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Comprehensive Analyses of Transport Proteins Encoded Within the Genome of “Aromatoleum aromaticum” Strain EbN1

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Abstract

The denitrifying bacterium “Aromatoleum aromaticum” strain EbN1 is specialized for the aerobic utilization of aromatic compounds including crude oil constituents. We here report whole-genome analyses for potential transport proteins in A. aromaticum strain EbN1. This organism encodes very few transporters for simple sugars and most other common carbon sources. However, up to 28% of its putative transporters may act on fairly hydrophobic aromatic and aliphatic compounds. We categorize the putative transporters encoded within the genome, assign them to recognized families, and propose their preferred substrates. The bioinformatic data are correlated with available metabolic information to obtain an integrated view of the metabolic network of A. aromaticum strain EbN1. The results thus indicate that this organism possesses a disproportionately large percentage of transporters for the uptake and efflux of hydrophobic and amphipathic aromatic and aliphatic compounds compared with previously analyzed organisms. We predict that these findings will have important implications for our ecophysiological understanding of bioremediation.

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References

  • Albrecht R, Zeth K, Soding J, Lupas A., Linke D (2006) Expression, crystallization and preliminary X-ray crystallographic studies of the outer membrane protein OmpW from Escherichia coli. Acta Crystallogr Sect F Struct Biol Cryst Commun 62:415–418

    Google Scholar 

  • Arispe N, De Maio A (2000) ATP and ADP modulate a cation channel formed by Hsc70 in acidic phospholipid membranes. J Biol Chem 275:30839–30843

    Article  PubMed  CAS  Google Scholar 

  • Barabote RD, Saier MH Jr (2005) Comparative genomic analyses of the bacterial phosphotransferase system. Microbiol Mol Biol Rev 69:608–634

    Article  PubMed  CAS  Google Scholar 

  • Barabote RD, Rendulic S, Schuster SC, Saier MH Jr (2007) Comprehensive analysis of transport proteins encoded within the genome of Bdellovibrio bacteriovorus. Genomics 90:424–446

    Article  PubMed  CAS  Google Scholar 

  • Beis K, Collins RF, Ford RC, Kamis AB, Whitfield C, Naismith JH (2004) Three-dimensional structure of Wza, the protein required for translocation of group 1 capsular polysaccharide across the outer membrane of Escherichia coli. J Biol Chem 279:28227–28232

    Article  PubMed  CAS  Google Scholar 

  • Berry RM, Armitage JP (1999) The bacterial flagella motor. Adv Microb Physiol 41:291–337

    Article  PubMed  CAS  Google Scholar 

  • Boll M, Fuchs G, Heider J (2002) Anaerobic oxidation of aromatic compounds and hydrocarbons. Curr Opin Chem Biol 6:604–611

    Article  PubMed  CAS  Google Scholar 

  • Bos MP, Tefsen B, Geurtsen J, Tommassen J (2004) Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. Proc Natl Acad Sci USA 101:9417–9422

    Article  PubMed  CAS  Google Scholar 

  • Bouveret E, Journet L, Walburger A, Cascales E, Benedetti H, Lloubes R (2002) Analysis of the Escherichia coli Tol-Pal and TonB systems by periplasmic production of Tol, TonB, colicin, or phage capsid soluble domains. Biochimie 84:413–421

    Article  PubMed  CAS  Google Scholar 

  • Calhoun MW, Thomas JW, Gennis RB (1994) The cytochrome oxidase superfamily of redox-driven proton pumps. Trends Biochem Sci 19:325–330

    Article  PubMed  CAS  Google Scholar 

  • Cao TB, Saier MH Jr (2001) Conjugal type IV macromolecular transfer systems of Gram-negative bacteria: organismal distribution, structural constraints and evolutionary conclusions. Microbiology 147:3201–3214

