subtilis and Its Closest Relatives. Washington, ASM Press, 2002, pp 385-391.
10. Bremer E, Krämer R: Coping with osmotic challenges: osmoregulation through accumulation and release of compatible solutes in bacteria; in Storz G, Hengge-Aronis R (eds): Bacterial Stress Responses. Washington, ASM, 2000, pp 79-97.
11. Brigulla M, Hoffmann T, Krisp A, Völker A, Bremer E, Völker U: Chill induction of the SigB-dependent general stress response in Bacillus subtilis and its contribution to low-temperature adaptation. J Bacteriol 2003;185:4305-4314.
12. Calamita G: The Escherichia coli aquaporin-Z water channel. Mol Microbiol 2000;37:254-262.
13. Calamita G, Kempf B, Bonhivers M, Bishai WR, Bremer E, Agre P: Regulation of the Escherichia coli water channel gene aqpZ. Proc Natl Acad Sci USA 1998;95:3627-3631.
14. Chang G: Structure of MsbA from Vibrio cholera: a multidrug resistance ABC transporter homolog in a closed conformation. J Mol Biol 2003;330:419-430.
15. Chang G, Roth CB: Structure of MsbA from E. coli: a homolog of the multidrug resistance ATP-binding cassette (ABC) transporters. Science 2001;293:1793-1800.
16. Chen J, Lu G, Lin J, Davidson AL, Quiocho FA: A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol Cell 2003;12:651-661.
17. Csonka LN, Epstein W: Osmoregulation; in Neidhardt FC (ed): Escherichia and Salmonella. Cellular and Molecular Biology. Washington, ASM Press, 1996, pp 1210-1223.
18. Dattananda CS, Gowrishankar J: Osmoregulation in Escherichia coli: complementation analysis and gene-protein relationships in the proU locus. J Bacteriol 1989;171:1915-1922.
19. Davidson AL: Mechanism of coupling of transport to hydrolysis in bacterial ATP-binding cassette transporters. J Bacteriol 2002;184:1225-1233.
20. Davidson AL, Chen J: ATP-binding cassette transporters in bacteria. Annu Rev Biochem 2004;73:241-268.
21. Diederichs K, Diez J, Greller G, Muller C, Breed J, Schnell C, Vonrhein C, Boos W, Welte W: Crystal structure of MalK, the ATPase subunit of the trehalose/maltose ABC transporter of the archaeon Thermococcus litoralis. EMBO J 2000;19:5951-5961.
22. Doige CA, Ames GF: ATP-dependent transport systems in bacteria and humans: relevance to cystic fibrosis and multidrug resistance. Annu Rev Microbiol 1993;47:291-319.
23. Ehrmann M, Ehrle R, Hofmann E, Boos W, Schlosser A: The ABC maltose transporter. Mol Microbiol 1998;29:685-694.
24. +-ATPase: evidence for two classes of nucleotide sites. Biochemistry 1989;28:6771-6778.
25. (+)-ATPase: evidence for cofactor-induced conformational changes in the enzyme. Biochemistry 1990;29:3179-3186.
26. Fersht A: Enzyme Structure and Mechanism, ed 2. New York, Freeman, 1997.
27. Fetch EE, Davidson AL: Vanadate-catalyzed photocleavage of the signature motif of an ATP-binding cassette (ABC) transporter. Proc Natl Acad Sci USA 2002;99:9685-9690.
28. Fukami-Kobayashi K, Tateno Y, Nishikawa K: Domain dislocation: a change of core structure in periplasmic binding proteins in their evolutionary history. J Mol Biol 1999;286:279-290.
29. Galinski EA, Trüper HG: Microbial behaviour in salt-stressed ecosystems. FEMS Microbiol Rev 1994;15:95-108.
30. Gaudet R, Wiley DC: Structure of the ABC ATPase domain of human TAP1, the transporter associated with antigen processing. EMBO J 2001;20:4964-4972.
31. Gowrishankar J: Nucleotide sequence of the osmoregulatory proU operon of Escherichia coli. J Bacteriol 1989;171:1923-1931.
32. Greller G, Horlacher R, DiRuggiero J, Boos W: Molecular and biochemical analysis of MalK, the ATP-hydrolyzing subunit of the trehalose/maltose transport system of the hyperthermophilic archaeon Thermococcus litoralis. J Biol Chem 1999;274:20259-20264.
33. Haardt M, Bremer E: Use of phoA and lacZ fusions to study the membrane topology of ProW, a component of the osmoregulated ProU transport system of Escherichia coli. J Bacteriol 1996;178:5370-5381.
