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Transport of Metals: A Key Process in Oxygenic Photosynthesis

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Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 11))

Summary

Metals play important roles in all phases of oxygenic photosynthesis in cyanobacteria, eukaryotic algae and green plants. For the photosynthetic electron transport reactions in the thylakoid membranes, iron, copper, manganese and magnesium are essential cofactors in various proteins and pigment-protein complexes. Zinc, iron and magnesium also play critical roles during the carbon-fixation reactions. In addition, iron, copper and zinc are constituents of superoxide dismutase and other protective enzymes that are essential to maintain the integrity and function of the photosynthetic apparatus in its highly reactive environment. Inside any living cell, concentrations of various metals are maintained within specific ranges. If the concentration of any metal is below a lower threshold level, organisms suffer from this metal ion deficiency. On the other hand, excess amount of many metals can be toxic. Since metals are both essential and potentially toxic, they are under strict homeostatic control that requires a balance between their uptake and efflux. Usually, metals are transported across cell and organellar membranes via specific transporters. Many families of metal uptake and efflux transporters have recently been described in both prokaryotes and eukaryotes. In 1996, the publication of the complete genome sequence of the cyanobacterium Synechocystis sp. PCC 6803, an oxygenic photosynthetic organism, provided valuable information about a number of potential metal transporters in this organism. During the past few years, genetic and biochemical dissection of some of these transporters has yielded important functional data about both the transport processes and their regulations, for a number of metals. Recent completion of the genome sequence of the Arabidopsis thaliana has opened additional exciting opportunities for functional genomic analysis of metal homeostasis and its influence on photosynthesis. In this chapter, we discuss transport of iron, copper, manganese, zinc and magnesium, primarily using the Synechocystis 6803 paradigm.

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References

  • Althaus EW, Outten CE, Olson KE, Cao H and O’Halloran TV (1999) The ferric uptake regulation (Fur) repressor is a zinc metalloprotein. Biochemistry 38: 6559–6569

    Article  CAS  PubMed  Google Scholar 

  • Bartsevich VV and Pakrasi HB (1995) Molecular identification of an ABC transporter complex for manganese: Analysis of a cyanobacterial mutant strain impaired in the photosynthetic oxygen evolution process. EMBO J 14: 1845–1853

    CAS  PubMed  Google Scholar 

  • Bartsevich VV and Pakrasi HB (1996) Manganese transport in the cyanobacterium Synechacystis sp. PCC 6803. J Biol Chem 271: 26057–26061

    CAS  PubMed  Google Scholar 

  • Bartsevich VV and Pakrasi HB (1999) Membrane topology of MntB, the transmembrane protein component of an ABC transporter system for manganese in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 181: 3591–3593

    CAS  PubMed  Google Scholar 

  • Buchanan BB, Gruissem W and Jones RL (2000) Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville

    Google Scholar 

  • Chadd HE, Newman J, Mann NH and Carr NG (1996) Identification of iron superoxide dismutase and a copper/zinc superoxide dismutase enzyme activity within the marine cyanobacterium Synechococcus sp. WH 7803. FEMS Microbiol Lett 138: 161–165

    CAS  PubMed  Google Scholar 

  • Cheniae GM and Martin IF (1970) Sites offunction of manganese within Photosystem II. Roles in O2 evolution and system II. Biochim Biophys Acta 197: 219–239

    CAS  PubMed  Google Scholar 

  • Cook WJ, Kar SR, Taylor KB and Hall LM (1998) Crystal structure of the cyanobacterial metallothionein repressor SmtB: a model for metalloregulatory proteins. J Mol Biol 275: 337–346

    Article  CAS  PubMed  Google Scholar 

  • Debus RJ (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102: 269–352

    CAS  PubMed  Google Scholar 

  • Dismukes CJ (1996) Manganese enzymes with binuclear sites. Chem. Rev. 96: 2909–2926