    PubMed  CAS  Google Scholar 

  • Cao TB, Saier MH Jr (2003) The general protein secretory pathway: phylogenetic analyses leading to evolutionary conclusions. Biochim Biophys Acta 1609:115–125

    Article  PubMed  CAS  Google Scholar 

  • Cao Z, Klebba PE (2002) Mechanisms of colicin binding and transport through outer membrane porins. Biochimie 84:399–412

    Article  PubMed  CAS  Google Scholar 

  • Chang G, Spencer RH, Lee AT, Barclay MT, Rees DC (1998) Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science 282:2220–2226

    Article  PubMed  CAS  Google Scholar 

  • Chang AB, Lin R, Keith Studley W, Tran CV, Saier MH Jr (2004) Phylogeny as a guide to structure and function of membrane transport proteins. Mol Membr Biol 21:171–181

    Article  PubMed  CAS  Google Scholar 

  • Chen M, Xie K, Jiang F, Yi L, Dalbey RE (2002) YidC, a newly defined evolutionarily conserved protein, mediates membrane protein assembly in bacteria. Biol Chem 383:1565–1572

    Article  PubMed  CAS  Google Scholar 

  • Chen M, Xie K, Nouwen N, Driessen AJ, Dalbey RE (2003) Conditional lethal mutations separate the M13 procoat and Pf3 coat functions of YidC: different YIDC structural requirements for membrane protein insertion. J Biol Chem 278:23295–23300

    Article  PubMed  CAS  Google Scholar 

  • Collins RF, Davidsen L, Derrick JP, Ford RC, Tonjum T (2001) Analysis of the PilQ secretin from Neisseria meningitidis by transmission electron microscopy reveals a dodecameric quaternary structure. J Bacteriol 183:3825–3832

    Article  PubMed  CAS  Google Scholar 

  • Collins RF, Ford RC, Kitmitto A, Olsen RO, Tonjum T, Derrick JP (2003) Three-dimensional structure of the Neisseria meningitidis secretin PilQ determined from negative-stain transmission electron microscopy. J Bacteriol 185:2611–2617

    Article  PubMed  CAS  Google Scholar 

  • Collins RF, Frye SA, Balasingham S, Ford RC, Tonjum T, Derrick JP (2005) Interaction with type IV pili induces structural changes in the bacterial outer membrane secretin PilQ. J Biol Chem 280:18923–18930

    Article  PubMed  CAS  Google Scholar 

  • Collins RF, Beis K, Dong C, Botting CH, McDonnell C, Ford RC, Clarke BR, Whitfield C, Naismith JH (2007) The 3D structure of a periplasm-spanning platform required for assembly of group 1 capsular polysaccharides in Escherichia coli. Proc Natl Acad Sci USA 104:2390–2395

    Article  PubMed  CAS  Google Scholar 

  • Dassa J, Fsihi H, Marck C, Dion M, Kieffer-Bontemps M, Boquet PL (1991) A new oxygen-regulated operon in Escherichia coli comprises the genes for a putative third cytochrome oxidase and for pH 2.5 acid phosphatase (appA). Mol Gen Genet 229:341–352

    Article  PubMed  CAS  Google Scholar 

  • DeRosier DJ (1998) The turn of the screw: the bacterial flagellar motor. Cell 93:17–20

    Article  PubMed  CAS  Google Scholar 

  • Dinh T, Paulsen IT, Saier MH Jr (1994) A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of gram-negative bacteria. J Bacteriol 176:3825–3831

    PubMed  CAS  Google Scholar 

  • Dong C, Beis K, Nesper J, Brunkan-Lamontagne AL, Clarke BR, Whitfield C, Naismith JH (2006) Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein. Nature 444:226–229

    Article  PubMed  CAS  Google Scholar 

  • Dubnau D (1999) DNA uptake in bacteria. Annu Rev Microbiol 53:217–244

    Article  PubMed  CAS  Google Scholar 

  • Fong RN, Kim KS, Yoshihara C, Inwood WB, Kustu S (2007) The W148L substitution in the Escherichia coli ammonium channel AmtB increases flux and indicates that the substrate is an ion. Proc Natl Acad Sci USA 104:18706–18711

