Substrate Transport

  • Rebecca E. Parales
  • Jayna L. Ditty
Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)


Hydrocarbon compounds are known to passively diffuse across bacterial cytoplasmic membranes, and this may be the primary mechanism of hydrocarbon entry into most bacteria. The participation of active transport systems has been suggested in some bacterial strains, but solid evidence for active transport of hydrocarbons is currently lacking. In contrast, many active transport systems have been identified for the energy-dependent uptake of aromatic acids in both Gram-negative and Gram-positive bacteria. In addition, Gram-negative bacteria often harbor specific inducible outer membrane channels that allow entry of various aromatic hydrocarbon substrates.



Research in the Parales and Ditty laboratories has been supported by the National Science Foundation (awards MCB 0627248 (REP), MCB 0919930 (REP and JLD), MCB 1022362 (REP)).


  1. Adebusuyi AA, Smith AY, Gray MR, Foght JM (2012) The EmhABC efflux pump decreases the efficiency of phenanthrene biodegradation by Pseudomonas fluorescens strain LP6a. Appl Microbiol Biotechnol 95:757–766CrossRefPubMedGoogle Scholar
  2. Allende JL, Suarez M, Gallego M, Garrido-Pertierra A (1993) 4-Hydroxybenzoate uptake in Klebsiella pneumoniae is driven by electric potential. Arch Biochem Biophys 300:142–147CrossRefPubMedGoogle Scholar
  3. Barnes MR, Duetz W, Williams PA (1997) A 3-(3-hydroxyphenyl)propionic acid catabolic pathway in Rhodococcus globerulus PWD1: cloning and characterization of the hpp operon. J Bacteriol 179:6145–6153CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bateman JN, Speer B, Feduik L, Hartline RA (1986) Naphthalene association and uptake in Pseudomonas putida. J Bacteriol 166:155–161CrossRefPubMedPubMedCentralGoogle Scholar
  5. Beal R, Betts WB (2000) Role of rhamnolipid biosurfactants in the uptake and mineralization of hexadecane in Pseudomonas aeruginosa. J Appl Microbiol 89:158–168CrossRefPubMedGoogle Scholar
  6. Black PN (1991) Primary sequence of Escherichia coli fadL gene encoding an outer membrane protein required for long-chain fatty acid transport. J Bacteriol 173:435–442CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bugg T, Foght JM, Pickard MA, Gray MR (2000) Uptake and active efflux of polycyclic aromatic hydrocarbons by Pseudomonas fluorescens LP6a. Appl Environ Microbiol 66:5387–5392CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chang H-K, Zylstra GJ (1999) Characterization of the phthalate permease OphD from Burkholderia cepacia ATCC 17616. J Bacteriol 181:6197–6199PubMedPubMedCentralGoogle Scholar
  9. Chaudhry MT, Huang Y, Shen X-H, Poetsch A, Jiang C-Y, Liu S-J (2007) Genome-wide investigation of aromatic acid transporters in Corynebacterium glutamicum. Microbiology 153:857–865CrossRefPubMedGoogle Scholar
  10. Chrzanowski L, Wick LY, Meulenkamp R, Kaestner M, Heipieper HJ (2009) Rhamnolipid biosurfactants decrease the toxicity of chlorinated phenols to Pseudomonas putida DOT-T1E. Lett Appl Microbiol 48:756–762PubMedGoogle Scholar
  11. Collier LS, Nichols NN, Neidle EL (1997) benK encodes a hydrophobic permease-like protein involved in benzoate degradation by Acinetobacter sp. strain ADP1. J Bacteriol 179:5943–5946CrossRefPubMedPubMedCentralGoogle Scholar
