Skip to main content
SpringerLink
Log in

Iron Deficiency in Cyanobacteria

  • Chapter
  • First Online:
Microbial Photosynthesis

  • 1137 Accesses

Abstract

Iron is very important for photosynthetic microorganisms, including cyanobacteria, because the electron transport system of photosynthesis is highly iron-dependent. However, iron limitation is frequently occurred in natural habitats, limiting the photosynthetic activity and biomass production of cyanobacteria and other photosynthetic microorganisms. Cyanobacteria have evolved various strategies to adapt the conditions of iron deficiency. In this chapter, we will review the iron stress responses of cyanobacteria, talking about both the physiological changes and the molecular mechanisms.

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

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Achilles, K. M., Church, T. M., Wilhelm, S. W., et al. (2003). Bioavailability of iron to Trichodesmium colonies in the western subtropical Atlantic Ocean. Limnology and Oceanography, 48, 2250–2255.

    CAS  Google Scholar 

  • Allen, J. F., & Vermaas, W. F. J. (2010). Evolution of photosynthesis. In eLS. Chichester: Wiley.

    Google Scholar 

  • Andrews, S. C., Robinson, A. K., & Rodríguez-Quiñones, F. (2003). Bacterial iron homeostasis. FEMS Microbiology Reviews, 27, 215–237.

    CAS  PubMed  Google Scholar 

  • Andrizhiyevskaya, E. G., Schwabe, T. M., Germano, M., et al. (2002). Spectroscopic properties of PSI-IsiA supercomplexes from the cyanobacterium Synechococcus PCC 7942. Biochimica et Biophysica Acta-Bioenergetics, 1556, 265–272.

    CAS  Google Scholar 

  • Andrizhiyevskaya, E. G., Frolov, D., van Grondelle, R., et al. (2004). Energy transfer and trapping in the photosystem I complex of Synechococcus PCC 7942 and in its supercomplex with IsiA. Biochimica et Biophysica Acta, 1656, 104–113.

    CAS  PubMed  Google Scholar 

  • Arnistroug, J. E., & Van Baalen, C. (1979). Iron transport in microalgae: The isolation and biochemical’activity of a hydroxamate siderophore from the blue-green’ alga, Agmenellum quadruplicatum. Journal of General Microbiology, 111, 253–262.

    Google Scholar 

  • Aspinwall, C. L., Duncan, J., Bibby, T., et al. (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 Letters, 574, 126–130.

    CAS  PubMed  Google Scholar 

  • Babykin, M. M., Obando, S. T. A., & Zinchenko, V. V. (2018). TonB-dependent utilization of dihydroxamate xenosiderophores in Synechocystis sp. PCC 6803. Current Microbiology, 75, 117–123.

    CAS  PubMed  Google Scholar 

  • Badarau, A., Firbank, S. J., Waldron, K. J., et al. (2008). FutA2 is a ferric binding protein from Synechocystis PCC 6803. The Journal of Biological Chemistry, 283, 12520–12527.

    CAS  PubMed  Google Scholar 

  • Bagg, A., & Neilands, J. B. (1987). Molecular mechanism of regulation of siderophore-mediated iron assimilation. Microbiological Reviews, 51, 509–518.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baniulis, D., Yamashita, E., Zhang, H., et al. (2008). Structure–function of the cytochrome b6f complex. Photochemistry and Photobiology, 84, 1349–1358.

    CAS  PubMed  Google Scholar 

  • Behrenfeld, M. J., & Kolber, Z. S. (1999). Widespread iron limitation of phytoplankton in the South Pacific Ocean. Science, 283, 840–843.

    CAS  PubMed  Google Scholar 

  • Behrenfeld, M. J., Bale, A. J., Kolber, Z. S., et al. (1996). Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial pacific ocean. Nature, 383, 508–511.

    CAS  Google Scholar 

  • Bekker, A., Holland, H. D., Wang, P. L., et al. (2004). Dating the rise of atmospheric oxygen. Nature, 427, 117–120.

    CAS  PubMed  Google Scholar 

  • Bellenger, J. P., Wichard, T., Xu, Y., & Kraepiel, A. M. L. (2011). Essential metals for nitrogen fixation in a free-living N2-fixing bacterium: Chelation, homeostasis and high use efficiency. Environmental Microbiology, 13, 1395–1411.

