1887

Microbiology Society logo

Volume 156, Issue 3

FdTonB is involved in the photoregulation of cellular morphology during complementary chromatic adaptation in Free

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 .

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): AP, allophycocyanin , CCA, complementary chromatic adaptation , chla , chlorophyll a , DIC, differential interference contrast microscopy, GL, green light , GRP, glycine-rich protein , PBP, phycobiliprotein , PBS, phycobilisome , PC, phycocyanin , PE, phycoerythrin , RL, red light , TBRD, TonB-related domain and WT, wild-type
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.035410-0
2010-03-01
2024-04-28
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
     [Google Scholar]
  2. Bennett A., Bogorad L. 1973; Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol 58:419–435
     [Google Scholar]
  3. Bogorad L. 1975; Phycobiliproteins and complementary chromatic adaptation. Annu Rev Plant Physiol 26:369–401
     [Google Scholar]
  4. Bordowitz J. R., Montgomery B. L. 2008; Photoregulation of cellular morphology during complementary chromatic adaptation requires sensor-kinase-class protein RcaE in Fremyella diplosiphon. J Bacteriol 190:4069–4074
     [Google Scholar]
  5. Bordowitz J. R., Whitaker M. J., Montgomery B. L. 2010; Independence and interdependence of the photoregulation of 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 7120 to select for double recombinants and to entrap insertion sequences. J Bacteriol 172:3138–3145
     [Google Scholar]
  7. Campbell D. 1996; Complementary chromatic adaptation alters photosynthetic strategies in the cyanobacterium Calothrix. Microbiology 142:1255–1263
     [Google Scholar]
  8. Cartron M. L., Maddocks S., Gillingham P., Craven C. J., Andrews S. C. 2006; Feo – transport of ferrous iron into bacteria. Biometals 19:143–157
     [Google Scholar]
  9. Chu B. C., Peacock R. S., Vogel H. J. 2007; Bioinformatic analysis of the TonB protein family. Biometals 20:467–483
     [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 efficiently mobilized from Escherichia coli into the chromatically adapting cyanobacterium, Fremyella diplosiphon. Plasmid 30:90–105
     [Google Scholar]
  11. Cobley J., Seneviratne L., Drong L., Thounaojam M., Oda J. F., Carroll J. 1999; Transposition of Tn 5 derivatives in the chromatically adapting cyanobacterium, Fremyella diplosiphon. In The Phototrophic Prokaryotes pp 443–451 Edited by Peschek G., Löffelhardt W., Schmetterer G. New York: Kluwer Academic;
     [Google Scholar]
  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 an activator required for expression of the phycoerythrin operon ( cpeBA) in the cyanobacterium Fremyella diplosiphon and is encoded in the phycoerythrin linker-polypeptide operon ( cpeCDESTR. Mol Microbiol 44:1517–1531
     [Google Scholar]
  13. Cserzö M., Wallin E., Simon I., von Heijne G., Elofsson A. 1997; Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng 10:673–676
     [Google Scholar]
  14. Divakaruni A. V., Loo R. R. O., Xie Y., Loo J. A., Gober J. W. 2005; The cell-shape protein MreC interacts with extracytoplasmic proteins including cell wall assembly complexes in Caulobacter crescentus. Proc Natl Acad Sci U S A 102:18602–18607
     [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 structural constraints in the TonB protein of Escherichia coli. FEBS Lett 208:211–216
     [Google Scholar]
  17. Finn R. D., Mistry J., Schuster-Bockler B., Griffiths-Jones S., Hollich V., Lassmann T., Moxon S., Marshall M., Khanna A. other authors 2006; Pfam: clans, web tools and services. Nucleic Acids Res 34:D247–D251
     [Google Scholar]
  18. Gasteiger E., Hoogland C., Gattiker A., Duvaud S., Wilkins M. R., Appel R. D., Bairoch A. 2005; Protein identification and analysis tools on the ExPASy server. In The Proteomics Protocols Handbook pp 571–607 Edited by Walker J. M. Totowa, NJ: Humana Press;
     [Google Scholar]
  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
     [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
     [Google Scholar]
  21. Keren N., Aurora R., Pakrasi H. B. 2004; Critical roles of bacterioferritins in iron storage and proliferation of cyanobacteria. Plant Physiol 135:1666–1673
