Skip to main content
Log in

Reflections on the function of IsiA, a cyanobacterial stress-inducible, Chl-binding protein

  • Research Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The isiA gene encodes a protein that is similar to the Photosystem II chlorophyll-binding protein CP43, but lacks the entire large lumenal loop of over 100 amino acids. What is the function of this IsiA protein? Research on IsiA has traveled a long and interesting path since it was first discovered by its large accumulation during growth under iron-limited conditions. What appeared to be a simple on–off switch for isiA based on iron concentration has developed into a much richer and more intriguing set of possibilities that involve its expression and function. We provide an overview of isiA transcriptional regulation by many environmental factors and its proposed functions. We also describe the response to oxidative stress by cells that lack the IsiA protein. It is now clear that isiA expression can be de-repressed in the presence of normal iron levels and that the regulatory mechanisms can be linked to the inter-relationship between iron homeostasis and oxidative stress. The de facto transcriptional control of isiA expression has expanded to include regulation at both the transcriptional and post-transcriptional levels.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ardelean I, Matthijs HC, Havaux M, Joset F, Jeanjean R (2002) Unexpected changes in photosystem I function in a cytochrome c6-deficient mutant of the cyanobacterium Synechocystis PCC 6803. FEMS Microbiol Lett 213:113–119

    Article  CAS  PubMed  Google Scholar 

  • Aspinwall CL, Duncan J, Bibby T, Mullineaux CW, Barber J (2004) The trimeric organisation of photosystem I is not necessary for the iron-stress induced CP43’ protein to functionally associate with this reaction centre. FEBS Lett 574:126–130

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bhaya D, Bianco NR, Bryant D, Grossman A (2000) Type IV pilus biogenesis and motility in the cyanobacterium Synechocystis sp. PCC 6803. Mol Microbiol 37:941–951

    Article  CAS  PubMed  Google Scholar 

  • Bhaya D, Takahashi A, Grossman AR (2001) Light regulation of type IV pilus-dependent motility by chemosensor-like elements in Synechocystis PCC6803. Proc Natl Acad Sci USA 98:7540–7545

    Article  CAS  PubMed  Google Scholar 

  • Bibby TS, Nield J, Barber J (2001) Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412:743–745

    Article  CAS  PubMed  Google Scholar 

  • Boekema EJ, Hifney A, Yakushevska AE, Piotrowski M, Keegstra W, Berry S, Michel KP, Pistorius EK, Kruip J (2001) A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria. Nature 412:745–748

    Article  CAS  PubMed  Google Scholar 

  • Bricker TM, Frankel LK (2002) The structure and function of CP47 and CP43 in Photosystem II. Photosynth Res 72:131–146

    Article  CAS  PubMed  Google Scholar 

  • Burnap RL, Troyan T, Sherman LA (1993) The highly abundant chlorophyll-protein complex of iron-deficient Synechococcus sp. PCC7942 (CP43’) is encoded by the isiA gene. Plant Physiol 103:893–902

    Article  CAS  PubMed  Google Scholar 

  • Cho F, Govindjee (1970a) Low-temperature (4–77°K) spectroscopy of Chlorella; temperature dependence of energy transfer efficiency. Biochim Biophys Acta 216:139–150

    Article  CAS  Google Scholar 

  • Cho F, Govindjee (1970b) Low-temperature (4–77°K) spectroscopy of Anacystis: temperature dependence of energy transfer efficiency. Biochim Biophys Acta 216:151–161

    Article  CAS  Google Scholar 

  • Cho F, Govindjee (1970c) Flourescence spectra of Chlorella in the 295-77°K range. Biochim Biophys Acta 205:371–378

    Article  CAS  Google Scholar 

  • Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54:93–107

    Article  CAS  PubMed  Google Scholar 

  • Dühring U, Axmann IM, Hess WR, Wilde A (2006) An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proc Natl Acad Sci USA 103:7054–7058

    Article  PubMed  CAS  Google Scholar 

  • Falk S, Samson G, Bruce D, Huner NP (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

    Article  CAS  Google Scholar 

  • Figge RM, Cassier-Chauvat C, Chauvat F, Cerff R (2000) The carbon metabolism-controlled Synechocystis gap2 gene harbours a conserved enhancer element and a Gram-positive-like -16 promoter box retained in some chloroplast genes. Mol Microbiol 36:44–54

    Article  CAS  PubMed  Google Scholar 

  • Foster JS, Singh AK, Rothschild LJ, Sherman LA (2006) Growth-phase dependent differential gene expression in Synechocystis sp. strain PCC 6803 and regulation by a goup two sigma factor. Dig Arch Microbiol DOI 10. 1007/s0020300601936

