1887

Abstract

We have characterized a TonB protein (FdTonB) and investigated its function during complementary chromatic adaptation. Sequence similarity analysis of FdTonB (571 aa) led to identification of several conserved domains characteristic of TonB proteins, including an N-terminal transmembrane domain, a central proline-rich spacer and a C-terminal TonB-related domain (TBRD). We identified a novel glycine-rich domain containing (Gly-X) repeats. To assess FdTonB function, we constructed a Δ mutant through homologous recombination based upon truncation of the central proline-rich spacer, glycine-rich domain and TBRD. Our Δ mutant exhibited an aberrant cellular morphology under green light, with expanded cell width compared to the parental wild-type (WT) strain. The cellular morphology of the Δ mutant recovered upon WT expression. Interestingly, expression was found to be independent of RcaE. As Δ and WT strains respond in the same way when grown under iron-replete versus iron-limited conditions, our results suggest that FdTonB is not involved in the classic TonB function of mediating cellular adaptation to iron limitation, but exhibits a novel function related to the photoregulation of cellular morphology in .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.035410-0
2010-03-01
2019-10-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/3/731.html?itemId=/content/journal/micro/10.1099/mic.0.035410-0&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 Biol 215, 403–410.[CrossRef]
    [Google Scholar]
  2. Bennett, A. & Bogorad, L. ( 1973; ).Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol 58, 419–435.[CrossRef]
    [Google Scholar]
  3. Bogorad, L. ( 1975; ). Phycobiliproteinsand complementary chromatic adaptation. Annu Rev Plant Physiol 26, 369–401.[CrossRef]
    [Google Scholar]
  4. Bordowitz, J. R. & Montgomery, B. L. ( 2008; ). Photoregulation of cellular morphology during complementarychromatic adaptation requires sensor-kinase-class protein RcaE in Fremyelladiplosiphon. J Bacteriol 190, 4069–4074.[CrossRef]
    [Google Scholar]
  5. Bordowitz, J. R., Whitaker, M. J. & Montgomery, B. L. ( 2010; ). Independence and interdependence of the photoregulationof pigmentation and development in Fremyella diplosiphon. Comm Integ Biol in press
    [Google Scholar]
  6. Cai, Y. P. & Wolk, C. P. ( 1990; ).Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120to select for double recombinants and to entrap insertion sequences. J Bacteriol 172, 3138–3145.
    [Google Scholar]
  7. Campbell, D. ( 1996; ). Complementary chromaticadaptation alters photosynthetic strategies in the cyanobacterium Calothrix. Microbiology 142, 1255–1263.[CrossRef]
    [Google Scholar]
  8. Cartron, M. L., Maddocks, S., Gillingham, P., Craven, C. J. &Andrews, S. C. ( 2006; ). Feo – transport of ferrousiron into bacteria. Biometals 19, 143–157.[CrossRef]
    [Google Scholar]
  9. Chu, B. C., Peacock, R. S. & Vogel, H. J. ( 2007; ). Bioinformatic analysis of the TonB protein family. Biometals 20, 467–483.[CrossRef]
    [Google Scholar]
  10. Cobley, J. G., Zerweck, E., Reyes, R., Mody, A., Seludo-Unson,J. R., Jaeger, H., Weerasuriya, S. & Navankasattusas, S. ( 1993; ). Construction of shuttle plasmids which can be efficientlymobilized from Escherichia coli into the chromatically adapting cyanobacterium, Fremyella diplosiphon. Plasmid 30, 90–105.[CrossRef]
    [Google Scholar]
  11. Cobley, J., Seneviratne, L., Drong, L., Thounaojam, M., Oda,J. F. & Carroll, J. ( 1999; ). Transposition of Tn5 derivatives in the chromatically adapting cyanobacterium, Fremyelladiplosiphon. In The Phototrophic Prokaryotes, pp. 443–451.Edited by G. Peschek, W. Löffelhardt & G. Schmetterer. New York:Kluwer Academic.
  12. Cobley, J. G., Clark, A. C., Weerasurya, S., Queseda, F. A.,Xiao, J. Y., Bandrapali, N., D'Silva, I., Thounaojam, M.,Oda, J. F. & other authors ( 2002; ). CpeR is anactivator required for expression of the phycoerythrin operon (cpeBA) in the cyanobacterium Fremyella diplosiphon and is encodedin the phycoerythrin linker-polypeptide operon (cpeCDESTR). Mol Microbiol 44, 1517–1531.[CrossRef]