    Article  CAS  PubMed  Google Scholar 

  • Driessen AJ, Rosen BP and Konings WN (2000) Diversity of transport mechanisms: Common structural principles. Trends Biochem Sci 25: 397–401

    Article  CAS  PubMed  Google Scholar 

  • Eide DJ (1998) The molecular biology of metal ion transport in Saccharomyces cerevisiae. Annu Rev Nutr 18: 441–469

    Article  CAS  PubMed  Google Scholar 

  • Escolar L, Perez-Martin J and de Lorenzo V (1999) Opening the iron box: Transcriptional metalloregulation by the Fur protein. J Bacteriol 181: 6223–6229

    CAS  PubMed  Google Scholar 

  • Garcia-Dominguez M, Lopez-Maury L, Florencio FJ and Reyes JC (2000) A gene cluster involved in metal homeostasis in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 182: 1507–1514

    Article  CAS  PubMed  Google Scholar 

  • Ghassemian M and Straus NA (1996) Fur regulates the expression of iron-stress genes in the cyanobacterium Synechococcus sp. strain PCC 7942. Microbiology 142: 1469–1476

    CAS  PubMed  Google Scholar 

  • Guerinot ML (1994) Microbial iron transport. Annu Rev Microbiol 48: 743–772

    Article  CAS  PubMed  Google Scholar 

  • Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465: 190–198

    CAS  PubMed  Google Scholar 

  • Guerinot ML and Eide D (1999) Zeroing in on zinc uptake in yeast and plants. Curr Opin Plant Biol 2: 244–249

    Article  CAS  PubMed  Google Scholar 

  • Harrison MD, Jones CE, Solioz M and Dameron CT (2000) Intracellular copper routing: the role of copper chaperones. Trends Biochem Sci 25: 29–32

    Article  CAS  PubMed  Google Scholar 

  • Kanamaru K, Kashiwagi S and Mizuno T (1993) The cyanobacterium, Synechococcus sp. PCC7942, possesses two distinct genes encoding cation-transporting P-type ATPases. FEBS Lett 330: 99–104

    Article  CAS  PubMed  Google Scholar 

  • Kanamaru K, Kashiwagi S and Mizuno T (1994) A copper-transporting P-type ATPase found in the thylakoid membrane of the cyanobacterium Synechococcus species PCC7942. Mol Microbiol 13: 369–377

    CAS  PubMed  Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M and Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3: 109–136

    CAS  PubMed  Google Scholar 

  • Katoh H, Grossman AR, Hagino N and Ogawa T (2000) A gene of Synechocystis sp. strain PCC 6803 encoding a novel iron transporter. J Bacteriol 182: 6523–6524

    Article  CAS  PubMed  Google Scholar 

  • Katoh H, Hagino N, Grossman AR and Ogawa T (2001) Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC6803. J Bacteriol 183: 2779–2784

    Article  CAS  PubMed  Google Scholar 

  • Kolenbrander PE, Andersen RN, Baker RA and Jenkinson HF (1998) The adhesion-associated sca operon in Streptococcus gordonii encodes an inducible high-affinity ABC transporter for Mn2+ uptake. J Bacteriol 180: 290–295

    CAS  PubMed  Google Scholar 

  • Lipscomb WN and Sträter N (1996) Recent advances in zinc enzymology. Chem. Rev. 96: 2375–2433

    Article  CAS  PubMed  Google Scholar 

  • Marschner H and Römheld V (1994) Strategies of plants for acquisition of iron. Plant Soil 165: 261–274

    Article  CAS  Google Scholar 

  • Moncrief MB and Maguire ME (1999) Magnesium transport in prokaryotes. J Biol Inorg Chem 4: 523–527

    CAS  PubMed  Google Scholar 

  • Morby AP, Turner JS, Huckle JW and Robinson NJ (1993) SmtB is a metal-dependent repressor of the cyanobacterial metallothionein gene smtA: Identification of a Zn inhibited DNA-protein complex. Nucleic Acids Res 21: 921–925