    Article  PubMed  CAS  Google Scholar 

  • Gibson J, Harwood CS (2002) Metabolic diversity in aromatic compound utilization by anaerobic microbes. Annu Rev Microbiol 56:345–369

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Harayama S, Kok M, Neidle EL (1992) Functional and evolutionary relationships among diverse oxygenases. Annu Rev Microbiol 46:565–601

    Article  PubMed  CAS  Google Scholar 

  • Harvat EM, Zhang YM, Tran CV, Zhang Z, Frank MW, Rock CO, Saier MH Jr (2005) Lysophospholipid flipping across the Escherichia coli inner membrane catalyzed by a transporter (LplT) belonging to the major facilitator superfamily. J Biol Chem 280:12028–12034

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Heider J, Fuchs G (1997) Anaerobic metabolism of aromatic compounds. Eur J Biochem 243:577–596

    Article  PubMed  CAS  Google Scholar 

  • Höffken HW, Duong M, Friedrich T, Breuer M, Hauer B, Reinhardt R, Rabus R, Heider J (2006) Crystal structure and enzyme kinetics of the (S)-specific 1-phenylethanol dehydrogenase of the denitrifying bacterium strain EbN1. Biochemistry 45:82–93

    Article  PubMed  CAS  Google Scholar 

  • Holzapfel E, Eisner G, Alami M, Barrett CM, Buchanan G, Luke I, Betton JM, Robinson C, Palmer T, Moser M, Muller M (2007) The entire N-terminal half of TatC is involved in twin-arginine precursor binding. Biochemistry 46:2892–2898

    Article  PubMed  CAS  Google Scholar 

  • Hosking ER, Vogt C, Bakker EP, Manson MD (2006) The Escherichia coli MotAB proton channel unplugged. J Mol Biol 364:921–937

    Article  PubMed  CAS  Google Scholar 

  • Hu K-Y, Saier MH Jr (2006) Bioinformatic analyses of gram-negative bacterial OstA outer membrane assembly homologues. Curr Genomics 7:447–461

    Article  Google Scholar 

  • Hvorup RN, Winnen B, Chang AB, Jiang Y, Zhou XF, Saier MH Jr (2003) The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. Eur J Biochem 270:799–813

    Article  PubMed  CAS  Google Scholar 

  • Ishikita H, Knapp EW (2007) Protonation states of ammonia/ammonium in the hydrophobic pore of ammonia transporter protein AmtB. J Am Chem Soc 129:1210–1215

    Article  PubMed  CAS  Google Scholar 

  • Jack DL, Yang NM, Saier MH Jr (2001) The drug/metabolite transporter superfamily. Eur J Biochem 268:3620–3639

    Article  PubMed  CAS  Google Scholar 

  • Javelle A, Thomas G, Marini AM, Kramer R, Merrick M (2005) In vivo functional characterization of the Escherichia coli ammonium channel AmtB: evidence for metabolic coupling of AmtB to glutamine synthetase. Biochem J 390:215–222

    Article  PubMed  CAS  Google Scholar 

  • Kehres DG, Lawyer CH, Maguire ME (1998) The CorA magnesium transporter gene family. Microb Comp Genomics 3:151–169

    PubMed  CAS  Google Scholar 

  • Kelly DJ, Thomas GH (2001) The tripartite ATP-independent periplasmic (TRAP) transporters of bacteria and archaea. FEMS Microbiol Rev 25:405–424

    Article  PubMed  CAS  Google Scholar 

  • Khademi S, O’Connell J III, Remis J, Robles-Colmenares Y, Miercke LJ, Stroud RM (2004) Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 A. Science 305:1587–1594

