1887

Abstract

Tripartite ATP-independent periplasmic transporters (TRAP-T) represent a novel type of secondary active transporter that functions in conjunction with an extracytoplasmic solute-binding receptor. The best characterized TRAP-T family member is from and is specific for C-dicarboxylates [Forward, J. A., Behrendt, M. C., Wyborn, N. R., Cross, R. & Kelly, D. J. (1997). 179, 5482–5493]. It consists of three essential proteins, DctP, a periplasmic C-dicarboxylate-binding receptor, and two integral membrane proteins, DctM and DctQ, which probably span the membrane 12 and 4 times, respectively. Homologues of DctM, DctP and DctQ were identified in all major bacterial subdivisions as well as in archaea. An orphan DctP homologue in the Gram-positive bacterium may serve as a receptor for a two- component transcriptional regulatory system rather than as a constituent of a TRAP-T system. Phylogenetic data suggest that all present day TRAP-T systems probably evolved from a single ancestral transporter with minimal shuffling of constituents between systems. Homologous TRAP-T constituents exhibit decreasing degrees of sequence identity in the order DctM>DctP>DctQ. DctM appears to belong to a large superfamily of transporters, the ion transporter (IT) superfamily, one member of which can function by either protonmotive force- or ATP-dependent energization. It is proposed that IT superfamily members exhibit the unusual capacity to function in conjunction with auxiliary proteins that modify the transport process by providing (i) high-affinity solute reception, (ii) altered energy coupling and (iii) additional yet to be defined functions.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-145-12-3431
1999-12-01
2020-04-03
Loading full text...

Full text loading...

/deliver/fulltext/micro/145/12/1453431a.html?itemId=/content/journal/micro/10.1099/00221287-145-12-3431&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J.. 1990; Basic local alignment search tool. J Mol Biol215:403–410[CrossRef]
    [Google Scholar]
  2. Altschul S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller W., Lipman D. J.. 1997; Gapped blast and psi- blast: a new generation of protein database search programs. . Nucleic Acids Res25:3389–3402[CrossRef]
    [Google Scholar]
  3. Ames G. F.-L.. 1986; Bacterial periplasmic transport systems: structure, mechanism, and evolution. Annu Rev Biochem55:397–425[CrossRef]
    [Google Scholar]
  4. Bailey T. L., Gribskov M.. 1998; Combining evidence using p-values: application to sequence homology searches. Bioinformatics14:48–54[CrossRef]
    [Google Scholar]
  5. Bairoch A., Bucher P., Hofmann K.. 1997; The PROSITE database, its status in 1997. Nucleic Acids Res25:217–221[CrossRef]
    [Google Scholar]
  6. Berks B. C., Richardson D. J., Reilly A., Willis A. C., Ferguson S. J.. 1995; The napEDABC gene cluster encoding the periplasmic nitrate reductase system of Thiosphaera pantotropha. Biochem J309:983–992
    [Google Scholar]
  7. Blair A., Ngo L., Park J., Paulsen I. T., Saier M. H. Jr. 1996; Phylogenetic analyses of the homologous transmembrane channel-forming proteins of the F0F1-ATPases of bacteria, chloroplasts and mitochondria. Microbiology142:17–32[CrossRef]
    [Google Scholar]
  8. Boos W., Lucht J. M.. 1996; Periplasmic binding protein-dependent ABC transporters. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp.1175–1209Edited by Neidhardt F. C..others Washington, DC: American Society for Microbiology;
    [Google Scholar]
  9. Cangelosi G. A., Ankenbauer R. G., Nester E. W.. 1990; Sugars induce the Agrobacterium virulence genes through a periplasmic binding protein and a transmembrane signal protein. Proc Natl Acad Sci USA87:6708–6712[CrossRef]
    [Google Scholar]
  10. Dayhoff M. O., Barker W. C., Hunt L. T.. 1983; Establishing homologies in protein sequences. Methods Enzymol91:524–545