  • Frausto da Silva JJR, Williams RJP (2001) The biological chemistry of the elements: the inorganic chemistry of life. Oxford University Press, Oxford, UK

    Google Scholar 

  • Geider RJ, 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

    Article  CAS  Google Scholar 

  • Geiss U, Vinnemeier J, Kunert A, Lindner I, Gemmer B, Lorenz M, Hagemann M, Schoor A (2001a) Detection of the isiA gene across cyanobacterial strains: potential for probing iron deficiency. Appl Environ Microbiol 67:5247–5253

    Article  CAS  Google Scholar 

  • Geiss U, Vinnemeier J, Schoor A, Hagemann M (2001b) The iron-regulated isiA gene of Fischerella muscicola strain PCC 73103 is linked to a likewise regulated gene encoding a Pcb-like chlorophyll-binding protein. FEMS Microbiol Lett 197:123–129

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gorby YA, Yanina S, McLean S, Rosso KM, Moyles D, Dohnalkova A, Beveridge TJ, Chang IS, Kim BH, Kim KS, Culley DE, Reed SB, Romine MF, Saffarini DA, Hill EA, Liang S, Elias DA, Kennedy DW, Pinchuk G, Watanabe K, Ishii S, Logan B, Nealson KH, Fredrickson JK (2006) Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorgansisms. Proc Natl Acad Sci USA 103:11358–11363

    Article  CAS  PubMed  Google Scholar 

  • Govindjee, Papageorgiou G (1971) Chlorophyll fluorescence and photosynthesis fluorescence transients. In: Giese AC (ed) Photophysiology,vol 6. Academic Press, Inc., New York London, pp 1–41

    Google Scholar 

  • Govindjee, Papageorgiou G, Rabinowitch E (1967) Chlorophyll fluorescence and photosynthesis. In: Guibault GG (ed) Fluorescence: theory, instrumentation and practice. Dekker, New York, pp 511–564

    Google Scholar 

  • Green BR (2003) The evolution of light-harvesting antennas. In: Green BR (ed) Light-harvesting antennas in photosynthesis. Kluwer Academic Publishers, Netherlands, pp 129–168

    Google Scholar 

  • Guerinot ML, Yi Y (1994) Iron: nutritious, noxious, and not readily available. Plant Physiol 104:815–820

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Guikema JA, Sherman LA (1984) Influence of iron deprivation on the membrane composition of Anacystis nidulans. Plant Physiol 74:90–95

    CAS  PubMed  Google Scholar 

  • Havaux M, Guedeney G, Hagemann M, Yeremenko N, Matthijs HC, Jeanjean R (2005) The chlorophyll-binding protein IsiA is inducible by high light and protects the cyanobacterium Synechocystis PCC6803 from photooxidative stress. FEBS Lett 579:2289–2293

    Article  CAS  PubMed  Google Scholar 

  • He Q, Vermaas W (1999) Genetic deletion of proteins resembling Type IV pilins in Synechocystis sp. PCC 6803: their role in binding or transfer of newly synthesized chlorophyll. Plant Mol Biol 39:1175–1188

    Article  CAS  PubMed  Google Scholar 

  • Huang F, Parmryd I, Nilsson F, Persson AL, Pakrasi HB, Andersson B, Norling B (2002) Proteomics of Synechocystis sp. strain PCC 6803: identification of plasma membrane proteins. Mol Cell Proteomics 1:956–966

    Article  CAS  PubMed  Google Scholar 

  • Jeanjean R, Zuther E, Yeremenko N, Havaux M, Matthijs HC, Hagemann M (2003) A photosystem 1 psaFJ-null mutant of the cyanobacterium Synechocystis PCC 6803 expresses the isiAB operon under iron replete conditions. FEBS Lett 549:52–56

    Article  CAS  PubMed  Google Scholar 

  • Keren N, Liberton M, Pakrasi HB (2005) Photochemical competence of assembled photosystem II core complex in cyanobacterial plasma membrane. J Biol Chem 280:6548–6553

    Article  CAS  PubMed  Google Scholar 

  • Kouril R, Arteni AA, Lax J, Yeremenko N, D’Haene S, Rögner M, Matthijs HC, Dekker JP, Boekema EJ (2005) Structure and functional role of supercomplexes of IsiA and Photosystem I in cyanobacterial photosynthesis. FEBS Lett 579:3253–3257

