Photosynthesis Research

, Volume 75, Issue 1, pp 71–84 | Cite as

Adaptation to iron deficiency: a comparison between the cyanobacterium Synechococcus elongatus PCC 7942 wild-type and a DpsA-free mutant

  • Klaus-Peter Michel
  • Stephan Berry
  • Awatief Hifney
  • Jochen Kruip
  • Elfriede K. Pistorius
Article

Abstract

To learn more about the adaptive response of Synechococcus elongatus PCC 7942 to iron starvation and the role of DpsA, presumably a protein protecting chromosomal DNA against oxidative damage, we performed a comparative analysis of S. elongatus PCC 7942 wild-type and a DpsA-free mutant, called K11. Relative to wild-type, the DpsA-free mutant had significantly higher amounts of phycocyanin and allophycocyanin, even upon iron limitation. While the Photosystem I activity in mutant K11 remained high under iron deficiency, the Photosystem II activity dropped severely with respect to wild-type. The DpsA content in wild-type was already fairly high under regular growth conditions and did not significantly increase under iron deficiency nor in the presence of 0.3 mM 2′2′-dipyridyl in iron-sufficient BG11 medium. Nevertheless, the absence of DpsA in K11 resulted in a significantly altered transcriptional/translational activity of genes known to be involved in adaptation to iron starvation. The amount of isiA/B transcript was about two-fold lower than in wild-type, resulting in a lower 77 K chlorophyll a fluorescence at 685 nm, implying a lower concentration of Photosystem I-IsiA supercomplexes. While in wild-type idiA, idiB, and irpA transcripts were highly up-regulated, hardly any were detectable in mutant K11 under iron limitation. The concentration of mapA transcript, however, was greatly increased in K11 compared to wild-type. Measurements of acridine yellow fluorescence with intact wild-type and K11 cells revealed that iron deficiency caused an increased contribution of cyclic electron transport to membrane energisation and ATP synthesis being in agreement with the formation of the Photosystem I-IsiA supercomplex. In addition, mutant K11 had a much higher respiratory activity compared to wild-type under iron limitation.