    [Google Scholar]
  13. Cserzö, M., Wallin, E., Simon, I., von Heijne, G. &Elofsson, A. ( 1997; ). Prediction of transmembrane alpha-helicesin prokaryotic membrane proteins: the dense alignment surface method. Protein Eng 10, 673–676.[CrossRef]
    [Google Scholar]
  14. Divakaruni, A. V., Loo, R. R. O., Xie, Y., Loo, J. A. &Gober, J. W. ( 2005; ). The cell-shape protein MreC interactswith extracytoplasmic proteins including cell wall assembly complexes in Caulobacter crescentus. Proc Natl Acad Sci U S A 102, 18602–18607.[CrossRef]
    [Google Scholar]
  15. Elhai, J. & Wolk, C. P. ( 1988; ).Conjugal transfer of DNA to cyanobacteria. Methods Enzymol 167, 747–754.
    [Google Scholar]
  16. Evans, J. S., Levine, B. A., Trayer, I. P., Dorman, C. J. &Higgins, C. F. ( 1986; ). Sequence-imposed structuralconstraints in the TonB protein of Escherichia coli. FEBS Lett 208, 211–216.[CrossRef]
    [Google Scholar]
  17. Finn, R. D., Mistry, J., Schuster-Bockler, B., Griffiths-Jones,S., Hollich, V., Lassmann, T., Moxon, S., Marshall, M., Khanna, A. & otherauthors ( 2006; ). Pfam: clans, web tools and services. Nucleic Acids Res 34, D247–D251.[CrossRef]
    [Google Scholar]
  18. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins,M. R., Appel, R. D. & Bairoch, A. ( 2005; ). Proteinidentification and analysis tools on the ExPASy server. In The ProteomicsProtocols Handbook, pp. 571–607. Edited by J. M. Walker. Totowa,NJ: Humana Press.
  19. Katoh, H., Hagino, N., Grossman, A. R. & Ogawa, T. ( 2001; ). Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183, 2779–2784.[CrossRef]
    [Google Scholar]
  20. Kehoe, D. M. & Gutu, A. ( 2006; ).Responding to color: the regulation of complementary chromatic adaptation. Annu Rev Plant Biol 57, 127–150.[CrossRef]
    [Google Scholar]
  21. Keren, N., Aurora, R. & Pakrasi, H. B. ( 2004; ). Critical roles of bacterioferritins in iron storage and proliferationof cyanobacteria. Plant Physiol 135, 1666–1673.[CrossRef]
    [Google Scholar]
  22. Küpper, H., Šetlík, I., Seibert, S., Prásil,O., Setlikova, E., Strittmatter, M., Levitan, O., Lohscheider, J., Adamska,I. & Berman-Frank, I. ( 2008; ). Iron limitationin the marine cyanobacterium Trichodesmium reveals new insights intoregulation of photosynthesis and nitrogen fixation. New Phytol 179, 784–798.[CrossRef]
    [Google Scholar]
  23. Larsen, R. A. & Postle, K. ( 2001; ).Conserved residues Ser16 and His20 and their relativepositioning are essential for TonB activity, cross-linking of TonB with ExbB,and the ability of TonB to respond to proton motive force. J BiolChem 276, 8111–8117.
    [Google Scholar]
  24. Larsen, R. A., Wood, G. E. & Postle, K. ( 1993; ). The conserved proline-rich motif is not essential for energytransduction by Escherichia coli TonB protein. Mol Microbiol 10, 943–953.[CrossRef]
    [Google Scholar]
  25. Larsen, R. A., Myers, P. S., Skare, J. T., Seachord, C. L.,Darveau, R. P. & Postle, K. ( 1996; ). Identificationof TonB homologs in the family Enterobacteriaceae and evidence forconservation of TonB-dependent energy transduction complexes. J Bacteriol 178, 1363–1373.
    [Google Scholar]
  26. Maglott, D., Ostell, J., Pruitt, K. D. & Tatusova, T. ( 2007; ). Entrez Gene: gene-centered information at NCBI. Nucleic Acids Res 35, D26–D31.[CrossRef]
    [Google Scholar]
  27. Mangeon, A., Magioli, C., Menezes-Salgueiro, A. D., Cardeal,V., de Oliveira, C., Galvao, V. C., Margis, R., Engler, G. & Sachetto-Martins,G. ( 2009; ). AtGRP5, a vacuole-located glycine-richprotein involved in cell elongation. Planta 230, 253–265.[CrossRef]
    [Google Scholar]
  28. Marchler-Bauer, A., Anderson, J. B., Chitsaz, F., Derbyshire,M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C., Gonzales,N. R. & other authors ( 2009; ). CDD: specific functionalannotation with the Conserved Domain Database. Nucleic Acids Res 37, D205–D210.[CrossRef]