    Article  CAS  PubMed  Google Scholar 

  • Kunert A, Vinnemeier J, Erdmann N, Hagemann M (2003) Repression by Fur is not the main mechanism controlling the iron-inducible isiAB operon in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett 227:255–262

    Article  CAS  PubMed  Google Scholar 

  • Kutzki C, Masepohl B, Bohme H (1998) The isiB gene encoding flavodoxin is not essential for photoautotrophic iron limited growth of the cyanobacterium Synechocystis sp. strain PCC 6803. FEMS Microbiol Lett 160:231–235

    Article  CAS  PubMed  Google Scholar 

  • La Roche J, van der Staay GW, Partensky F, Ducret A, Aebersold R, Li R, Golden SS, Hiller RG, Wrench PM, Larkum AW, Green BR (1996) Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins. Proc Natl Acad Sci USA 93:15244–15248

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Laudenbach DE, Reith ME, Straus NA (1988) Isolation, sequence analysis, and transcriptional studies of the flavodoxin gene from Anacystis nidulans R2. J Bacteriol 170:258–265

    CAS  PubMed  Google Scholar 

  • Leonhardt K, Straus NA (1994) Photosystem II genes isiA, psbDI and psbC in Anabaena sp. PCC 7120: cloning, sequencing and the transcriptional regulation in iron-stressed and iron-repleted cells. Plant Mol Biol 24:63–73

    Article  CAS  PubMed  Google Scholar 

  • Li H, Singh AK, McIntyre LM, Sherman LA (2004) Differential gene expression in response to hydrogen peroxide and the putative PerR regulon of Synechocystis sp. strain PCC 6803. J Bacteriol 186:3331–3345

    Article  CAS  PubMed  Google Scholar 

  • Marraccini P, Bulteau S, Cassier-Chauvat C, Mermet-Bouvier P, Chauvat F (1993) A conjugative plasmid vector for promoter analysis in several cyanobacteria of the genera Synechococcus and Synechocystis. Plant Mol Biol 23:905–909

    Article  CAS  PubMed  Google Scholar 

  • Martin JH, Fitzwater SE (1988) Iron deficiency limits phytoplankton growth in the north-east Pacific subartic. Nature 331:341–343

    Article  CAS  Google Scholar 

  • Martin JH, Coale KH, Johnson KS, Fitzwater SE, Gordon RM, Tanner SJ, Hunter CN, Elrod VA, Nowicki JL, Coley TL, Barber RT, Lindley S, Watson AJ, Van Scoy K, Law CS, Liddicoat MI, Ling R, Stanton T, Stockel J, Collins C, Anderson A, Bidigare R, Ondrusek M, Latasa M, Millero FJ, Lee K, Yao W, Zhang JZ, Friederich G, Sakamoto C, Chavez F, Buck K, Kolber ZS, Greene R, Falkowksi P, Chrisholm SW, Hoge F, Swift R, Yungel J, Turner S, Nightingale P, Hatton A, Liss P, Tindale NW (1994) Testing the iron hypothesis in the ecosystem of the equatorial Pacific Ocean. Nature 371:123–129

    Article  CAS  Google Scholar 

  • Nunn D (1999) Bacterial type II protein export and pilus biogenesis: more than just homologies? Trend Cell Biol 9:402–408

    Article  CAS  Google Scholar 

  • Öquist G (1971) Changes in pigment compositon and photosynthesis induced by iron deficiency in the blue-green algae Anacystis nidulas. Physiol Plant 25:188–191

    Article  Google Scholar 

  • Öquist G (1974a) Iron deficiency in the blue-green algae Anacystis nidulans. Physiol Plant 30:30–37

    Article  Google Scholar 

  • Öquist G (1974b) Iron deficiency in the blue-green algae Anacystis nidulans: fluorescence and absorption spectra recorded at 77 K. Physiol Plant 31:55–58

    Article  Google Scholar 

  • Pakrasi HB, Riethman HC, Sherman LA (1985a) Membrane development in the cyanobacterium Anacystis nidulans during recovery from iron starvation. Plant Physiol 79:290–295

    CAS  Google Scholar 

  • Pakrasi HB, Riethman HC, Sherman LA (1985b) Organization of pigment proteins in the photosystem II complex of the cyanobacterium Anacystis nidulans R2. Proc Natl Acad Sci USA 82:6903–6907

    Article  CAS  Google Scholar 

  • Park YI, Sandström S, Gustafsson P, 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

