Tripartite ATP-independent periplasmic (TRAP) transporters in bacteria and archaea

FEMS Microbiology Reviews

Volumn 35, Issue 1, 2011, Pages 68-86

  Mulligan, Christopher ^a   Fischer, Marcus ^a   Thomas, Gavin H ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Extracytoplasmic solute receptor; Periplasmic binding protein; Sialic acid; SiaP; TRAP transporter; Tripartite ATP independent periplasmic

Indexed keywords

2 OXOBUTYRIC ACID; 2,3 DIOXOGULONIC ACID; 4 CHLOROBENZOIC ACID; ABC TRANSPORTER; AMINO ACID TRANSPORTER; BINDING PROTEIN; CARRIER PROTEIN; DEOXYCYTIDINE TRIPHOSPHATE; ECTOINE; GLUCONIC ACID; LACTIC ACID; MALONIC ACID; PROTEIN SIAP; PYRUVIC ACID; SIALIC ACID; TAURINE; TRIPARTITE ATP INDEPENDENT PERIPLASMIC TRANSPORTER; UNCLASSIFIED DRUG;

ARCHAEBACTERIUM; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GENOME; BINDING SITE; BIODIVERSITY; CATABOLISM; COMPUTER MODEL; GENE EXPRESSION; HAEMOPHILUS INFLUENZAE; HALOMONAS; IN VIVO STUDY; LIGAND BINDING; NONHUMAN; OSMOTIC PRESSURE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN STRUCTURE; RHODOBACTER CAPSULATUS; RHODOBACTER SPHAEROIDES; SIAPQM GENE;

ARCHAEA; ARCHAEAL PROTEINS; BACTERIA; BACTERIAL PROTEINS; MEMBRANE TRANSPORT PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PERIPLASMIC PROTEINS;

EUKARYOTA; HAEMOPHILUS INFLUENZAE; PROKARYOTA;

EID: 78649982124     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2010.00236.x     Document Type: Article

References (89)

1. Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR & Iwata S (2003) Structure and mechanism of the lactose permease of Escherichia coli. Science 301: 610-615.
2. Akiyama N, Takeda K & Miki K (2009) Crystal structure of a periplasmic substrate-binding protein in complex with calcium lactate. J Mol Biol 392: 559-565.
3. Allen S, Zaleski A, Johnston JW, Gibson BW & Apicella MA (2005) Novel sialic acid transporter of Haemophilusinfluenzae. Infect Immun 73: 5291-5300.
4. Almagro-Moreno S & Boyd EF (2009) Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine. Infect Immun 77: 3807-3816.
5. An JH, Lee HY, Ko KN, Kim ES & Kim YS (2002) Symbiotic effects of deltamatB Rhizobium leguminosarum bv. trifolii mutant on clovers. Mol Cells 14: 261-266.
6. Angata T & Varki A (2002) Chemical diversity in the sialic acids and related alpha-keto acids: an evolutionary perspective. Chem Rev 102: 439-469.
7. Asai K, Baik SH, Kasahara Y, Moriya S & Ogasawara N (2000) Regulation of the transport system for C4-dicarboxylic acids in Bacillus subtilis. Microbiology 146: 263-271.
8. Badia J, Ibanez E, Sabate M, Baldoma L & Aguilar J (1998) A rare 920-kilobase chromosomal inversion mediated by IS1 transposition causes constitutive expression of the yiaK-S operon for carbohydrate utilization in Escherichia coli. J Biol Chem 273: 8376-8381.
9. Bakermans C, Sloup RE, Zarka DG, Tiedje JM & Thomashow MF (2009) Development and use of genetic system to identify genes required for efficient low-temperature growth of Psychrobacter arcticus 273-4. Extremophiles 13: 21-30.
10. Bode AM, Cunningham L & Rose RC (1990) Spontaneous decay of oxidized ascorbic acid (dehydro-l-ascorbic acid) evaluated by high-pressure liquid chromatography. Clin Chem 36: 1807-1809.
11. Bouchet V, Hood DW, Li J et al. (2003) Host-derived sialic acid is incorporated into Haemophilusinfluenzae lipopolysaccharide and is a major virulence factor in experimental otitis media. P Natl Acad Sci USA 100: 8898-8903.
12. Bruggemann C, Denger K, Cook AM & Ruff J (2004) Enzymes and genes of taurine and isethionate dissimilation in Paracoccus denitrificans. Microbiology 150: 805-816.
13. Chae JC, Kim Y, Kim YC, Zylstra GJ & Kim CK (2000) Genetic structure and functional implication of the fcb gene cluster for hydrolytic dechlorination of 4-chlorobenzoate from Pseudomonas sp. DJ-12. Gene 258: 109-116.
14. Contzen M & Stolz A (2000) Characterization of the genes for two protocatechuate 3, 4-dioxygenases from the 4-sulfocatechol-degrading bacterium Agrobacterium radiobacter strain S2. J Bacteriol 182: 6123-6129.
15. Cuneo MJ, Changela A, Miklos AE, Beese LS, Krueger JK & Hellinga HW (2008) Structural analysis of a periplasmic binding protein in the tripartite ATP-independent transporter family reveals a tetrameric assembly that may have a role in ligand transport. J Biol Chem 283: 32812-32820.
16. Davidson AL, Dassa E, Orelle C & Chen J (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol R 72: 317-364.
17. Dean DA, Davidson AL & Nikaido H (1989) Maltose transport in membrane vesicles of Escherichia coli is linked to ATP hydrolysis. P Natl Acad Sci USA 86: 9134-9138.
18. Denger K, Smits TH & Cook AM (2006) Genome-enabled analysis of the utilization of taurine as sole source of carbon or of nitrogen by Rhodobacter sphaeroides 2.4.1. Microbiology 152: 3197-3206.
19. Deutsch JC (1998) Spontaneous hydrolysis and dehydration of dehydroascorbic acid in aqueous solution. Anal Biochem 260: 223-229.
20. Dippel R & Boos W (2005) The maltodextrin system of Escherichia coli: metabolism and transport. J Bacteriol 187: 8322-8331.
21. Doeven MK, Abele R, Tampe R & Poolman B (2004) The binding specificity of OppA determines the selectivity of the oligopeptide ATP-binding cassette transporter. J Biol Chem 279: 32301-32307.
22. Eichhorn E, Van DP Jr & Leisinger T (2000) Deletion analysis of the Escherichia coli taurine and alkanesulfonate transport systems. J Bacteriol 182: 2687-2695.
23. +/sugar symport. Science 321: 810-814.
24. Finn RD, Mistry J, Tate J et al. (2010) The Pfam protein families database. Nucleic Acids Res 38: D211-D222.
25. Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Bult CJ, Tomb JF, Dougherty BA & Merrick JM (1995) Whole-genome random sequencing and assembly of Haemophilusinfluenzae Rd. Science 269: 496-512.
26. Forward JA, Behrendt MC, Wyborn NR, Cross R & Kelly DJ (1997) TRAP transporters: a new family of periplasmic solute transport systems encoded by the dctPQM genes of Rhodobactercapsulatus and by homologs in diverse gram-negative bacteria. J Bacteriol 179: 5482-5493.
27. Fuller TE, Kennedy MJ & Lowery DE (2000) Identification of Pasteurella multocida virulence genes in a septicemic mouse model using signature-tagged mutagenesis. Microb Pathogenesis 29: 25-38.
28. Gonin S, Arnoux P, Pierru B, Lavergne J, Alonso B, Sabaty M & Pignol D (2007) Crystal structures of an Extracytoplasmic Solute Receptor from a TRAP transporter in its open and closed forms reveal a helix-swapped dimer requiring a cation for alpha-keto acid binding. BMC Struct Biol 7: 11.
29. Gorzynska AK, Denger K, Cook AM & Smits TH (2006) Inducible transcription of genes involved in taurine uptake and dissimilation by Silicibacter pomeroyi DSS-3T. Arch Microbiol 185: 402-406.
30. Grammann K, Volke A & Kunte HJ (2002) New type of osmoregulated solute transporter identified in halophilic members of the bacteria domain: TRAP transporter TeaABC mediates uptake of ectoine and hydroxyectoine in Halomonas elongata DSM 2581(T). J Bacteriol 184: 3078-3085.
31. Hood DW, Makepeace K, Deadman ME, Rest RF, Thibault P, Martin A, Richards JC & Moxon ER (1999) Sialic acid in the lipopolysaccharide of Haemophilusinfluenzae: strain distribution, influence on serum resistance and structural characterization. Mol Microbiol 33: 679-692.
32. Hosie AH, Allaway D, Jones MA, Walshaw DL, Johnston AW & Poole PS (2001) Solute-binding protein-dependent ABC transporters are responsible for solute efflux in addition to solute uptake. Mol Microbiol 40: 1449-1459.
33. Ibanez E, Campos E, Baldoma L, Aguilar J & Badia J (2000) Regulation of expression of the yiaKLMNOPQRS operon for carbohydrate utilization in Escherichia coli: involvement of the main transcriptional factors. J Bacteriol 182: 4617-4624.
34. Jacobs MH, Van Der Heide T, Driessen AJ & Konings WN (1996) Glutamate transport in Rhodobacter sphaeroides is mediated by a novel binding protein-dependent secondary transport system. P Natl Acad Sci USA 93: 12786-12790.
35. Jenkins GA, Figueira M, Kumar GA, Sweetman WA, Makepeace K, Pelton SI, Moxon R & Hood DW (2010) Sialic acid mediated transcriptional modulation of a highly conserved sialometabolism gene cluster in Haemophilus influenzae and its effect on virulence. BMC Microbiol 10: 48.
36. Jermyn WS & Boyd EF (2002) Characterization of a novel Vibrio pathogenicity island (VPI-2) encoding neuraminidase (nanH) among toxigenic Vibrio cholerae isolates. Microbiology 148: 3681-3693.
37. Jermyn WS & Boyd EF (2005) Molecular evolution of Vibrio pathogenicity island-2 (VPI-2): mosaic structure among Vibrio cholerae and Vibrio mimicus natural isolates. Microbiology 151: 311-322.
38. Johnston JW, Zaleski A, Allen S, Mootz JM, Armbruster D, Gibson BW, Apicella MA & Munson RS Jr (2007) Regulation of sialic acid transport and catabolism in Haemophilus influenzae. Mol Microbiol 66: 26-39.
39. Johnston JW, Coussens NP, Allen S, Houtman JC, Turner KH, Zaleski A, Ramaswamy S, Gibson BW & Apicella MA (2008) Characterization of the N-acetyl-5-neuraminic acid-binding site of the extracytoplasmic solute receptor (SiaP) of nontypeable Haemophilus influenzae strain 2019. J Biol Chem 283: 855-865.
40. Kelly AP & Weed LL (1965) Taurine as a constituent of a bacterial cell wall. J Biol Chem 240: 2519-2523.
41. Kelly DJ & Thomas GH (2001) The tripartite ATP-independent periplasmic (TRAP) transporters of bacteria and archaea. FEMS Microbiol Rev 25: 405-424.
42. Kertesz MA (2000) Riding the sulfur cycle - metabolism of sulfonates and sulfate esters in gram-negative bacteria. FEMS Microbiol Rev 24: 135-175.
43. Kim YS (2002) Malonate metabolism: biochemistry, molecular biology, physiology, and industrial application. J Biochem Mol Biol 35: 443-451.