34. Haardt M, Kempf B, Faatz E, Bremer E: The osmoprotectant proline betaine is a major substrate for the binding-protein-dependent transport system ProU of Escherichia coli K-12. Mol Gen Genet 1995;246:783-786.
35. Higgins CF: ABC transporters: from microorganisms to man. Annu Rev Cell Biol 1992;8:67-113.
36. + uptake systems in Bacillus subtilis and their role in adaptation to hypertonicity. J Bacteriol 2003;185:1289-1298.
37. Holtmann G, Bremer E: Thermoprotection of Bacillus subtilis by exogenously provided glycine betaine and structurally related compatible solutes: involvement of Opu transporters. J Bacteriol 2004;186:1683-1693.
38. Hor LI, Shuman HA: Genetic analysis of periplasmic binding protein-dependent transport in Escherichia coli. Each lobe of maltose-binding protein interacts with a different subunit of the MalFGK2 membrane transport complex. J Mol Biol 1993;233:659-670.
39. Horn C, Bremer E, Schmitt L: Nucleotide-dependent monomer/dimer equilibrium of OpuAA, the nucleotide-binding protein of the osmotically regulated ABC transporter OpuA from Bacillus subtilis. J Mol Biol 2003;334:403-419.
40. Horn C, Bremer E, Schmitt L: Functional overexpression and re-association of OpuA, an osmotically regulated ABC-transporter from Bacillus subtilis. FEBS Lett 2005;579:5765-5768.
41. Hung LW, Wang IXY, Nikaido K, Liu PQ, Ames GFL, Kim SH: Crystal structure of the ATP-binding subunit of an ABC transporter. Nature 1998;396:703-707.
42. Janas E, Hofacker M, Chen M, Gompf S, van der Does C, Tampe R: The ATP hydrolysis cycle of the nucleotide-binding domain of the mitochondrial ATP-binding cassette transporter Mdl1p. J Biol Chem 2003;278:26862-26869.
43. + and ionic strength directly influence the autophosphorylation activity of the putative turgor sensor KdpD of Escherichia coli. J Biol Chem 2000;275:40142-40147.
44. Kappes RM, Kempf B, Bremer E: Three transport systems for the osmoprotectant glycine betaine operate in Bacillus subtilis: characterization of OpuD. J Bacteriol 1996;178:5071-5079.
45. Kappes RM, Kempf B, Kneip S, Boch J, Gade J, Meier-Wagner J, Bremer E: Two evolutionarily closely related ABC transporters mediate the uptake of choline for synthesis of the osmoprotectant glycine betaine in Bacillus subtilis. Mol Microbiol 1999;32:203-216.
46. Kempf B, Bremer E: OpuA, an osmotically regulated binding protein-dependent transport system for the osmoprotectant glycine betaine in Bacillus subtilis. J Biol Chem 1995;270:16701-16713.
47. Kempf B, Bremer E: Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch Microbiol 1998;170:319-330.
48. Kempf B, Gade J, Bremer E: Lipoprotein from the osmoregulated ABC transport system OpuA of Bacillus subtilis: purification of the glycine betaine binding protein and characterization of a functional lipidless mutant. J Bacteriol 1997;179:6213-6220.
49. Ko R, Smith LT: Identification of an ATP-driven, osmoregulated glycine betaine transport system in Listeria monocytogenes. Appl Environ Microbiol 1999;65:4040-4048.
50. Kramer R, Morbach S: BetP of Corynebacterium glutamicum, a transporter with three different functions: betaine transport, osmosensing, and osmoregulation. Biochim Biophys Acta 2004;1658:31-36.
51. Liu CE, Liu PQ, Ames GF: Characterization of the adenosine triphosphatase activity of the periplasmic histidine permease, a traffic ATPase (ABC transporter). J Biol Chem 1997;272:21883-21891.
52. Liu PQ, Ames GF: In vitro disassembly and reassembly of an ABC transporter, the histidine permease. Proc Natl Acad Sci USA 1998;95:3495-3500.
53. Locher KP, Lee AT, Rees DC: The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 2002;296:1091-1098.
54. Ma JC, Dougherty DA: The cation-pi Interaction. Chem Rev 1997;97:1303-1324.
55. Mao B, Pear MR, McCammon JA, Quiocho FA: Hinge-bending in L-arabinose-binding protein. The 'Venus's-flytrap' model. J Biol Chem 1982;257:1131-1133.