    [Google Scholar]
  11. Devereux J., Haeberli P., Smithies O.. 1984; A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res12:387–395[CrossRef]
    [Google Scholar]
  12. Felsenstein J.. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution39:783–791[CrossRef]
    [Google Scholar]
  13. Feng D.-F., Doolittle R. F.. 1990; Progressive alignment and phylogenetic tree construction of protein sequences. Methods Enzymol183:375–387
    [Google Scholar]
  14. Forward J. A., Behrendt, M. C., Wyborn, N. R., Cross R., Kelly D. J.. 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 Bacteriol179:5482–5493
    [Google Scholar]
  15. Grundy W. N., Bailey T. L., Elkan C. P., Baker M. E.. 1997; Meta-meme: motif-based hidden Markov models of protein families. Comput Appl Biosci13:397–406
    [Google Scholar]
  16. Hamblin M. J., Shaw J. G., Curson J. P., Kelly D. J.. 1990; Mutagenesis, cloning and complementation analysis of C4-dicarboxylate transport genes from Rhodobacter capsulatus. Mol Microbiol4:1567–1574[CrossRef]
    [Google Scholar]
  17. Higgins C. F.. 1992; ABC transporters: from microorganisms to man. Annu Rev Cell Biol8:67–113[CrossRef]
    [Google Scholar]
  18. Higgins C. F., Hyde S. C., Mimmack M. M., Gileadi U., Gill D. R., Gallagher M. P.. 1990; Binding protein- dependent transport systems. J Bioenerg Biomembr22:571–592[CrossRef]
    [Google Scholar]
  19. Huala E., Stigter J., Ausubel F. M.. 1992; The central domain of Rhizobium leguminosarum DctD functions independently to activate transcription. J Bacteriol174:1428–1431
    [Google Scholar]
  20. Hyde S. C., Emsley P., Hartshorn M. J..7 other authors 1990; Structural model of ATP- binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature346:362–365[CrossRef]
    [Google Scholar]
  21. Jacobs M. H. J., van der Heide T., Driessen A. J. M., Konings W. N.. 1996; Glutamate transport in Rhodobacter sphaeroides is mediated by a novel binding protein-dependent secondary transport system. Proc Natl Acad Sci USA93:12786–12790[CrossRef]
    [Google Scholar]
  22. Kemner J. M., Liang X., Nester E. W.. 1997; The Agrobacterium tumefaciens virulence gene chvE is part of a putative ABC- type sugar transport operon. J Bacteriol179:2452–2458
    [Google Scholar]
  23. Klenk H.-P., Clayton R. A., Tomb J.-F..48 other authors 1997; The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature390:364–370[CrossRef]
    [Google Scholar]
  24. Kuan G., Dassa E., Saurin W., Hofnung M., Saier M. H. Jr. 1995; Phylogenetic analyses of the ATP-binding constituents of bacterial extracytoplasmic receptor-dependent ABC-type nutrient uptake permeases. Res Microbiol146:271–278[CrossRef]
    [Google Scholar]
  25. Kuroda M., Dey S., Sanders O. I., Rosen B. P.. 1997; Alternate energy coupling of ArsB, the membrane subunit of the Ars anion-translocating ATPase. J Biol Chem272:326–331[CrossRef]
    [Google Scholar]
  26. Kyte J., Doolittle R. F.. 1982; A simple method for displaying the hydropathic character of a protein. J Mol Biol157:105–132[CrossRef]
    [Google Scholar]
  27. Le T., Tseng T.-T., Saier M. H. Jr. 1999; Flexible programs for the prediction of average amphipathicity of multiply aligned homologous proteins: application to integral membrane transport proteins. Mol Membr Biol16:173–179[CrossRef]
    [Google Scholar]
  28. Maloney P. C.. 1994; Bacterial transporters. Curr Opin Cell Biol6:571–582[CrossRef]
    [Google Scholar]
  29. Maloney P. C., Wilson T. H.. 1996; Ion-coupled transport and transporters. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp.1130–1148Edited by Neidhardt F. C..others Washington, DC: American Society for Microbiology;
    [Google Scholar]
  30. Nakatsu C. H., Korona R., Lenski R. E., DeBruijn F. J., Marsh T. L., Forney L. J.. 1998; Parallel and divergent genotypic evolution in experimental populations of Ralstonia sp. J Bacteriol180:4325–4331
    [Google Scholar]