44. Kogure K (1998) Bioenergetics of marine bacteria. Curr Opin Biotech 9: 278-282.
45. Kolker E, Makarova KS, Shabalina S et al. (2004) Identification and functional analysis of 'hypothetical' genes expressed in Haemophilus influenzae. Nucleic Acids Res 32: 2353-2361.
46. Krogh A, Larsson B, Von Heijne G & Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580.
47. Kuhlmann SI, Terwisscha van Scheltinga AC, Bienert R, Kunte HJ & Ziegler C (2008) 1.55 Å structure of the ectoine binding protein TeaA of the osmoregulated TRAP-transporter TeaABC from Halomonas elongata. Biochemistry 47: 9475-9485.
48. Lecher J, Pittelkow M, Zobel S, Bursy J, Bonig T, Smits SH, Schmitt L & Bremer E (2009) The crystal structure of UehA in complex with ectoine-A comparison with other TRAP-T binding proteins. J Mol Biol 389: 58-73.
49. Lolkema JS & Slotboom DJ (2003) Classification of 29 families of secondary transport proteins into a single structural class using hydropathy profile analysis. J Mol Biol 327: 901-909.
50. Marty-Teysset C, Lolkema JS, Schmitt P, Divies C & Konings WN (1996) The citrate metabolic pathway in Leuconostoc mesenteroides: expression, amino acid synthesis, and alpha-ketocarboxylate transport. J Bacteriol 178: 6209-6215.
51. Mauchline TH, Fowler JE, East AK, Sartor AL, Zaheer R, Hosie AH, Poole PS & Finan TM (2006) Mapping the Sinorhizobiummeliloti 1021 solute-binding protein-dependent transportome. P Natl Acad Sci USA 103: 17933-17938.
52. Miller DM III, Olson JS & Quiocho FA (1980) The mechanism of sugar binding to the periplasmic receptor for galactose chemotaxis and transport in Escherichia coli. J Biol Chem 255: 2465-2471.
53. Miller DM III, Olson JS, Pflugrath JW & Quiocho FA (1983) Rates of ligand binding to periplasmic proteins involved in bacterial transport and chemotaxis. J Biol Chem 258: 13665-13672.
54. Morris RM, Rappé MS, Connon SA, Vergin KL, Siebold WA, Carlson CA & Giovannoni SJ (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420: 806-810.
55. Muller A, Severi E, Mulligan C, Watts AG, Kelly DJ, Wilson KS, Wilkinson AJ & Thomas GH (2006) Conservation of structure and mechanism in primary and secondary transporters exemplified by SiaP, a sialic acid binding virulence factor from Haemophilus influenzae. J Biol Chem 281: 22212-22222.
56. Mulligan C, Kelly DJ & Thomas GH (2007) Tripartite ATP-independent periplasmic transporters: application of a relational database for genome-wide analysis of transporter gene frequency and organization. J Mol Microb Biotech 12: 218-226.
57. Mulligan C, Geertsma ER, Severi E, Kelly DJ, Poolman B & Thomas GH (2009) The substrate-binding protein imposes directionality on an electrochemical sodium gradient-driven TRAP transporter. P Natl Acad Sci USA 106: 1778-1783.
58. Nichols NN & Harwood CS (1995) Repression of 4-hydroxybenzoate transport and degradation by benzoate: a new layer of regulatory control in the Pseudomonas putida beta-ketoadipate pathway. J Bacteriol 177: 7033-7040.
59. Novak RT, Gritzer RF, Leadbetter ER & Godchaux W (2004) Phototrophic utilization of taurine by the purple nonsulfur bacteria Rhodopseudomonas palustris and Rhodobacter sphaeroides. Microbiology 150: 1881-1891.
60. Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol R 63: 334-348.
61. Plantinga TH, Van Der Does C, Badia J, Aguilar J, Konings WN & Driessen AJ (2004) Functional characterization of the Escherichia coli K-12 yiaMNO transport protein genes. Mol Membr Biol 21: 51-57.
62. Plantinga TH, Van Der Does C, Tomkiewicz D, Van Keulen G, Konings WN & Driessen AJ (2005) Deletion of the yiaMNO transporter genes affects the growth characteristics of Escherichia coli K-12. Microbiology 151: 1683-1689.
63. Plumbridge J & Vimr E (1999) Convergent pathways for utilization of the amino sugars N-acetylglucosamine, N-acetylmannosamine, and N-acetylneuraminic acid by Escherichia coli. J Bacteriol 181: 47-54.
64. Poolman B & Konings WN (1993) Secondary solute transport in bacteria. Biochim Biophys Acta 1183: 5-39.
65. Prakash S, Cooper G, Singhi S & Saier MH Jr (2003) The ion transporter superfamily. Biochim Biophys Acta 1618: 79-92.