  12. D’Argenio DA, Segura A, Coco WM, Bunz PV, Ornston LN (1999) The physiological contribution of Acinetobacter PcaK, a transport system that acts upon protocatechuate, can be masked by overlapping specificity of VanK. J Bacteriol 181:3505–3515PubMedPubMedCentralGoogle Scholar
  13. Díaz E, Ferrández A, García JL (1998) Characterization of the hca cluster encoding the dioxygenolytic pathway for initial catabolism of 3-phenylpropionic acid in Escherichia coli K-12. J Bacteriol 180:2915–2923PubMedPubMedCentralGoogle Scholar
  14. DiRusso CC, Black PN (2004) Bacterial long chain fatty acid transport: gateway to a fatty acid-responsive signaling system. J Biol Chem 279:49563–49566CrossRefPubMedGoogle Scholar
  15. Ditty JL, Harwood CS (1999) Conserved cytoplasmic loops are important for both the transport and chemotaxis functions of PcaK, a protein from Pseudomonas putida with 12-membrane-spanning regions. J Bacteriol 181:5068–5074PubMedPubMedCentralGoogle Scholar
  16. Ditty JL, Harwood CS (2002) Charged amino acids conserved in the aromatic acid/H+ symporter family of permeases are required for 4-hydroxybenzoate transport by PcaK from Pseudomonas putida. J Bacteriol 184:1444–1448CrossRefPubMedPubMedCentralGoogle Scholar
  17. Eaton RW (1997) p-Cymene catabolic pathway in Pseudomonas putida F1: cloning and characterization of DNA encoding conversion of p-cymene to p-cumate. J Bacteriol 179:3171–3180CrossRefPubMedPubMedCentralGoogle Scholar
  18. Eaton RW, Timmis KN (1986) Characterization of a plasmid-specified pathway for catabolism of isopropylbenzene in Pseudomonas putida RE204. J Bacteriol 168:123–131CrossRefPubMedPubMedCentralGoogle Scholar
  19. Groenewegen PEJ, Driessen AJM, Konigs WN, de Bont JAM (1990) Energy-dependent uptake of 4-chlorobenzoate in the corneyform bacterium NTB-1. J Bacteriol 172:419–423CrossRefPubMedPubMedCentralGoogle Scholar
  20. Habe H, Kasuga K, Nojiri H, Yamane H, Omori T (1996) Analysis of cumene (isopropylbenzene) degradation genes from Pseudomonas fluorescens IP01. Appl Environ Microbiol 62:4471–4477PubMedPubMedCentralGoogle Scholar
  21. Hara H, Stewart GR, Mohn WW (2010) Involvement of a novel ABC transporter and monoalkyl phthalate ester hydrolase in phthalate ester catabolism by Rhodococcus jostii RHA1. Appl Environ Microbiol 76:1516–1523CrossRefPubMedGoogle Scholar
  22. Harwood CS, Parales RE (1996) The β-ketoadipate pathway and the biology of self-identity. Annu Rev Microbiol 50:533–590CrossRefGoogle Scholar
  23. Harwood CS, Nichols NN, Kim M-K, Ditty JL, Parales RE (1994) Identification of the pcaRKF gene cluster from Pseudomonas putida: involvement in chemotaxis, biodegradation, and transport of 4-hydroxybenzoate. J Bacteriol 176:6479–6488CrossRefPubMedPubMedCentralGoogle Scholar
  24. Hearn EM, Dennis JJ, Gray MR, Foght JM (2003) Identification and characterization of the emhABC efflux system for polycyclic aromatic hydrocarbons in Pseudomonas fluorescens cLP6a. J Bacteriol 185:6233–6240CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hearn EM, Patel DR, van den Berg B (2008) Outer-membrane transport of aromatic hydrocarbons as a first step in biodegradation. Proc Natl Acad Sci U S A 105:8601–8606CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hearn EM, Patel DR, Lepore BW, Indic M, van den Berg B (2009) Transmembrane passage of hydrophobic compounds through a protein channel wall. Nature 458:367–370CrossRefPubMedPubMedCentralGoogle Scholar