     [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 limitation in the marine cyanobacterium Trichodesmium reveals new insights into regulation of photosynthesis and nitrogen fixation. New Phytol 179:784–798
     [Google Scholar]
  23. Larsen R. A., Postle K. 2001; Conserved residues Ser16 and His20 and their relative positioning are essential for TonB activity, cross-linking of TonB with ExbB, and the ability of TonB to respond to proton motive force. J Biol Chem 276:8111–8117
     [Google Scholar]
  24. Larsen R. A., Wood G. E., Postle K. 1993; The conserved proline-rich motif is not essential for energy transduction by Escherichia coli TonB protein. Mol Microbiol 10:943–953
     [Google Scholar]
  25. Larsen R. A., Myers P. S., Skare J. T., Seachord C. L., Darveau R. P., Postle K. 1996; Identification of TonB homologs in the family Enterobacteriaceae and evidence for conservation 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
     [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-rich protein involved in cell elongation. Planta 230:253–265
     [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 functional annotation with the Conserved Domain Database. Nucleic Acids Res 37:D205–D210
     [Google Scholar]
  29. Mirus O., Strauss S., Nicolaisen K., von Haeseler A., Schleiff E. 2009; TonB-dependent transporters and their occurrence in cyanobacteria. BMC Biol 7:68
     [Google Scholar]
  30. Moeck G. S., Coulton J. W. 1998; TonB-dependent iron acquisition: mechanisms of siderophore-mediated active transport. Mol Microbiol 28:675–681
     [Google Scholar]
  31. Montgomery B. L. 2008; Shedding new light on the regulation of complementary chromatic adaptation. Cent Eur J Biol 3:351–358
     [Google Scholar]
  32. Neilands J. B. 1995; Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726
     [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 transporter for the siderophore schizokinen in Anabaena sp. Strain PCC 7120. J Bacteriol 190:7500–7507
     [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 membrane receptor. Science 312:1399–1402
     [Google Scholar]
  35. Postle K., Good R. F. 1983; DNA sequence of the Escherichia coli tonB gene. Proc Natl Acad 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
     [Google Scholar]
  37. Postle K., Larsen R. A. 2007; TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 20:453–465
     [Google Scholar]
  38. Sachetto-Martins G., Franco L. O., de Oliveira D. E. 2000; Plant glycine-rich proteins: a family or just proteins with a common motif?. Biochim Biophys Acta 1492:1–14
     [Google Scholar]
  39. Schalk I. J., Yue W. W., Buchanan S. K. 2004; Recognition of iron-free siderophores by TonB-dependent iron transporters. Mol Microbiol 54:14–22
     [Google Scholar]
  40. Schwyn B., Neilands J. B. 1987; Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56
     [Google Scholar]
  41. Seib L. O., Kehoe D. M. 2002; A turquoise mutant genetically separates expression of genes encoding phycoerythrin and its associated linker peptides. J Bacteriol 184:962–970
     [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 iron deficiency and iron reconstitution in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 132:1825–1839
     [Google Scholar]
  44. Stowe-Evans E. L., Ford J., Kehoe D. M. 2004; Genomic DNA microarray analysis: identification of new genes regulated by light color in the cyanobacterium Fremyella diplosiphon. J Bacteriol 186:4338–4349
     [Google Scholar]
  45. Thomas C. M., Smith C. A. 1987; Incompatibility group P plasmids: genetics, evolution, and use in genetic manipulation. Annu Rev Microbiol 41:77–101
     [Google Scholar]
  46. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.035410-0
Loading
FdTonB is involved in the photoregulation of cellular morphology during complementary chromatic adaptation in Fremyella diplosiphon
Microbiology 156, 731 (2010); https://doi.org/10.1099/mic.0.035410-0
/content/journal/micro/10.1099/mic.0.035410-0
/content/journal/micro/10.1099/mic.0.035410-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

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