66. Quintero MJ, Montesinos ML, Herrero A & Flores E (2001) Identification of genes encoding amino acid permeases by inactivation of selected ORFs from the Synechocystis genomic sequence. Genome Res 11: 2034-2040.
67. Rabus R, Jack DL, Kelly DJ & Saier MH Jr (1999) TRAP transporters: an ancient family of extracytoplasmic solute-receptor-dependent secondary active transporters. Microbiology 145: 3431-3445.
68. Rucktooa P, Antoine R, Herrou J, Huvent I, Locht C, Jacob-Dubuisson F, Villeret V & Bompard C (2007) Crystal structures of two Bordetella pertussis periplasmic receptors contribute to defining a novel pyroglutamic acid binding DctP subfamily. J Mol Biol 370: 93-106.
69. Schauer R (2004) Sialic acids: fascinating sugars in higher animals and man. Zoology 107: 49-64.
70. Severi E, Randle G, Kivlin P, Whitfield K, Young R, Moxon R, Kelly D, Hood D & Thomas GH (2005) Sialic acid transport in Haemophilus influenzae is essential for lipopolysaccharide sialylation and serum resistance and is dependent on a novel tripartite ATP-independent periplasmic transporter. Mol Microbiol 58: 1173-1185.
71. Severi E, Hood DW & Thomas GH (2007) Sialic acid utilization by bacterial pathogens. Microbiology 153: 2817-2822.
72. Shaw JG, Hamblin MJ & Kelly DJ (1991) Purification, characterization and nucleotide sequence of the periplasmic C4-dicarboxylate-binding protein (DctP) from Rhodobacter capsulatus. Mol Microbiol 5: 3055-3062.
73. Steele TT, Fowler CW & Griffitts JS (2009) Control of gluconate utilization in Sinorhizobiummeliloti. J Bacteriol 191: 1355-1358.
74. Steenbergen SM, Lichtensteiger CA, Caughlan R, Garfinkle J, Fuller TE & Vimr ER (2005) Sialic acid metabolism and systemic pasteurellosis. Infect Immun 73: 1284-1294.
75. Stein MA, Schafer A & Giffhorn F (1997) Cloning, nucleotide sequence, and overexpression of smoS, a component of a novel operon encoding an ABC transporter and polyol dehydrogenases of Rhodobacter sphaeroides Si4. J Bacteriol 179: 6335-6340.
76. Takahashi H, Inagaki E, Kuroishi C & Tahirov TH (2004) Structure of the Thermus thermophilus putative periplasmic glutamate/glutamine-binding protein. Acta Crystallogr D 60: 1846-1854.
77. Tatum FM, Tabatabai LB & Briggs RE (2009) Sialic acid uptake is necessary for virulence of Pasteurella multocida in turkeys. Microb Pathogenesis 46: 337-344.
78. Thomas GH, Southworth T, Leon-Kempis MR, Leech A & Kelly DJ (2006) Novel ligands for the extracellular solute receptors of two bacterial TRAP transporters. Microbiology 152: 187-198.
79. + circulation in Vibrio parahaemolyticus. J Bacteriol 162: 794-798.
80. Ullmann R, Gross R, Simon J, Unden G & Kroger A (2000) Transport of C(4)-dicarboxylates in Wolinellasuccinogenes. J Bacteriol 182: 5757-5764.
81. Vimr E, Lichtensteiger C & Steenbergen S (2000) Sialic acid metabolism's dual function in Haemophilus influenzae. Mol Microbiol 36: 1113-1123.
82. Vimr ER, Kalivoda KA, Deszo EL & Steenbergen SM (2004) Diversity of microbial sialic acid metabolism. Microbiol Mol Biol R 68: 132-153.
83. 4-dicarboxylate binding protein (DctP) from Rhodobacter capsulatus. J Biol Chem 267: 8064-8072.
84. Weyand S, Shimamura T, Yajima S et al. (2008) Structure and molecular mechanism of a nucleobase-cation-symport-1 family transporter. Science 322: 709-713.
85. Wilkinson AJ & Verschueren KHG (2003) Crystal structures of periplasmic solute-binding proteins in ABC transport complexes illuminate their function. ABC Proteins: From Bacteria to Man (Holland IB, Cole SPC, Kuchler K & Higgins CF, eds). Elsevier, Amsterdam.
86. Winnen B, Hvorup RN & Saier MH Jr (2003) The tripartite tricarboxylate transporter (TTT) family. Res Microbiol 154: 457-465.
87. Wong PT & Wilson TH (1970) Counterflow of galactosides in Escherichia coli. Biochim Biophys Acta 196: 336-350.
88. Wyborn NR, Alderson J, Andrews SC & Kelly DJ (2001) Topological analysis of DctQ, the small integral membrane protein of the C4-dicarboxylate TRAP transporter of Rhodobacter capsulatus. FEMS Microbiol Lett 194: 13-17.
89. - dependent neurotransmitter transporters. Nature 437: 215-223.