  27. Higgins SJ, Mandelstam J (1972) Evidence for induced synthesis of an active transport factor for mandelate in Pseudomonas putida. Biochem J 126:917–922CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hong H, Patel DR, Tamm LK, van den Berg B (2006) The outer membrane protein OmpW forms an eight-stranded β-barrel with a hydrophobic channel. J Biol Chem 28:7568–7577CrossRefGoogle Scholar
  29. Hosaka M, Kamimura N, Toribami S, Mori K, Kasai D, Fukuda M, Masai E (2013) Novel tripartite aromatic acid transporter essential for terephthalate uptake in Comamonas sp. strain E6. Appl Environ Microbiol 79:6148–6155CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kahng H-Y, Byrne AM, Olsen RH, Kukor JJ (2000) Characterization and role of tbuX in utilization of toluene by Ralstonia pickettii PKO1. J Bacteriol 182:1232–1242CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kallimanis A, Frillingos S, Drainas C, Koukkou AI (2007) Taxonomic identification, phenanthrene uptake activity, and membrane lipid alterations of the PAH degrading Arthrobacter sp. strain Sphe3. Appl Microbiol Biotechnol 76:709–717CrossRefPubMedGoogle Scholar
  32. Kasai Y, Inoue J, Harayama S (2001) The TOL plasmid pWWO xylN gene product from Pseudomonas putida is involved in m-xylene uptake. J Bacteriol 183:6662–6666CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kieboom J, Dennis JJ, de Bont JA, Zylstra GJ (1998) Identification and molecular characterization of an efflux pump involved in Pseudomonas putida S12 solvent tolerance. J Biol Chem 273:85–91CrossRefPubMedGoogle Scholar
  34. Kim IS, Foght JM, Gray MR (2002) Selective transport and accumulation of alkanes by Rhodococcus erythropolis S+14He. Biotechnol Bioeng 80:650–659CrossRefPubMedGoogle Scholar
  35. Kiran GS, Ninawe AS, Lipton AN, Pandian V, Selvin J (2016) Rhamnolipid biosurfactants: evolutionary implications, applications and future prospects from untapped marine resource. Crit Rev Biotechnol 36:399–415PubMedGoogle Scholar
  36. Kitagawa W, Miyauchi K, Masai E, Fukuda M (2001) Cloning and characterization of benzoate catabolic genes in the Gram-positive polychlorinated biphenyl degrader Rhodococcus sp. strain RHA1. J Bacteriol 183:6598–6606CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kitagawa W, Takami S, Miyauchi K, Masai E, Kamagata Y, Tiedje JM, Fukuda M (2002) Novel 2,4-dichlorophenoxyacetic acid degradation genes from oligotrophic Bradyrhizobium sp. strain HW13 isolated from a pristine environment. J Bacteriol 184:509–518CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lau PCK, Bergeron H, Labbe D, Wang Y, Brousseau R, Gibson DT (1994) Sequence and expression of the todGIH genes involved in the last three steps of toluene degradation by Pseudomonas putida F1. Gene 146:7–13CrossRefPubMedGoogle Scholar
  39. Leveau JH, Zehnder AJ, van der Meer JR (1998) The tfdK gene product facilitates uptake of 2,4-dichlorophenoxyacetate by Ralstonia eutropha JMP134(pJP4). J Bacteriol 180:2237–2243PubMedPubMedCentralGoogle Scholar
  40. Li Y, Wang H, Hua F, Su M, Zhao Y (2014) Trans-membrane transport of fluoranthene by Rhodococcus sp. BAP-1 and optimization of uptake process. Bioresour Technol 155:213–219CrossRefPubMedGoogle Scholar