    Article  PubMed  CAS  Google Scholar 

  • Kidane D, Graumann PL (2005) Intracellular protein and DNA dynamics in competent Bacillus subtilis cells. Cell 122:73–84

    Article  PubMed  CAS  Google Scholar 

  • Kimball RA, Saier MH Jr (2002) Voltage-gated H+ channels associated with human phagocyte superoxide-generating NADPH oxidases: sequence comparisons, structural predictions, and phylogenetic analyses. Mol Membr Biol 19:137–147

    Article  PubMed  CAS  Google Scholar 

  • Kloer DP, Hagel C, Heider J, Schulz GE (2006) Crystal structure of ethylbenzene dehydrogenase from Aromatoleum aromaticum. Structure 14:1377–1388

    Article  PubMed  CAS  Google Scholar 

  • Krause A, Ramakumar A, Bartels D, Battistoni F, Bekel T, Boch J, Bohm M, Friedrich F, Hurek T, Krause L, Linke B, McHardy AC, Sarkar A, Schneiker S, Syed AA, Thauer R, Vorholter FJ, Weidner S, Puhler A, Reinhold-Hurek B, Kaiser O, Goesmann A (2006) Complete genome of the mutualistic, N2-fixing grass endophyte Azoarcus sp. strain BH72. Nat Biotechnol 24:1385–1391

    Article  PubMed  CAS  Google Scholar 

  • Kühner S, Wöhlbrand L, Fritz I, Wruck W, Hultschig C, Hufnagel P, Kube M, Reinhardt R, Rabus R (2005) Substrate-dependent regulation of anaerobic degradation pathways for toluene and ethylbenzene in a denitrifying bacterium, strain EbN1. J Bacteriol 187:1493–1503

    Article  PubMed  CAS  Google Scholar 

  • Larimer FW, Chain P, Hauser L, Lamerdin J, Malfatti S, Do L, Land ML, Pelletier DA, Beatty JT, Lang AS, Tabita FR, Gibson JL, Hanson TE, Bobst C, Torres JL, Peres C, Harrison FH, Gibson J, Harwood CS (2004) Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat Biotechnol 22:55–61

    Article  PubMed  CAS  Google Scholar 

  • Llamas MA, Rodriguez-Herva JJ, Hancock RE, Bitter W, Tommassen J, Ramos JL (2003) Role of Pseudomonas putida tol-oprL gene products in uptake of solutes through the cytoplasmic membrane. J Bacteriol 185:4707–4716

    Article  PubMed  CAS  Google Scholar 

  • Lloubes R, Cascales E, Walburger A, Bouveret E, Lazdunski C, Bernadac A, Journet L (2001) The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity? Res Microbiol 152:523–529

    Article  PubMed  CAS  Google Scholar 

  • Lorca GL, Barabote RD, Zlotopolski V, Tran C, Winnen B, Hvorup RN, Stonestrom AJ, Nguyen E, Huang LW, Kim DS, Saier MH Jr (2007) Transport capabilities of eleven gram-positive bacteria: comparative genomic analyses. Biochim Biophys Acta 1768:1342–1366

    Article  PubMed  CAS  Google Scholar 

  • Luirink J, Samuelsson T, de Gier JW (2001) YidC/Oxa1p/Alb3: evolutionarily conserved mediators of membrane protein assembly. FEBS Lett 501:1–5

    Article  PubMed  CAS  Google Scholar 

  • Maguire ME (2006) Magnesium transporters: properties, regulation and structure. Front Biosci 11:3149–3163

    Article  PubMed  CAS  Google Scholar 

  • Mansour NM, Sawhney M, Tamang DG, Vogl C, Saier MH Jr (2007) The bile/arsenite/riboflavin transporter (BART) superfamily. FEBS J 274:612–629

    Article  PubMed  CAS  Google Scholar 

  • Martinac B, Buechner M, Delcour AH, Adler J, Kung C (1987) Pressure-sensitive ion channel in Escherichia coli. Proc Natl Acad Sci USA 84:2297–2301