    Article  CAS  PubMed  Google Scholar 

  • Postier BL, Wang HL, Singh A, Impson L, Andrews HL, Klahn J, Li H, Risinger G, Pesta D, Deyholos M, Galbraith DW, Sherman LA, Burnap RL (2003) The construction and use of bacterial DNA microarrays based on an optimized two-stage PCR strategy. BMC Genomics 4:23

    Article  PubMed  Google Scholar 

  • Ratledge C, Dover LG (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54:881–941

    Article  CAS  PubMed  Google Scholar 

  • Regelsberger G, Jakopitsch C, Plasser L, Schwaiger H, Furtmuller PG, Peschek GA, Zamocky M, Obinger C (2002) Occurence and biochemistry of hydroperoxidases in oxygenic phototrophic prokaryotes (cyanobacteria). Plant Physiol Biochem. 40:479–490

    Article  CAS  Google Scholar 

  • Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rögner M, Chisholm DA, Diner BA (1991) Site-directed mutagenesis of the psbC gene of photosystem II: isolation and functional characterization of CP43-less photosystem II core complexes. Biochemistry 30:5387–5395

    Article  PubMed  Google Scholar 

  • Sandström S, Park YI, Öquist G, Gustafsson P (2001) CP43’, the isiA gene product, functions as an excitation energy dissipator in the cyanobacterium Synechococcus sp. PCC 7942. Photochem Photobiol 74:431–437

    Article  PubMed  Google Scholar 

  • Sandström S, Ivanov AG, Park YI, Öquist G, Gustafsson P (2002) Iron stress responses in the cyanobacterium Synechococcus sp. PCC7942. Physiol Plant 116:255–263

    Article  PubMed  Google Scholar 

  • Sarcina M, Mullineaux CW (2004) Mobility of the IsiA chlorophyll-binding protein in cyanobacterial thylakoid membranes. J Biol Chem 279:36514–36518

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Singh AK, Sherman LA (2006) Iron-independent dynamics of IsiA production during the transition to stationary phase in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett 256:159–164

    Article  CAS  PubMed  Google Scholar 

  • Singh AK, McIntyre LM, Sherman LA (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

    Article  CAS  PubMed  Google Scholar 

  • Singh AK, Li H, Sherman LA (2004) Microarray analysis and redox control of gene expression in the cyanobacterium Synechocystis sp. PCC 6803. Physiol Plant 120:27–35

    Article  CAS  PubMed  Google Scholar 

  • Singh AK, Li H, Bono L, Sherman LA (2005) Novel adaptive responses revealed by transcription profiling of a Synechocystis sp. PCC 6803 ΔisiA mutant in the presence and absence of hydrogen peroxide. Photosynth Res 84:65–70

    Article  CAS  PubMed  Google Scholar 

  • Stork T, Michel K-P, Pistorius EK, Dietz K-J (2005) Bioinformatic analysis of the genomes of the cyanobacteria Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942 for the presence of peroxiredoxins and their transcript regulation under stress. J Exp Bot 56:3193–3206

    Article  CAS  PubMed  Google Scholar 

  • Straus NA (1994) Iron deprivation: physiology and gene regulation. In: Bryant DA (ed) The molecular biology of cyanobacteria, advances in photosynthesis and respiration, vol 1. Kluwer Academic Publishers, Dordrect, The Netherlands, pp 731–750

    Google Scholar 

  • Vinnemeier J, Hagemann M (1999) Identification of salt-regulated genes in the genome of the cyanobacterium Synechocystis sp. strain PCC 6803 by subtractive RNA hybridization. Arch Microbiol 172:377–386

    Article  CAS  PubMed  Google Scholar 

  • Vinnemeier J, Kunert A, Hagemann M (1998) Transcriptional analysis of the isiAB operon in salt-stressed cells of the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett 169:323–330

    Article  CAS  PubMed  Google Scholar 

  • Yeremenko N, Kouril R, Ihalainen JA, D’Haene S, van Oosterwijk N, Andrizhiyevskaya EG, Keegstra W, Dekker HL, Hagemann M, Boekema EJ, Matthijs HC, Dekker JP (2004) Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria. Biochemistry 43:10308–10313

    Article  CAS  PubMed  Google Scholar 

  • Zak E, Norling B, Maitra R, Huang F, Andersson B, Pakrasi HB (2001) The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes. Proc Natl Acad Sci USA 98:13443–13448

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Louis A. Sherman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Singh, A.K., Sherman, L.A. Reflections on the function of IsiA, a cyanobacterial stress-inducible, Chl-binding protein. Photosynth Res 93, 17–25 (2007). https://doi.org/10.1007/s11120-007-9151-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-007-9151-7

Keywords

Navigation