  41. Luu RA, Kootstra JD, Nesteryuk V, Brunton C, Parales JV, Ditty JL, Parales RE (2015) Integration of chemotaxis, transport and catabolism in Pseudomonas putida and identification of the aromatic acid chemoreceptor PcaY. Mol Microbiol 96:134–147CrossRefPubMedGoogle Scholar
  42. Master ER, McKinlay JJ, Stewart GR, Mohn WW (2005) Biphenyl uptake by psychrotolerant Pseudomonas sp. strain Cam-1 and mesophilic Burkholderia sp. strain LB400. Can J Microbiol 51:399–404CrossRefPubMedGoogle Scholar
  43. Menn F-M, Zylstra GJ, Gibson DT (1991) Location and sequence of the todF gene encoding 2-hydroxy-6-oxohepta-2,4-dienoate hydrolase in Pseudomonas putida F1. Gene 104:91–94CrossRefPubMedGoogle Scholar
  44. Miyata N, Iwahori K, Foght JM, Gray MR (2004) Saturable, energy-dependent uptake of phenanthrene in aqueous phase by Mycobacterium sp. strain RJGII-135. Appl Environ Microbiol 70:363–369CrossRefPubMedPubMedCentralGoogle Scholar
  45. Mooney A, O’Leary ND, Dobson AD (2006) Cloning and functional characterization of the styE gene, involved in styrene transport in Pseudomonas putida CA-3. Appl Environ Microbiol 72:1302–1309CrossRefPubMedPubMedCentralGoogle Scholar
  46. Neher TM, Lueking DR (2009) Pseudomonas fluorescens ompW: plasmid localization and requirement for naphthalene uptake. Can J Microbiol 55:553–563CrossRefPubMedGoogle Scholar
  47. Nichols NN, Harwood CS (1997) PcaK, a high-affinity permease for the aromatic compounds 4-hydroxybenzoate and protocatechuate from Pseudomonas putida. J Bacteriol 179:5056–5061CrossRefPubMedPubMedCentralGoogle Scholar
  48. Nikaido H (2003) Molecular basis of bacterial outer membrane permeability. Microbiol Mol Biol Rev 67:593–656CrossRefPubMedPubMedCentralGoogle Scholar
  49. Noda K, Watanabe K, Maruhashi K (2003) Isolation of the Pseudomonas aeruginosa gene affecting uptake of dibenzothiophene in n-tetradecane. J Biosci Bioeng 95:504–511CrossRefPubMedGoogle Scholar
  50. Noordman WH, Janssen DB (2002) Rhamnolipid stimulates uptake of hydrophobic compounds by Pseudomonas aeruginosa. Appl Environ Microbiol 68:4502–4508CrossRefPubMedPubMedCentralGoogle Scholar
  51. Olsen RH, Kukor JJ, Kaphammer B (1994) A novel toluene-3-monooxygenase pathway cloned from Pseudomonas pickettii PKO1. J Bacteriol 176:3749–3756CrossRefPubMedPubMedCentralGoogle Scholar
  52. Pao SS, Paulsen IT, Saier MH Jr (1998) Major facilitator superfamily. Microbiol Mol Rev 62:1–34Google Scholar
  53. Phoenix P, Keane A, Patel A, Bergeron H, Ghoshal S, Lau PCK (2003) Characterization of a new solvent-responsive gene locus in Pseudomonas putida F1 and its functionalization as a versatile biosensor. Environ Microbiol 12:1309–1327CrossRefGoogle Scholar
  54. Prieto MA, García JL (1997) Identification of the 4-hydroxyphenylacetate transport gene of Escherichia coli W: construction of a highly sensitive cellular biosensor. FEBS Lett 414:293–297CrossRefPubMedGoogle Scholar
  55. Ramos JL, Duque E, Godoy P, Segura A (1998) Efflux pumps involved in toluene tolerance in Pseudomonas putida DOT-T1E. J Bacteriol 180:3323–3329PubMedPubMedCentralGoogle Scholar
  56. Ramos JL, Duque E, Gallegos MT, Godoy P, Ramos-Gonzalez MI, Rojas A, Teran W, Segura A (2002) Mechanisms of solvent tolerance in Gram-negative bacteria. Annu Rev Microbiol 56:743–768CrossRefPubMedGoogle Scholar
  57. Ramos JL, Sol Cuenca M, Molina-Santiago C, Segura A, Duque E, Gómez-García MR, Udaondo Z, Roca A (2015) Mechanisms of solvent resistance mediated by interplay of cellular factors in Pseudomonas putida. FEMS Microbiol Rev 39:555–566CrossRefPubMedGoogle Scholar