    Article  PubMed  CAS  Google Scholar 

  • Martinac B, Adler J, Kung C (1990) Mechanosensitive ion channels of E. coli activated by amphipaths. Nature 348:261–263

    Article  PubMed  CAS  Google Scholar 

  • Mohamed Mel S, Ismail W, Heider J, Fuchs G (2002) Aerobic metabolism of phenylacetic acids in Azoarcus evansii. Arch Microbiol 178:180–192

    Article  CAS  Google Scholar 

  • 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 Microbiol Biotechnol 12:218–226

    Article  PubMed  CAS  Google Scholar 

  • Nakamoto H, Bardwell JC (2004) Catalysis of disulfide bond formation and isomerization in the Escherichia coli periplasm. Biochim Biophys Acta 1694:111–119

    Article  PubMed  CAS  Google Scholar 

  • Nelson KE, Weinel C, Paulsen IT, Dodson RJ, Hilbert H, Martins dos Santos VA, Fouts DE, Gill SR, Pop M, Holmes M, Brinkac L, Beanan M, DeBoy RT, Daugherty S, Kolonay J, Madupu R, Nelson W, White O, Peterson J, Khouri H, Hance I, Chris Lee P, Holtzapple E, Scanlan D, Tran K, Moazzez A, Utterback T, Rizzo M, Lee K, Kosack D, Moestl D, Wedler H, Lauber J, Stjepandic D, Hoheisel J, Straetz M, Heim S, Kiewitz C, Eisen JA, Timmis KN, Dusterhoft A, Tummler B, Fraser CM (2002) Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 4:799–808

    Article  PubMed  CAS  Google Scholar 

  • Nesper J, Hill CM, Paiment A, Harauz G, Beis K, Naismith JH, Whitfield C (2003) Translocation of group 1 capsular polysaccharide in Escherichia coli serotype K30. Structural and functional analysis of the outer membrane lipoprotein Wza. J Biol Chem 278:29772–49763

    Article  CAS  Google Scholar 

  • Nies DH, Koch S, Wachi S, Peitzsch N, Saier MH Jr (1998) CHR, a novel family of prokaryotic proton motive force-driven transporters probably containing chromate/sulfate antiporters. J Bacteriol 180:5799–5802

    PubMed  CAS  Google Scholar 

  • Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656

    Article  PubMed  CAS  Google Scholar 

  • Nishijyo T, Haas D, Itoh Y (2001) The CbrA-CbrB two-component regulatory system controls the utilization of multiple carbon and nitrogen sources in Pseudomonas aeruginosa. Mol Microbiol 40:917–931

    Article  PubMed  CAS  Google Scholar 

  • Nouwen N, Driessen AJ (2002) SecDFyajC forms a heterotetrameric complex with YidC. Mol Microbiol 44:1397–1405

    Article  PubMed  CAS  Google Scholar 

  • Paulsen IT, Park JH, Choi PS, Saier MH Jr (1997) A family of gram-negative bacterial outer membrane factors that function in the export of proteins, carbohydrates, drugs and heavy metals from gram-negative bacteria. FEMS Microbiol Lett 156:1–8

    PubMed  CAS  Google Scholar 

  • Paulsen IT, Nguyen L, Sliwinski MK, Rabus R, Saier MH Jr (2000) Microbial genome analyses: comparative transport capabilities in eighteen prokaryotes. J Mol Biol 301:75–100

    Article  PubMed  CAS  Google Scholar 

  • Peabody CR, Chung YJ, Yen MR, Vidal-Ingigliardi D, Pugsley AP, Saier MH Jr (2003) Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149:3051–3072

    Article  PubMed  CAS  Google Scholar 

  • Perozo E, Kloda A, Cortes DM, Martinac B (2001) Site-directed spin-labeling analysis of reconstituted Mscl in the closed state. J Gen Physiol 118:193–206