adaptation to iron deficiency DpsA IdiA IsiA linear and cyclic electron flow respiration Synechococcus sp. strain PCC 7942 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Almiron M, Link AJ, Furlong D and Kolter R (1992) A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev 6: 2646–2654Google Scholar
  2. Behrenfeld MJ and Kolber ZS (1999) Widespread iron limitation of phytoplankton in the south pacific ocean. Science 283: 840–843Google Scholar
  3. Bibby TS, Nield J and Barber J (2001a) Iron deficiency induces the formation of an antenna ring around trimeric Photosystem I in cyanobacteria. Nature 412: 743–745Google Scholar
  4. Bibby TS, Nield J and Barber J (2001b) Three-dimensional model and characterisation of the iron-stress induced CP43'-Photosystem I supercomplex isolated from the cyanobacterium Synechocystis PCC 6803. J Biol Chem 22: 22–30Google Scholar
  5. Boekema EJ, Hifney A, Yakushevska AE, Piotrowski M, Keegstra W, Berry S, Michel KP, Pistorius EK and Kruip J (2001) A giant chlorophyll–protein complex induced by iron deficiency in cyanobacteria. Nature 412: 745–748Google Scholar
  6. Boyer GL, Gilliam AH and Trick C (1987) Iron chelation and uptake. In: Fay P and van Baalen C (eds) The Cyanobacteria, pp 415–436. Elsevier, Amsterdam/New York/OxfordGoogle Scholar
  7. Burnap RL, Troyan T and Sherman LA (1993) The highly abundant chlorophyll–protein complex of iron-deficient Synechococcus sp. PCC 7942 (CP43') is encoded by the isiA gene. Plant Physiol 103: 893–902Google Scholar
  8. Dwivedi K, Sen A and Bullerjahn GS (1997) Expression and mutagenesis of the dpsA gene of Synechococcus sp. PCC 7942, encoding a DNA-binding protein involved in oxidative stress protection. FEMS Microbiol Lett 155: 85–91Google Scholar
  9. Escolar L, Perez-Martin J and de Lorenzo V (1999) Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181: 6223–6229Google Scholar
  10. Exss-Sonne P, Tölle J, Bader KP, Pistorius EK and Michel KP (2000) The IdiA protein of Synechococcus sp. PCC 7942 functions in protecting Photosystem II under oxidative stress. Photosynth Res 63: 145–157Google Scholar
  11. Falk S, Samson G, Bruce D, Huner NPA and Laudenbach DE (1995) Functional analysis of the iron-stress induced CP43 polypeptide of PS II in the cyanobacterium Synechococcus sp. PCC 7942. Photosynth Res 45: 51–60Google Scholar
  12. Ferreira F and Straus NA (1994) Iron deprivation in cyanobacteria. J Appl Phycol 6: 199–210Google Scholar
  13. Geider RJ and La Roche J (1994) The role of iron in phytoplankton photosynthesis, and the potential for iron-limitation of primary productivity in the sea. Photosynth Res 39: 275–301Google Scholar
  14. Ghassemian M and Straus NA (1996) Fur regulates the expression of iron-stress genes in the cyanobacterium Synechococcus sp. strain PCC 7942. Microbiology 142: 1469–1476Google Scholar
  15. Grimme LH and Boardman NK (1972) Photochemical activation of a particle fraction P1 obtained from the green alga Chlorella fusca. Biochem Biophys Res Commun 49: 1617–1623Google Scholar
  16. Grossman AR, Bhaya D and He Q (2001) Tracking the light environment by cyanobacteria and the dynamic nature of light harvesting. J Biol Chem 276: 11449–11452Google Scholar
  17. Guikema JA and Sherman LA (1983) Chlorophyll-protein organization of membranes from the cyanobacterium Anacystis nidulans. Arch Biochem Biophys 220: 155–166Google Scholar
  18. Helmann JD (1998) Metal cation regulation in gram-positive bacteria. In: Silver S and Walden W (eds) Metal Ions in Gene Regulation, pp 45–76. Thomson International Publishing, New YorkGoogle Scholar
  19. Herdman M, Castenholz RW, Iteman L, Waterbury JB, and Rippka R (2000) The Archae, cyanobacteria and deeply branching bacteria. In: Boone DR, Castenholz RW and Garrity GM(eds) Bergey's Manual of Systematic Bacteriology, p 776. Springer-Verlag, New YorkGoogle Scholar
  20. Hiyama T and Ke B (1972) Difference spectra and excitation coefficients of P700. Biochim Biophys Acta 267: 160–171Google Scholar
  21. Ivanov AG, Park YI, Miskiewicz E, Raven JA, Huner NP and Öquist G (2000) Iron stress restricts photosynthetic intersystem electron transport in Synechococcus sp. PCC 7942. FEBS Lett 485: 173–177Google Scholar
  22. Katoh H, Hagino N, Grossman AR and Ogawa T (2001) Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183: 2779–2784Google Scholar
  23. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685Google Scholar
  24. Laudenbach DE and Straus NA (1988) Characterization of a cyanobacterial iron stress-induced gene similar to psbC. J Bacteriol 170: 5018–5026Google Scholar
  25. Laudenbach DE, Reith ME and Straus NA (1988) Isolation, sequence analysis, and transcriptional studies of the flavodoxin gene from Anacystis nidulans R2. J Bacteriol 170: 258–265Google Scholar
  26. Mann NH (2000) Detecting the environment. In: Whitton BA and Potts M (eds) The Ecology of Cyanobacteria, pp 367–395. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  27. Marjorette M, Pena O and Bullerjahn GS (1995) The DpsA protein of Synechococcus sp. strain PCC 7942 is a DNA-binding hemoprotein. J Biol Chem 270: 22478–22782Google Scholar
  28. Martinez A and Kolter R (1997) Protection of DNA during oxidative stress by the non-specific DNA-binding protein Dps. J Bacteriol 179: 5188–5194Google Scholar
  29. Matin A (1991) The molecular basis of carbon-starvation-induced general resistance in Escherichia coli. Mol Microbiol 5: 3–10Google Scholar
  30. Michel KP and Pistorius EK (1992) Isolation of a Photosystem II associated 36 kDa polypeptide and an iron stress 34 kDa polypeptide from thylakoid membranes of the cyanobacterium Synechococcus PCC 6301 grown under mild iron deficiency. Z Naturforsch 47c: 867–874Google Scholar