  58. Ramos-Gonzalez MI, Olson M, Gatenby AA, Mosqueda G, Manzanera M, Campos MJ, Vichez S, Ramos JL (2002) Cross-regulation between a novel two-component signal transduction system for catabolism of toluene in Pseudomonas mendocina and the TodST system from Pseudomonas putida. J Bacteriol 184:7062–7067CrossRefPubMedPubMedCentralGoogle Scholar
  59. Rodrigues AC, Wuertz S, Brito AG, Melo LF (2005) Fluorene and phenanthrene uptake by Pseudomonas putida ATCC 17514: kinetics and physiological aspects. Biotechnol Bioeng 90:281–289CrossRefPubMedGoogle Scholar
  60. Rojas A, Duque E, Mosqueda G, Golden G, Hurtado A, Ramos JL, Segura A (2001) Three efflux pumps are required to provide efficient tolerance to toluene in Pseudomonas putida DOT-T1E. J Bacteriol 183:3967–3973CrossRefPubMedPubMedCentralGoogle Scholar
  61. Romero-Silva MJ, Méndez V, Agulló L, Seeger M (2013) Genomic and functional analyses of the gentisate and protocatechuate ring-cleavage pathways and related 3-hydroxybenzoate and 4-hydroxybenzoate peripheral pathways in Burkholderia xenovorans LB400. PLoS One 8:e56038CrossRefPubMedPubMedCentralGoogle Scholar
  62. Saier MH Jr (2006) Transport classification database.
  63. Saier MH Jr, Paulsen IT (2001) Phylogeny of multidrug transporters. Semin Cell Dev Biol 12:205–213Google Scholar
  64. Saier MH Jr, Beatty JT, Goffeau A, Harley KT, Heijne WH, Huang SC, Jack DL, Jahn PS, Lew K, Liu J, Pao SS, Paulsen IT, Tseng TT, Virk PS (1999) The major facilitator superfamily. J Mol Microbiol Biotechnol 1:257–279Google Scholar
  65. Scott CC, Finnerty WR (1976) Characterization of intracytoplasmic hydrocarbon inclusions from the hydrocarbon-oxidizing Acinetobacter species HO1-N. J Bacteriol 127:481–489PubMedPubMedCentralGoogle Scholar
  66. Shetty A, Hickey WJ (2014) Effects of outer membrane vesicle formation, surface-layer production and nanopod development on the metabolism of phenanthrene by Delftia acidovorans Cs1-4. PLoS One 9:e92143CrossRefPubMedPubMedCentralGoogle Scholar
  67. Shetty A, Chen S, Tocheva EI, Jensen GJ, Hickey WJ (2011) Nanopods: a new bacterial structure and mechanism for deployment of outer membrane vesicles. PLoS One 6:e20725CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sikkema J, De Bont JAM, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222PubMedPubMedCentralGoogle Scholar
  69. Tan K, Chang C, Cuff M, Osipiuk J, Landorf E, Mack JC, Zerbs S, Joachimiak A, Collart FR (2013) Structural and functional characterization of solute binding proteins for aromatic compounds derived from lignin: p-coumaric acid and related aromatic acids. Proteins 81:1709–1726CrossRefPubMedPubMedCentralGoogle Scholar
  70. 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 6:3121–3136CrossRefPubMedGoogle Scholar
  71. van Beilen JB, Wubbolts MG, Witholt B (1994) Genetics of alkane oxidation by Pseudomonas oleovorans. Biodegradation 5:161–174CrossRefPubMedGoogle Scholar
  72. van Beilen JB, Panke S, Lucchini S, Franchini AG, Röthlisberger M, Witholt B (2001) Analysis of Pseudomonas putida alkane-degradation gene clusters and flanking insertion sequences: evolution and regulation of the alk genes. Microbiology 147:1621–1630CrossRefPubMedGoogle Scholar