    CAS  PubMed  Google Scholar 

  • Pakrasi HB (1995) Genetic analysis of the form and function of Photosystem I and Photosystem II. Annu Rev Genet 29: 755–776

    Article  CAS  PubMed  Google Scholar 

  • Patzer SI and Hantke K (1998) The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol Microbiol 28: 1199–1210

    Article  CAS  PubMed  Google Scholar 

  • Patzer SI and Hantke K (2000) The zinc-responsive regulator Zur and its control of the znu gene cluster encoding the ZnuABC zinc uptake system in Escherichia coli. 3 Biol Chem 275: 24321–24332

    CAS  Google Scholar 

  • Robinson NJ, Rutherford JC, Pocock MR and Cavet JS (2000) Metal metabolism and toxicity: Repetitive DNA. In: Whitton BA and Potts M (eds) The Ecology of Cyanobacteria, pp 443–463. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Saier MH, Jr. (1998) Molecular phylogeny as a basis for the classification of transport proteins from bacteria, archaea and eukarya. Adv Microb Physiol 40: 81–136

    CAS  PubMed  Google Scholar 

  • Saier MH, Jr. (2000) A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol Mol Biol Rev 64: 354–411

    CAS  PubMed  Google Scholar 

  • Smith RL and Maguire ME (1998) Microbial magnesium transport: unusual transporters searching for identity. Mol Microbiol 28: 217–226

    Article  CAS  PubMed  Google Scholar 

  • Supek F, Supekova L, Nelson H and Nelson N (1997) Function of metal-ion homeostasis in the cell division cycle, mitochondrial protein processing, sensitivity to mycobacterial infection and brain function. J Exp Biol 200: 321–330

    CAS  PubMed  Google Scholar 

  • Tam R and Saier MH, Jr. (1993) Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev 57: 320–346

    CAS  PubMed  Google Scholar 

  • Thelwell C, Robinson NJ and Turner-Cavet JS (1998) An SmtB-like repressor from Synechocystis PCC 6803 regulates a zinc exporter. Proc Natl Acad Sci U S A 95: 10728–10733

    Article  CAS  PubMed  Google Scholar 

  • Walbot V (2000) Arabidopsis thaliana genome. A green chapter in the book of life. Nature 408: 794–795

    Article  CAS  PubMed  Google Scholar 

  • Williams LE, Pittman JK and Hall JL (2000) Emerging mechanisms for heavy metal transport in plants. Biochim Biophys Acta 1465: 104–126

    CAS  PubMed  Google Scholar 

  • Zhang L, McSpadden B, Pakrasi HB and Whitmarsh J (1992) Copper-mediated regulation of cytochrome c553 and plastocyanin in the cyanobacterium Synechocystis 6803. J Biol Chem 267: 19054–19059

    CAS  PubMed  Google Scholar 

  • Zhang L, Pakrasi HB and Whitmarsh J (1994) Photoautotrophic growth of the cyanobacterium Synechocystis sp. PCC 6803 in the absence of cytochrome c553 and plastocyanin. J Biol Chem 269: 5036–5042

    CAS  PubMed  Google Scholar 

Download references

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© 2001 Kluwer Academic Publishers

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Pakrasi, H., Ogawa, T., Bhattacharrya-Pakrasi, M. (2001). Transport of Metals: A Key Process in Oxygenic Photosynthesis. In: Aro, EM., Andersson, B. (eds) Regulation of Photosynthesis. Advances in Photosynthesis and Respiration, vol 11. Springer, Dordrecht. https://doi.org/10.1007/0-306-48148-0_14

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  • DOI: https://doi.org/10.1007/0-306-48148-0_14

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-0-7923-6332-3

  • Online ISBN: 978-0-306-48148-2

  • eBook Packages: Springer Book Archive

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