56. May G, Faatz E, Villarejo M, Bremer E: Binding protein dependent transport of glycine betaine and its osmotic regulation in Escherichia coli K12. Mol Gen Genet 1986;205:225-233.
57. Miller KJ, Wood JM: Osmoadaptation by rhizosphere bacteria. Annu Rev Microbiol 1996;50:101-136.
58. Miroux B, Walker JE: Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J Mol Biol 1996;260:289-298.
59. Moody JE, Millen L, Binns D, Hunt JF, Thomas PJ: Cooperative, ATP-dependent association of the nucleotide binding cassettes during the catalytic cycle of ATP-binding cassette transporters. J Biol Chem 2002;277:21111-21114.
60. Morbach S, Tebbe S, Schneider E: The ATP-binding cassette (ABC) transporter for maltose/maltodextrins of Salmonella typhimurium. Characterization of the ATPase activity associated with the purified MalK subunit. J Biol Chem 1993;268:18617-18621.
61. Obis D, Guillot A, Gripon JC, Renault P, Bolotin A, Mistou MY: Genetic and biochemical characterization of a high-affinity betaine uptake system (BusA) in Lactococcus lactis reveals a new functional organization within bacterial ABC transporters. J Bacteriol 1999;181:6238-6246.
62. Panagiotidis CH, Boos W, Shuman HA: The ATP-binding cassette subunit of the maltose transporter MalK antagonizes MalT, the activator of the Escherichia coli mal regulon. Mol Microbiol 1998;30:535-546.
63. Peter H, Burkovski A, Krämer R: Isolation, characterization, and expression of the Corynebacterium glutamicum betP gene, encoding the transport system for the compatible solute glycine betaine. J Bacteriol 1996;178:5229-5234.
64. Quiocho FA, Ledvina PS: Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes. Mol Microbiol 1996;20:17-25.
65. Record MT Jr, Courtenay ES, Cayley DS, Guttman HJ: Responses of E. coli to osmotic stress: large changes in amounts of cytoplasmic solutes and water. Trends Biochem Sci 1998a;23:143-148.
66. Record MT Jr, Courtenay ES, Cayley S, Guttman HJ: Biophysical compensation mechanisms buffering E. coli protein-nucleic acid interactions against changing environments. Trends Biochem Sci 1998b;23:190-194.
67. Reyes CL, Chang G: Structure of the ABC transporter MsbA in complex with ADP vanadate and lipopolysaccharide. Science 2005;308:1028-1031.
68. Saier MH Jr: Families of transmembrane transporters selective for amino acids and their derivatives. Microbiology 2000;146:1775-1795.
69. Samanta S, Ayvaz T, Reyes M, Shuman HA, Chen J, Davidson AL: Disulfide cross-linking reveals a site of stable interaction between C-terminal regulatory domains of the two MalK subunits in the maltose transport complex. J Biol Chem 2003;278:35265-35271.
70. Scheffel F, Demmer U, Warkentin E, Hulsmann A, Schneider E, Ermler U: Structure of the ATPase subunit CysA of the putative sulfate ATP-binding cassette (ABC) transporter from Alicyclobacillus acidocaldarius. FEBS Lett 2005;579:2953-2958.
71. Schiefner A, Breed J, Bosser L, Kneip S, Gade J, Holtmann G, Diederichs K, Welte W, Bremer E: Cation-pi interactions as determinants for binding of the compatible solutes glycine betaine and proline betaine by the periplasmic ligand-binding protein ProX from Escherichia coli. J Biol Chem 2004;279:5588-5596.
72. + as an osmotic stimulus. Biochemistry 2004;43:5583-5591.
73. Schmitt L, Benabdelhak H, Blight MA, Holland IB, Stubbs MT: Crystal structure of the ABC-domain of the ABC-transporter HlyB: Identification of a variable region within the helical domain of ABC domains. J Mol Biol 2003;330:333-342.
74. Schmitt L, Tampé R: Structure and mechanism of ABC transporters. Cur Opin Struct Biol 2002;12:754-760.
75. Schneider E: ABC transporters catalyzing carbohydrate uptake. Res Microbiol 2001;152:303-310.
76. Sharff AJ, Rodseth LE, Spurlino JC, Quiocho FA: Crystallographic evidence of a large ligand-induced hinge-twist motion between the two domains of the maltodextrin binding protein involved in active transport and chemotaxis. Biochemistry 1992;31:10657-10663.
77. Sharma S, Davidson AL: Vanadate-induced trapping of nucleotides by purified maltose transport complex requires ATP hydrolysis. J Bacteriol 2000;182:6570-6576.
