The CouPSTU and TarPQM Transporters in Rhodopseudomonas palustris: Redundant, Promiscuous Uptake Systems for Lignin-Derived Aromatic Substrates

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Salmon, Robert C ^a   Cliff, Matthew J ^b   Rafferty, John B ^a   Kelly, David J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LIGNIN; PROTEIN COUPSTU; PROTEIN TARPQM; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GROWTH; BINDING AFFINITY; BIODEGRADATION; BIOTRANSFORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; HYDROGEN BOND; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; OXIDATION; PHOTOSYNTHESIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN METABOLISM; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TRANSPORT; RHODOPSEUDOMONAS PALUSTRIS; SEQUENCE ALIGNMENT; THERMODYNAMICS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CALORIMETRY; CRYSTALLOGRAPHY, X-RAY; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN BONDING; LIGANDS; LIGNIN; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN FOLDING; RHODOPSEUDOMONAS; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, FLUORESCENCE;

PHOTOBACTERIA; RHODOPSEUDOMONAS PALUSTRIS;

EID: 84875544888     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059844     Document Type: Article

References (35)

1. Hara H, Masai E, Miyauchi K, Katayama Y, Fukuda M, (2003) Characterization of the 4-carboxy-4-hydroxy-2-oxoadipate aldolase gene and operon structure of the protocatechuate 4,5-cleavage pathway genes in Sphingomonas paucimobilis SYK-6. J Bacteriol 185: 41-50.
2. Gold MH, Alic M, (1993) Molecular biology of the lignin-degrading basidiomycete Phanerochaete chrysosporium. Microbiol Revs 57: 605-622.
3. Masai E, Katayama Y, Kubota S, Kawai S, Yamasaki M, et al. (1993) A bacterial enzyme degrading the model lignin compound β-etherase is a member of the glutathione-S-transferase superfamily. FEBS Letters 323: 135-140.
4. Whetten R, Sederoff R, (1995) Lignin biosynthesis. Plant Cell 7: 1001-1013.
5. Larimer FW, Chain P, Hauser L, Lamerdin J, Malfatti S, et al. (2004) Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat Biotechnol 22: 55-61.
6. Harwood CS, Gibson J, (1988) Anaerobic and aerobic metabolism of diverse aromatic compounds by the photosynthetic bacterium Rhodopseudomonas palustris. Appl Environ Microbiol 54: 712-717.
7. Geissler JF, Harwood CS, Gibson J, (1988) Purification and properties of benzoate-coenzyme A ligase, a Rhodopseudomonas palustris enzyme involved in the anaerobic degradation of benzoate. J Bacteriol 170: 1709-1714.
8. Egland PG, Gibson J, Harwood CS, (1995) Benzoate-coenzyme A ligase, encoded by badA, is one of three ligases able to catalyze benzoyl-coenzyme A formation during anaerobic growth of Rhodopseudomonas palustris on benzoate. J Bacteriol 177: 6545-6551.
9. Egland PG, Pelletier DA, Dispensa M, Gibson J, Harwood CS, (1997) A cluster of bacterial genes for anaerobic benzene ring biodegradation. Proc Natl Acad Sci USA 94: 6484-6489.
10. Hirakawa H, Schaefer AL, Greenberg EP, Harwood CS, (2012) Anaerobic p-coumarate degradation by Rhodopseudomonas palustris and identification of CouR, a MarR repressor protein that binds p-coumaroyl Coenzyme A. J Bacteriol. 194: 1960-1967.
11. Toms A, Wood JM, (1970) Degradation of trans-ferulic acid by Pseudomonas acidovorans Biochemistry. 9: 337-343.
12. Plaggenborg R, Steinbuchel A, Priefert H, (2001) The coenzyme A-dependent, non-β-oxidation pathway and not direct deacetylation is the major route for ferulic acid degradation in Delftia acidovorans. FEMS Microbiol Lett 205: 9-16.