    Article  PubMed  CAS  Google Scholar 

  • Pivetti CD, Yen MR, Miller S, Busch W, Tseng YH, Booth IR, Saier MH Jr (2003) Two families of mechanosensitive channel proteins. Microbiol Mol Biol Rev 67:66–85

    Article  PubMed  CAS  Google Scholar 

  • Rabus R, Widdel F (1995) Anaerobic degradation of ethylbenzene and other aromatic hydrocarbons by new denitrifying bacteria. Arch Microbiol 163:96–103

    Article  PubMed  CAS  Google Scholar 

  • Rabus R, Widdel F (1996) Utilization of alkylbenzenes during anaerobic growth of pure cultures of denitrifying bacteria on crude oil. Appl Environ Microbiol 62:1238–1241

    PubMed  CAS  Google Scholar 

  • Rabus R, Reizer J, Paulsen I, Saier MH Jr (1999) Enzyme I(Ntr) from Escherichia coli. A novel enzyme of the phosphoenolpyruvate-dependent phosphotransferase system exhibiting strict specificity for its phosphoryl acceptor, NPr. J Biol Chem 274:26185–26191

    Article  PubMed  CAS  Google Scholar 

  • Rabus R, Kube M, Heider J, Beck A, Heitmann K, Widdel F, Reinhardt R (2005) The genome sequence of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Arch Microbiol 183:27–36

    Article  PubMed  CAS  Google Scholar 

  • Ramsey IS, Moran MM, Chong JA, Clapham DE (2006) A voltage-gated proton-selective channel lacking the pore domain. Nature 440:1213–1216

    Article  PubMed  CAS  Google Scholar 

  • Reinhold-Hurek B, Hurek T (2000) Reassessment of the taxonomic structure of the diazotrophic genus Azoarcus sensu lato and description of three new genera and new species, Azovibrio restrictus gen. nov., sp. nov., Azospira oryzae gen nov., sp. nov. and Azonexus fungiphilus gen nov., sp. nov. Int J Syst Evol Microbiol 50(Pt 2):649–659

    PubMed  CAS  Google Scholar 

  • Ren Q, Paulsen IT (2007) Large-scale comparative genomic analyses of cytoplasmic membrane transport systems in prokaryotes. J Mol Microbiol Biotechnol 12:165–179

    Article  PubMed  CAS  Google Scholar 

  • Reuter G, Janvilisri T, Venter H, Shahi S, Balakrishnan L, van Veen HW (2003) The ATP binding cassette multidrug transporter LmrA and lipid transporter MsbA have overlapping substrate specificities. J Biol Chem 278:35193–35198

    Article  PubMed  CAS  Google Scholar 

  • Rothery RA, Workun GJ, Weiner JH (2008) The prokaryotic complex iron–sulfur molybdoenzyme family. Biochim Biophys Acta 1778:1897–1929

    Article  PubMed  CAS  Google Scholar 

  • Saier MH Jr (2003) Tracing pathways of transport protein evolution. Mol Microbiol 48:1145–1156

    Article  PubMed  CAS  Google Scholar 

  • Saier MH Jr (2006) Protein secretion and membrane insertion systems in gram-negative bacteria. J Membr Biol 214:75–90

    Article  PubMed  CAS  Google Scholar 

  • Sandkvist M (2001) Biology of type II secretion. Mol Microbiol 40:271–283

    Article  PubMed  CAS  Google Scholar 

  • Santiviago CA, Fuentes JA, Bueno SM, Trombert AN, Hildago AA, Socias LT, Youderian P, Mora GC (2002) The Salmonella enterica sv. Typhimurium smvA, yddG and ompD (porin) genes are required for the efficient efflux of methyl viologen. Mol Microbiol 46:687–698

    Article  PubMed  CAS  Google Scholar 

  • Sasaki M, Takagi M, Okamura Y (2006) A voltage sensor-domain protein is a voltage-gated proton channel. Science 312:589–592