78. Sharma S, Davis JA, Ayvaz T, Traxler B, Davidson AL: Functional reassembly of the Escherichia coli maltose transporter following purification of a MalF-MalG subassembly. J Bacteriol 2005;187:2908-2911.
79. Smith PC, Karpowich N, Millen L, Moody JE, Rosen J, Thomas PJ, Hunt JF: ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol Cell 2002;10:139-149.
80. B-dependent stress-responsive promoters. Mol Microbiol 1998;29:285-296.
81. Strange K: Cellular volume homeostasis. Adv Physiol Educ 2004;28:155-159.
82. Strøm AR, Kaasen I: Trehalose metabolism in Escherichia coli: stress protection and stress regulation of gene expression. Mol Microbiol 1993;8:205-210.
83. +-uptake systems; in Konings WN, Kaback HR, Lolkema JS (eds): Transport Processes in Eukaryotic and Prokaryotic Organisms. Handbook of Biological Physics. Amsterdam, Elsevier, 1996, vol 2, pp 473-499.
84. Tam R, Saier MH Jr: Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev 1993;57:320-346.
85. Treptow NA, Shuman HA: Genetic evidence for substrate and periplasmic-binding-protein recognition by the MalF and MalG proteins, cytoplasmic membrane components of the Escherichia coli maltose transport system. J Bacteriol 1985;163:654-660.
86. Van der Heide T, Poolman B: Glycine betaine transport in Lactococcus lactis is osmotically regulated at the level of expression and translocation activity. J Bacteriol 2000a;182:203-206.
87. Van der Heide T, Poolman B: Osmoregulated ABC-transport system of Lactococcus lactis senses water stress via changes in the physical state of the membrane. Proc Natl Acad Sci USA 2000b;97:7102-7106.
88. Van der Heide T, Poolman B: ABC transporters: one, two or four extracytoplasmic substrate-binding sites? EMBO Rep 2002;3:938-943.
89. Van der Heide T, Stuart MC, Poolman B: On the osmotic signal and osmosensing mechanism of an ABC transport system for glycine betaine. EMBO J 2001;20:7022-7032.
90. Ventosa A, Nieto JJ, Oren A: Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 1998;62:504-544.
91. Verdon G, Albers SV, Dijkstra BW, Driessen AJ, Thunnissen AM: Crystal structures of the ATPase subunit of the glucose ABC transporter from Sulfolobus solfataricus: nucleotide-free and nucleotide-bound conformations. J Mol Biol 2003;330:343-358.
92. Von Blohn C, Kempf B, Kappes RM, Bremer E: Osmostress response in Bacillus subtilis: characterization of a proline uptake system (OpuE) regulated by high osmolarity and the alternative transcription factor sigma B. Mol Microbiol 1997;25:175-187.
93. Walker JE, Saraste M, Runswick MJ, Gay NJ: Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1982;1:945-951.
94. Welsh DT: Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol Rev 2000;24:263-290.
95. Whatmore AM, Chudek JA, Reed RH: The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis. J Gen Microbiol 1990;136:2527-2535.
96. + in turgor regulation. J Gen Microbiol 1990;136:2521-2526.
97. Wood JM: Osmosensing by bacteria: signals and membrane-based sensors. Microbiol Mol Biol Rev 1999;63:230-262.
98. Yancey PH: Compatible and counteracting solutes; in Strange K (ed): Cellular and Molecular Physiology of Cell Volume Regulation. Boca Raton, CRC Press, 1994, pp 81-109.
99. Yuan YR, Blecker S, Martsinkevich O, Millen L, Thomas PJ, Hunt JF: The crystal structure of the MJ0796 ATP-binding cassette. Implications for the structural consequences of ATP hydrolysis in the active site of an ABC transporter. J Biol Chem 2001;276:32313-32321.
100. Zaitseva J, Jenewein S, Jumpertz T, Holland IB, Schmitt L: H662 is the linchpin of ATP hydrolysis in the nucleotide-binding domain of the ABC transporter HlyB. EMBO J 2005a;24:1901-1910.
101. Zaitseva J, Jenewein S, Wiedenmann A, Benabdelhak H, Holland IB, Schmitt L: Functional characterization and ATP-induced dimerization of the isolated ABC domain of the haemolysin B transporter. Biochemistry 2005b;44:9680-9690.
102. Zaitseva J, Zhang H, Binnie RA, Hermodson M: The proteins encoded by the rbs operon of Escherichia coli. II. Use of chimeric protein constructs to isolate and characterize RbsC. Protein Sci 1996;5:1100-1107.