  31. Michel KP, Thole HH and Pistorius EK (1996) IdiA, a 34 kDa protein in the cyanobacteria Synechococcus sp. strains PCC 6301and PCC 7942, is required for growth under iron and manganese limitations. Microbiology 142: 2635–2645Google Scholar
  32. Michel KP, Exss-Sonne P, Scholten-Beck G, Kahmann U, Ruppel HG and Pistorius EK (1998) Immunocytochemical localization of IdiA, a protein expressed under iron or manganese limitation in the mesophilic cyanobacterium Synechococcus PCC 6301 and the thermophilic cyanobacterium Synechococcus elongatus. Planta 205: 73–81Google Scholar
  33. Michel KP, Krüger F, Pühler A and Pistorius EK (1999) Molecular characterization of idiA and adjacent genes in the cyanobacteria Synechococcus sp. strains PCC 6301 and PCC 7942. Microbiology 145: 1473–1484Google Scholar
  34. Michel KP, Pistorius EK and Golden SS (2001) Unusual regulatory elements for iron deficiency induction of the idiA gene of Synechococcus elongatus PCC 7942. J Bacteriol 183: 5015–5024Google Scholar
  35. Mullineaux CW and Allen F (1990) State 1-State 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between Photosystem I and II. Photosynth Res 23: 297–311Google Scholar
  36. Park YI, Sandström S, Gustafsson P and Öquist G (1999) Expression of the isiA gene is essential for the survival of the cyanobacterium Synechococcus sp. PCC 7942 by protecting Photosystem II from excess light under iron limitation. Mol Microbiol 32: 123–129Google Scholar
  37. Pena MM and Bullerjahn GS (1995) The DpsA protein of Synechococcus sp. strain PCC 7942 is a DNA-binding hemoprotein. Linkage of the Dps and bacterioferritin protein families. J Biol Chem 270: 22478–22482Google Scholar
  38. Pena MM, Burkhart W and Bullerjahn GS (1995) Purification and characterization of a Synechococcus sp. strain PCC 7942polypeptide structurally similar to the stress-induced Dps/PexB protein of Escherichia coli. Arch Microbiol 163: 337–344Google Scholar
  39. Reddy KJ, Bullerjahn GS, Sherman DM and Sherman LA (1988) Cloning, nucleotide sequence, and mutagenesis of a gene (irpA) involved in iron-deficient growth of the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 170: 4466–4476Google Scholar
  40. Reddy KJ, Webb R and Sherman LA (1990) Bacterial RNA isolation with one hour centrifugation in a table-top ultracentrifuge. BioTechniques 8: 250–251Google Scholar
  41. Riethman HC and Sherman D (1988a) Immunological characterization of iron-regulated membrane proteins in the cyanobacterium Anacystis nidulans R2. Plant Physiol 88: 497–505Google Scholar
  42. Riethman HC and Sherman LA (1988b) Regulation of cyanobacterial pigment-protein composition and organization by environmental factors. Photosynth Res 18: 133–161Google Scholar
  43. Schaegger H and von Jagow G (1987) Tricine-sodium dodecylsulphate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166: 368–379Google Scholar
  44. Sen A, Dwivedi K, Rice KA and Bullerjahn GS (2000) Growth phase and metal-dependent regulation of the dpsA gene in Synechococcus sp. strain PCC 7942. Arch Microbiol 173: 352–357Google Scholar
  45. Sherman DM and Sherman LA (1983) Effect of iron deficiency and iron restoration on ultrastructure of Anacystis nidulans. J Bacteriol 156: 393–401Google Scholar
  46. Singh AK and Sherman LA (2000) Identification of iron-responsive, differential gene expression in the cyanobacterium Synechocystis sp. strain PCC 6803 with a customized amplification library. J Bacteriol 182: 3536–3543Google Scholar
  47. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provencano MD, Fujimoto EK, Goecke NM, Olson BJ and Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150: 368–379Google Scholar
  48. Straus NA (1994) Iron deprivation: physiology and gene regulation. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 731–750. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  49. Tandeau de Marsac N and Houmard J (1988) Complementary chromatic adaptation: Physiological conditions and action spectra. In: Packer L and Glazer AN (eds) Methods Enzymol, pp 318–328. Academic Press, San Diego, CaliforniaGoogle Scholar
  50. Tandeau de Marsac N and Houmard J (1993) Adaptation of cyanobacteria to environmental stimuli: new steps towards molecular mechanisms. FEMS Microbiol Rev 104: 119–190Google Scholar
  51. Teuber M, Rögner M and Berry S (2001) Fluorescent probes for non-invasive bioenergetic studies of whole cyanobacterial cells. Biochim Biophys Acta 1506: 31–46Google Scholar
  52. van Thor JJ, Mullineaux CW, Matthijs HCP and Hellingwerf KJ (1998) Light-harvesting and state transitions in cyanobacteria. Bot Acta 111: 430–443Google Scholar
  53. Webb EA, Moffett JW and Waterbury JB (2001) Iron stress in open-ocean cyanobacteria (Synechococcus, Trichodesmium, and Crocosphaera spp.): identification of the IdiA protein. Appl Environ Microbiol 67: 5444–5452Google Scholar
  54. Webb R, Troyan T, Sherman D and Sherman LA (1994) MapA, an iron-regulated, cytoplasmic membrane protein in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 176: 4906–4913Google Scholar
  55. Wenk SO and Kruip J (2000) Novel, rapid purification of the membrane protein Photosystem I by high-performance liquid chromatography on porous materials. J Chromatogr B Biomed Sci Appl 737: 131–142Google Scholar
  56. Wilhelm SWand Trick CG (1994) Iron-limited growth of cyanobacteria: multiple siderophore production is a common response. Limnol Oceanogr 39: 1979–1984Google Scholar
  57. Wolf SG, Frenkiel D, Arad T, Finkel SE, Kolter R and Minsky A (1999) DNA protection by stress-induced biocrystallization. Nature 400: 83–85Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Klaus-Peter Michel
    • 1
  • Stephan Berry
    • 2
  • Awatief Hifney
    • 1
  • Jochen Kruip
    • 2
  • Elfriede K. Pistorius
    • 1
  1. 1.Biologie VIII: ZellphysiologieUniversität BielefeldBielefeldGermany
  2. 2.Lehrstuhl für Biochemie der Pflanzen, Ruhr-Universität BochumBochumGermany

Personalised recommendations