    Article  PubMed  CAS  Google Scholar 

  • Schleissner C, Olivera ER, Fernandez-Valverde M, Luengo JM (1994) Aerobic catabolism of phenylacetic acid in Pseudomonas putida U: biochemical characterization of a specific phenylacetic acid transport system and formal demonstration that phenylacetyl-coenzyme A is a catabolic intermediate. J Bacteriol 176:7667–7676

    PubMed  CAS  Google Scholar 

  • Schneiker S, Martins dos Santos VA, Bartels D, Bekel T, Brecht M, Buhrmester J, Chernikova TN, Denaro R, Ferrer M, Gertler C, Goesmann A, Golyshina OV, Kaminski F, Khachane AN, Lang S, Linke B, McHardy AC, Meyer F, Nechitaylo T, Puhler A, Regenhardt D, Rupp O, Sabirova JS, Selbitschka W, Yakimov MM, Timmis KN, Vorholter FJ, Weidner S, Kaiser O, Golyshin PN (2006) Genome sequence of the ubiquitous hydrocarbon-degrading marine bacterium Alcanivorax borkumensis. Nat Biotechnol 24:997–1004

    Article  PubMed  CAS  Google Scholar 

  • Spormann AM, Widdel F (2000) Metabolism of alkylbenzenes, alkanes, and other hydrocarbons in anaerobic bacteria. Biodegradation 11:85–105

    Article  PubMed  CAS  Google Scholar 

  • Sukharev SI, Schroeder MJ, McCaslin DR (1999) Stoichiometry of the large conductance bacterial mechanosensitive channel of E. coli. A biochemical study. J Membr Biol 171:183–193

    Article  PubMed  CAS  Google Scholar 

  • Sukharev S, Betanzos M, Chiang CS, Guy HR (2001) The gating mechanism of the large mechanosensitive channel MscL. Nature 409:720–724

    Article  PubMed  CAS  Google Scholar 

  • Suzuki H, Koyanagi T, Izuka S, Onishi A, Kumagai H (2005) The yliA, -B, -C, and -D genes of Escherichia coli K-12 encode a novel glutathione importer with an ATP-binding cassette. J Bacteriol 187:5861–5867

    Article  PubMed  CAS  Google Scholar 

  • Trautwein K, Kühner S, Wöhlbrand L, Halder T, Kuchta K, Steinbüchel A, Rabus R (2008) Solvent stress response of the denitrifying bacterium “Aromatoleum aromaticum” strain EbN1. Appl Environ Microbiol 74:2267–2274

    Article  PubMed  CAS  Google Scholar 

  • van Beilen JB, Eggink G, Enequist H, Bos R, Witholt B (1992) DNA sequence determination and functional characterization of the OCT-plasmid-encoded alkJKL genes of Pseudomonas oleovorans. Mol Microbiol 6:3121–3136

    Article  PubMed  Google Scholar 

  • van den Berg B, Black PN, Clemons WM Jr, Rapoport TA (2004) Crystal structure of the long-chain fatty acid transporter FadL. Science 304:1506–1509

    Article  PubMed  CAS  Google Scholar 

  • Wackett LP, Hershberger CD (2001) Biocatalysis and biodegradation: microbial transformation of organic compounds. American Society Microbiolgy, Washington, DC

    Google Scholar 

  • Widdel F, Rabus R (2001) Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr Opin Biotechnol 12:259–276

    Article  PubMed  CAS  Google Scholar 

  • Williams MD, Ouyang TX, Flickinger MC (1994) Glutathione S-transferase-sspA fusion binds to E. coli RNA polymerase and complements delta sspA mutation allowing phage P1 replication. Biochem Biophys Res Commun 201:123–127

    Article  PubMed  CAS  Google Scholar 

  • Winter J, Jakob U (2004) Beyond transcription—new mechanisms for the regulation of molecular chaperones. Crit Rev Biochem Mol Biol 39:297–317