  31. Nikaido H., Saier M. H. Jr. 1992; Transport proteins in bacteria: common themes in their design. Science258:936–942[CrossRef]
    [Google Scholar]
  32. Obis D., Guillot A., Gripon J.-C., Renault P., Bolotine A., Mistou M. Y.. 1999; 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 (in press)
    [Google Scholar]
  33. Pearson W. R., Lipman D. J.. 1988; Improved tools for biological sequence comparison. Proc Natl Acad Sci USA85:2444–2448[CrossRef]
    [Google Scholar]
  34. Postma P. W., Lengeler J. W., Jacobson G. R.. 1993; Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev57:543–594
    [Google Scholar]
  35. Quiocho F. A., Ledvina P. S.. 1996; Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes. Mol Microbiol20:17–25[CrossRef]
    [Google Scholar]
  36. Saier M. H. Jr. 1994; Computer-aided analyses of transport protein sequences: gleaning evidence concerning function, structure, biogenesis, and evolution. Microbiol Rev58:71–93
    [Google Scholar]
  37. Saier M. H. Jr. 1998; Molecular phylogeny as a basis for the classification of transport proteins from Bacteria, Archaea and Eukarya. Adv Microb Physiol40:81–136
    [Google Scholar]
  38. Saier M. H. Jr. 1999; Eukaryotic transmembrane solute transport systems. In International Review of Cytology: a Survey of Cell Biology pp.61–136Edited by Jeon K. W.. San Diego: Academic Press;
    [Google Scholar]
  39. Saier M. H. Jr, Tseng T.-T.. 1999; Evolutionary origins of transmembrane transport systems. In Transport of Molecules Across Microbial MembranesSociety for General Microbiology Symposium58 pp.252–274 Cambridge: Cambridge University Press;
    [Google Scholar]
  40. Saurin W., Hofnung M., Dassa E.. 1999; Getting in or out: early segregation between importers and exporters in the evolution of ATP-binding cassette (ABC) transporters. J Mol Evol48:22–41[CrossRef]
    [Google Scholar]
  41. Shaw J. G., Kelly D. J.. 1991; Binding protein dependent transport of C4-dicarboxylates in Rhodobacter capsulatus. Arch Microbiol155:466–472[CrossRef]
    [Google Scholar]
  42. Shaw J. G., Hamblin M. J., Kelly D. J.. 1991; Purification, characterization and nucleotide sequence of the periplasmic C4 -dicarboxylate-binding protein (DctP) from Rhodobacter capsulatus. Mol Microbiol5:3055–3062[CrossRef]
    [Google Scholar]
  43. Silver S., Ji G., Bröer, S., Dey, S., Du D., Rosen B. P.. 1993; Orphan enzyme or patriarch of a new tribe: the arsenic resistance ATPase of bacterial plasmids. Mol Microbiol8:637–642[CrossRef]
    [Google Scholar]
  44. Tam R., Saier M. H. Jr. 1993; Structural, functional, and evolutionary relationships among extracellular solute- binding receptors of bacteria. Microbiol Rev57:320–346
    [Google Scholar]
  45. Thompson J. D., Gibson, T. J., Plewniak, F., Jeanmougin F., Higgins D. G.. 1997; The clustal x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res25:4876–4882[CrossRef]
    [Google Scholar]
  46. Tseng T.-T., Gratwick K. S., Kollman J., Park D., Nies D. H., Goffeau A., Saier M. H. Jr. 1999; The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J Mol Microbiol Biotechnol1:107–125
    [Google Scholar]
  47. Walmsley A. R., Shaw J. G., Kelly D. J.. 1992; The mechanism of ligand binding to the periplasmic C4-dicarboxylate binding protein (DctP) from Rhodobacter capsulatus. J Biol Chem267:8064–8072
    [Google Scholar]
  48. Winans S. C.. 1991; An Agrobacterium two-component regulatory system for the detection of chemicals released from plant wounds. Mol Microbiol5:2345–2350[CrossRef]
    [Google Scholar]
  49. Young G. B., Jack D. L., Smith D. W., Saier M. H. Jr. 1999; The amino acid/auxin:proton symport permease family. Biochim Biophys Acta1415:306–322[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-145-12-3431
Loading
/content/journal/micro/10.1099/00221287-145-12-3431
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error