    [Google Scholar]
  29. Mirus, O., Strauss, S., Nicolaisen, K., von Haeseler, A. &Schleiff, E. ( 2009; ). TonB-dependent transporters andtheir occurrence in cyanobacteria. BMC Biol 7, 68 [CrossRef]
    [Google Scholar]
  30. Moeck, G. S. & Coulton, J. W. ( 1998; ). TonB-dependent iron acquisition: mechanisms of siderophore-mediated activetransport. Mol Microbiol 28, 675–681.
    [Google Scholar]
  31. Montgomery, B. L. ( 2008; ). Shedding newlight on the regulation of complementary chromatic adaptation. Cent Eur J Biol 3, 351–358.[CrossRef]
    [Google Scholar]
  32. Neilands, J. B. ( 1995; ). Siderophores:structure and function of microbial iron transport compounds. J Biol Chem 270, 26723–26726.[CrossRef]
    [Google Scholar]
  33. Nicolaisen, K., Moslavac, S., Samborski, A., Valdebenito, M.,Hantke, K., Maldener, I., Muro-Pastor, A. M., Flores, E. & Schleiff, E. ( 2008; ). Alr0397 is an outer membrane transporterfor the siderophore schizokinen in Anabaena sp. Strain PCC 7120. J Bacteriol 190, 7500–7507.[CrossRef]
    [Google Scholar]
  34. Pawelek, P. D., Croteau, N., Ng-Thow-Hing, C., Khursigara, C.M., Moiseeva, N., Allaire, M. & Coulton, J. W. ( 2006; ). Structure of TonB in complex with FhuA, E. coli outer membranereceptor. Science 312, 1399–1402.[CrossRef]
    [Google Scholar]
  35. Postle, K. & Good, R. F. ( 1983; ).DNA sequence of the Escherichia coli tonB gene. Proc NatlAcad Sci U S A 80, 5235–5239.
    [Google Scholar]
  36. Postle, K. & Kadner, R. J. ( 2003; ).Touch and go: tying TonB to transport. Mol Microbiol 49, 869–882.[CrossRef]
    [Google Scholar]
  37. Postle, K. & Larsen, R. A. ( 2007; ).TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 20, 453–465.[CrossRef]
    [Google Scholar]
  38. Sachetto-Martins, G., Franco, L. O. & de Oliveira, D. E. ( 2000; ). Plant glycine-rich proteins: a family orjust proteins with a common motif? Biochim Biophys Acta 1492, 1–14.[CrossRef]
    [Google Scholar]
  39. Schalk, I. J., Yue, W. W. & Buchanan, S. K. ( 2004; ). Recognition of iron-free siderophores by TonB-dependentiron transporters. Mol Microbiol 54, 14–22.[CrossRef]
    [Google Scholar]
  40. Schwyn, B. & Neilands, J. B. ( 1987; ). Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160, 47–56.[CrossRef]
    [Google Scholar]
  41. Seib, L. O. & Kehoe, D. M. ( 2002; ).A turquoise mutant genetically separates expression of genes encoding phycoerythrinand its associated linker peptides. J Bacteriol 184, 962–970.[CrossRef]
    [Google Scholar]
  42. Sherman, D. M. & Sherman, L. A. ( 1983; ). Effect of iron deficiency and iron restoration on ultrastructure of Anacystis nidulans. J Bacteriol 156, 393–401.
    [Google Scholar]
  43. Singh, A. K., McIntyre, L. M. & Sherman, L. A. ( 2003; ). Microarray analysis of the genome-wide response to irondeficiency and iron reconstitution in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 132, 1825–1839.[CrossRef]
    [Google Scholar]
  44. Stowe-Evans, E. L., Ford, J. & Kehoe, D. M. ( 2004; ). Genomic DNA microarray analysis: identification of new genesregulated by light color in the cyanobacterium Fremyella diplosiphon. J Bacteriol 186, 4338–4349.[CrossRef]
    [Google Scholar]
  45. Thomas, C. M. & Smith, C. A. ( 1987; ). Incompatibility group P plasmids: genetics, evolution, and use in geneticmanipulation. Annu Rev Microbiol 41, 77–101.[CrossRef]
    [Google Scholar]
  46. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). clustal w: improving the sensitivityof progressive multiple sequence alignment through sequence weighting, position-specificgap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.035410-0
Loading
/content/journal/micro/10.1099/mic.0.035410-0
Loading

Data & Media loading...

Supplements

vol. , part 3, pp. 731 - 741

[ PDF, 120 kb], including: Primers used in this study Plasmids Variable cellular morphology of Δ mutants grown under green light



PDF
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