13. Pan C, Oda Y, Lankford PK, Zhang B, Samatova NF, et al. (2008) Characterization of anaerobic catabolism of p-coumarate in Rhodopseudomonas palustris by integrating transcriptomics and quantitative proteomics. Mol Cell Proteomics 7: 938-948.
14. Elder DJ, Morgan P, Kelly DJ, (1992) Anaerobic degradation of trans-cinnamate and omega-phenylalkane carboxylic acids by the photosynthetic bacterium Rhodopseudomonas palustris: evidence for a beta-oxidation mechanism. Arch Microbiol 157: 148-154.
15. 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 Rhodobacter capsulatus and by homologs in diverse Gram-negative bacteria. J Bacteriol 179: 5482-93.
16. Phattarasukol S, Radey MC, Lappala CR, Oda Y, Hirakawa H, et al. (2012) Identification of a p-coumarate degradation regulon in Rhodopseudomonas palustris using Xpression, an integrated tool for prokaryotic RNA-seq data processing. Appl Environ Microbiol 8: 6812-6818.
17. Guiliani SE, Frank AM, Corgliano DM, Seifert C, Hauser L, et al. (2011) Environment sensing and response mediated by ABC transporters. BMC Genomics 12Suppl 1: S8.
18. Pietri R, Zerbs S, Corgliano DM, Allaire M, Collart FR, et al. (2012) Biophysical and structural characterization of a sequence-diverse set of solute-binding proteins for aromatic compounds. J Biol Chem 287: 23748-23756.
19. Smart JP, Cliff MJ, Kelly DJ, (2009) A role for tungsten in the biology of Campylobacter jejuni: tungstate stimulates formate dehydrogenase activity and is transported via an ultra-high affinity ABC system distinct from the molybdate transporter. Mol Microbiol 74: 742-57.
20. Kabsch W, (2010) Integration, scaling, space-group assignment and post-refinement. Acta Cryst. D66: 133-144.
21. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Cryst 40: 658-674.
22. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, et al. (2011) Overview of the CCP 4 suite and current developments. Acta Cryst D67: 235-242.
23. Kelley LA, Sternberg MJE, (2009) Protein structure prediction on the web: a case study using the Phyre server. Nat Protocols 4: 363-371.
24. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Cryst D60: 2126-2132.
25. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Cryst D53: 240-255.
26. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, et al. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Cryst D66: 12-21.
27. Laskowski RA, Swindells MB, (2011) LigPlot+: Multiple ligand-protein interaction diagrams for drug discovery. J Chem Inf Model 51: 2778-2786.
28. 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.
29. Gunsior M, Ravel J, Challis GL, Townsend CA, (2004) Engineering p-hydroxyphenylpyruvate dioxygenase to a p-hydroxymandelate synthase and evidence for the proposed benzene oxide intermediate in homogentisate formation. Biochemistry 43: 663-674.
30. Kelly DJ, Thomas GH, (2001) The tripartite ATP-independent periplasmic (TRAP) transporters of bacteria and archaea. FEMS Microbiol Revs 25: 405-424.
31. Mulligan C, Geertsma ER, Severi E, Kelly DJ, Poolman B, et al. (2009) The substrate-binding protein imposes directionality on an electrochemical sodium gradient-driven TRAP transporter. Proc Natl Acad Sci USA 106: 1778-1783.
32. Fischer M, Zhang QY, Hubbard RE, Thomas GH, (2010) Caught in a TRAP: substrate-binding proteins in secondary transport. Trends Microbiol 18: 471-478.
33. Müller A, Severi E, Mulligan C, Watts AG, Kelly DJ, et al. (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.
34. Lecher J, Pittelkow M, Zobel S, Bursy J, Bönig T, et al. (2009) The crystal structure of UehA in complex with ectoine-A comparison with other TRAP-T binding proteins. J Mol Biol 389: 58-73.
35. Johnston JW, Coussens NP, Allen S, Houtman JC, Turner KH, et al. (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.