Skip to main content
Log in

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

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • 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: 2646–2654

    Google Scholar 

  • Behrenfeld MJ and Kolber ZS (1999) Widespread iron limitation of phytoplankton in the south pacific ocean. Science 283: 840–843

    Google Scholar 

  • 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: 743–745

    Google Scholar 

  • 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: 22–30

    Google Scholar 

  • 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: 745–748

    Google Scholar 

  • 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/Oxford

    Google Scholar 

  • 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: 893–902

    Google Scholar 

  • 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: 85–91

    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

    Google Scholar 

  • 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: 145–157

    Google Scholar 

  • 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: 51–60

    Google Scholar 

  • Ferreira F and Straus NA (1994) Iron deprivation in cyanobacteria. J Appl Phycol 6: 199–210

    Google Scholar 

  • 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: 275–301

    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

    Google Scholar 

  • 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: 1617–1623

    Google Scholar 

  • 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: 11449–11452

    Google Scholar 

  • Guikema JA and Sherman LA (1983) Chlorophyll-protein organization of membranes from the cyanobacterium Anacystis nidulans. Arch Biochem Biophys 220: 155–166

    Google Scholar 

  • 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 York

    Google Scholar 

  • 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 York

    Google Scholar 

  • Hiyama T and Ke B (1972) Difference spectra and excitation coefficients of P700. Biochim Biophys Acta 267: 160–171

    Google Scholar 

  • 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: 173–177

    Google Scholar 

  • 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: 2779–2784

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685

    Google Scholar 

  • Laudenbach DE and Straus NA (1988) Characterization of a cyanobacterial iron stress-induced gene similar to psbC. J Bacteriol 170: 5018–5026

    Google Scholar 

  • 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: 258–265

    Google Scholar 

  • 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 Netherlands

    Google Scholar 

  • 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: 22478–22782

    Google Scholar 

  • Martinez A and Kolter R (1997) Protection of DNA during oxidative stress by the non-specific DNA-binding protein Dps. J Bacteriol 179: 5188–5194

    Google Scholar 

  • Matin A (1991) The molecular basis of carbon-starvation-induced general resistance in Escherichia coli. Mol Microbiol 5: 3–10

    Google Scholar 

  • 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: 867–874

    Google Scholar 

  • 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: 2635–2645

    Google Scholar 

  • 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: 73–81

    Google Scholar 

  • 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: 1473–1484

    Google Scholar 

  • 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: 5015–5024

    Google Scholar 

  • 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: 297–311

    Google Scholar 

  • 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: 123–129

    Google Scholar 

  • 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: 22478–22482

    Google Scholar 

  • 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: 337–344

    Google Scholar 

  • 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: 4466–4476

    Google Scholar 

  • Reddy KJ, Webb R and Sherman LA (1990) Bacterial RNA isolation with one hour centrifugation in a table-top ultracentrifuge. BioTechniques 8: 250–251

    Google Scholar 

  • Riethman HC and Sherman D (1988a) Immunological characterization of iron-regulated membrane proteins in the cyanobacterium Anacystis nidulans R2. Plant Physiol 88: 497–505

    Google Scholar 

  • Riethman HC and Sherman LA (1988b) Regulation of cyanobacterial pigment-protein composition and organization by environmental factors. Photosynth Res 18: 133–161

    Google Scholar 

  • 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: 368–379

    Google Scholar 

  • 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: 352–357

    Google Scholar 

  • Sherman DM and Sherman LA (1983) Effect of iron deficiency and iron restoration on ultrastructure of Anacystis nidulans. J Bacteriol 156: 393–401

    Google Scholar 

  • 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: 3536–3543

    Google Scholar 

  • 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: 368–379

    Google Scholar 

  • 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 Netherlands

    Google Scholar 

  • 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, California

    Google Scholar 

  • Tandeau de Marsac N and Houmard J (1993) Adaptation of cyanobacteria to environmental stimuli: new steps towards molecular mechanisms. FEMS Microbiol Rev 104: 119–190

    Google Scholar 

  • Teuber M, Rögner M and Berry S (2001) Fluorescent probes for non-invasive bioenergetic studies of whole cyanobacterial cells. Biochim Biophys Acta 1506: 31–46

    Google Scholar 

  • van Thor JJ, Mullineaux CW, Matthijs HCP and Hellingwerf KJ (1998) Light-harvesting and state transitions in cyanobacteria. Bot Acta 111: 430–443

    Google Scholar 

  • 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: 5444–5452

    Google Scholar 

  • 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: 4906–4913

    Google Scholar 

  • 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: 131–142

    Google Scholar 

  • Wilhelm SWand Trick CG (1994) Iron-limited growth of cyanobacteria: multiple siderophore production is a common response. Limnol Oceanogr 39: 1979–1984

    Google Scholar 

  • Wolf SG, Frenkiel D, Arad T, Finkel SE, Kolter R and Minsky A (1999) DNA protection by stress-induced biocrystallization. Nature 400: 83–85

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elfriede K. Pistorius.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Michel, KP., Berry, S., Hifney, A. et al. Adaptation to iron deficiency: a comparison between the cyanobacterium Synechococcus elongatus PCC 7942 wild-type and a DpsA-free mutant. Photosynthesis Research 75, 71–84 (2003). https://doi.org/10.1023/A:1022459919040

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022459919040

Navigation