    Article  PubMed  CAS  Google Scholar 

  • Wöhlbrand L, Rabus R (2008) Development of a genetic system for the denitrifying bacterium ‘Aromatoleum aromaticum’ strain EbN1. J Mol Microbiol Biotechnol (in press)

  • Wöhlbrand L, Kallerhoff B, Lange D, Hufnagel P, Thiermann J, Reinhardt R, Rabus R (2007) Functional proteomic view of metabolic regulation in “Aromatoleum aromaticum” strain EbN1. Proteomics 7:2222–2239

    Article  PubMed  CAS  Google Scholar 

  • Wöhlbrand L, Wilkes H, Halder T, Rabus R (2008) Anaerobic degradation of p-ethylphenol by “Aromatoleum aromaticum” strain EbN1: pathway, regulation, and involved proteins. J Bacteriol 190:5699–5709

    Article  PubMed  CAS  Google Scholar 

  • Wu T, Malinverni J, Ruiz N, Kim S, Silhavy TJ, Kahne D (2005) Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121:235–245

    Article  PubMed  CAS  Google Scholar 

  • Wu T, McCandlish AC, Gronenberg LS, Chng SS, Silhavy TJ, Kahne D (2006) Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 103:11754–11759

    Article  PubMed  CAS  Google Scholar 

  • Wylie JL, Worobec EA (1995) The OprB porin plays a central role in carbohydrate uptake in Pseudomonas aeruginosa. J Bacteriol 177:3021–3026

    PubMed  CAS  Google Scholar 

  • Yen MR, Harley KT, Tseng YH, Saier MH Jr (2001) Phylogenetic and structural analyses of the oxa1 family of protein translocases. FEMS Microbiol Lett 204:223–231

    Article  PubMed  CAS  Google Scholar 

  • Yen MR, Peabody CR, Partovi SM, Zhai Y, Tseng YH, Saier MH Jr (2002a) Protein-translocating outer membrane porins of Gram-negative bacteria. Biochim Biophys Acta 1562:6–31

    Article  PubMed  CAS  Google Scholar 

  • Yen MR, Tseng YH, Nguyen EH, Wu LF, Saier MH Jr (2002b) Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system. Arch Microbiol 177:441–450

    Article  PubMed  CAS  Google Scholar 

  • Zaar A, Eisenreich W, Bacher A, Fuchs G (2001) A novel pathway of aerobic benzoate catabolism in the bacteria Azoarcus evansii and Bacillus stearothermophilus. J Biol Chem 276:24997–25004

    Article  PubMed  CAS  Google Scholar 

  • Zhai YF, Heijne W, Saier MH Jr (2003) Molecular modeling of the bacterial outer membrane receptor energizer, ExbBD/TonB, based on homology with the flagellar motor, MotAB. Biochim Biophys Acta 1614:201–210

    Article  PubMed  CAS  Google Scholar 

  • Zou Z, DiRusso CC, Ctrnacta V, Black PN (2002) Fatty acid transport in Saccharomyces cerevisiae. Directed mutagenesis of FAT1 distinguishes the biochemical activities associated with Fat1p. J Biol Chem 277:30171–31062

    Google Scholar 

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Acknowledgments

This work was supported by NIH Grant GM077402 from the National Institute of General Medical Sciences. We thank Mary Beth Hiller, Van T. Duong, and Jeeni Criscenzo for assistance in the preparation of the manuscript.

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Correspondence to Milton H. Saier Jr..

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Tamang, D.G., Rabus, R., Barabote, R.D. et al. Comprehensive Analyses of Transport Proteins Encoded Within the Genome of “Aromatoleum aromaticum” Strain EbN1. J Membrane Biol 229, 53–90 (2009). https://doi.org/10.1007/s00232-009-9168-2

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  • DOI: https://doi.org/10.1007/s00232-009-9168-2

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