  73. van den Berg B (2005) The FadL family: unusual transporters for unusual substrates. Curr Opin Struct Biol 15:401–407CrossRefPubMedGoogle Scholar
  74. van den Berg B (2010a) Bacterial cleanup: lateral diffusion of hydrophobic molecules through protein channel walls. Biomol Concepts 1:263–270PubMedGoogle Scholar
  75. van den Berg B (2010b) Going forward laterally: transmembrane passage of hydrophobic molecules through protein channel walls. Chembiochem 11:1339–1343CrossRefPubMedPubMedCentralGoogle Scholar
  76. van den Berg B, Black PN, Clemons WMJ, Rapoport TA (2004) Crystal structure of the long-chain fatty acid transporter FadL. Science 304:1506–1509CrossRefPubMedGoogle Scholar
  77. Vaneechoutte M, Young DM, Ornston LN, De Baere T, Nemec A, Van Der Reijden T, Carr E, Tjernberg I, Dijkshoorn L (2006) Naturally transformable Acinetobacter sp. strain ADP1 belongs to the newly described species Acinetobacter baylyi. Appl Environ Microbiol 72:932–936CrossRefPubMedPubMedCentralGoogle Scholar
  78. Volkering F, Breure AM, Sterkenberg A, van Andel JG (1992) Microbial degradation of polycyclic aromatic hydrocarbons: effect of substrate availability on bacterial growth kinetics. Appl Microbiol Biotechnol 36:548–552CrossRefGoogle Scholar
  79. Wang Y, Rawlings M, Gibson DT, Labbé D, Bergeron H, Brousseau R, Lau PCK (1995) Identification of a membrane protein and a truncated LysR-type regulator associated with the toluene degradation pathway in Pseudomonas putida F1. Mol Gen Genet 246:570–579CrossRefPubMedGoogle Scholar
  80. Whitman BE, Lueking DR, Mihelcic JR (1998) Naphthalene uptake by a Pseudomonas fluorescens isolate. Can J Microbiol 44:1086–1093CrossRefPubMedGoogle Scholar
  81. Wick LY, de Munain AR, Springael D, Harms H (2002) Responses of Mycobacterium sp. LB501T to the low bioavailability of solid anthracene. Appl Microbiol Biotechnol 58:378–385CrossRefPubMedGoogle Scholar
  82. Wodzinski RS, Bertolini D (1972) Physical state in which naphthalene and bibenzyl are utilized by bacteria. Appl Microbiol 23:1077–1081PubMedPubMedCentralGoogle Scholar
  83. Wodzinski RS, Coyle JE (1974) Physical state of phenanthrene for utilization by bacteria. Appl Microbiol 27:1081–1084PubMedPubMedCentralGoogle Scholar
  84. Xu Y, Gao X, Wang S-H, Liu H, Williams PA, Zhou N-Y (2012a) MhbT is a specific transporter for 3-hydroxybenzoate uptake by Gram-negative bacteria. Appl Environ Microbiol 78:6113–6120CrossRefPubMedPubMedCentralGoogle Scholar
  85. Xu Y, Wang S-H, Chao H-J, Liu S-J, Zhou N-Y (2012b) Biochemical and molecular characterization of the gentisate transporter GenK in Corynebacterium glutamicum. PLoS One 7:e38701CrossRefPubMedPubMedCentralGoogle Scholar
  86. Xu Y, Chen B, Chao H-J, Zhou N-Y (2013) mhpT encodes an active transporter involved in 3-(3-hydroxyphenyl)propionate catabolism by Escherichia coli K-12. Appl Environ Microbiol 79:6362–6368CrossRefPubMedPubMedCentralGoogle Scholar
  87. Zylstra GJ, Gibson DT (1989) Toluene degradation by Pseudomonas putida F1: nucleotide sequence of the todC1C2BADE genes and their expression in E. coli. J Biol Chem 264:14940–14946PubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Microbiology and Molecular Genetics, College of Biological SciencesUniversity of CaliforniaDavisUSA
  2. 2.Department of Biology, College of Arts and SciencesUniversity of St. ThomasSt. PaulUSA

Personalised recommendations