    CAS  PubMed  Google Scholar 

  • Bes, M. T., Herna’ndez, J. A., Peleato, M. L., et al. (2001). Cloning, overexpression and interaction of recombinant Fur from the cyanobacterium Anabaena PCC 7119 with isiB and its own promoter. FEMS Microbiology Letters, 194(2), 187–192.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Bibby, T. S., Nield, J., & Barber, J. (2001b). Three-dimensional model and characterization of the iron stress-induced CP43’-photosystem I supercomplex isolated from the cyanobacterium Synechocystis PCC 6803. The Journal of Biological Chemistry, 276, 43246–43252.

    CAS  PubMed  Google Scholar 

  • Boekema, E. J., Hifney, A., Yakushevska, A. E., et al. (2001). A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria. Nature, 412, 745–748.

    CAS  PubMed  Google Scholar 

  • Boyd, P. W., & Ellwood, M. J. (2010). The biogeochemical cycle of iron in the ocean. Nature Geoscience, 3, 675–682.

    CAS  Google Scholar 

  • Boyer, G. L., Gillam, A. H., & Trick, C. (1987). Iron chelation and uptake. In P. Fay & C. Van Baalen (Eds.), The cyanobacteria (pp. 415–436). Amsterdam: Elsevier Scientific Publishers.

    Google Scholar 

  • Brand, L. E. (1991). Minimum iron requirements of marine phytoplankton and the implications for the biogeochemical control of new production. Limnology and Oceanography, 36, 1756–1771.

    Google Scholar 

  • Brand, L. E., Sunda, W. G., & Guillard, R. R. L. (1983). Limitation of marine phytoplankton reproductive rates by zinc, manganese, and iron. Limnology and Oceanography, 28, 1182–1198.

    CAS  Google Scholar 

  • Brandt, A. M., Raksajit, W., Mulo, P., et al. (2009). Transcriptional regulation and structural modeling of the FutC subunit of an ABC-type iron transporter in Synechocystis sp. strain PCC 6803. Archives of Microbiology, 191, 561–570.

    CAS  PubMed  Google Scholar 

  • Braun, V., Schaffer, S., Hantke, K., et al. (1990). Regulation of gene expression by iron. In G. Hauska & R. Thauer (Eds.), The molecular basis of bacterial metabolism (pp. 35–51). Berlin: VCH-Verlagsgesellschaft.

    Google Scholar 

  • Bricker, T. M., & Frankel, L. K. (2002). The structure and function of CP47 and CP43 in photosystem II. Photosynthesis Research, 72, 131–146.

    CAS  PubMed  Google Scholar 

  • Burnap, R. L., Troyan, T., & Sherman, L. A. (1993). The highly abundant chlorophyll-protein complex of iron-deficient Synechococcus sp. PCC7942 (CP43’) is encoded by the isiA gene. Plant Physiology, 103(3), 893–902.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carr, N. G., & Mann, N. H. (1994). The oceanic cyanobacterial picoplankton. In D. A. Bryant (Ed.), The molecular biology of cyanobacteria (Advances in photosynthesis) (Vol. 1, pp. 27–48). Dordrecht: Springer.

    Google Scholar 

  • Chauhan, D., Folea, I. M., Jolley, C. C., et al. (2011). A novel photosynthetic strategy for adaptation to low-iron aquatic environments. Biochemistry, 50, 686–692.

    CAS  PubMed  Google Scholar 

  • Cheng, D., & He, Q. (2014). PfsR is a key regulator of iron homeostasis in Synechocystis PCC 6803. PLoS One, 9(7), e101743.

    PubMed  PubMed Central  Google Scholar 

  • Fraústo da Silva, J. J. R., & Williams, R. J. P. (2001). The biological chemistry of the elements: The inorganic chemistry of life. Oxford: Oxford University Press.

    Google Scholar 

  • Daddy, S., Zhan, J., Jantaro, S., et al. (2015). A novel high light-inducible carotenoid-binding protein complex in the thylakoid membranes of Synechocystis PCC 6803. Scientific Reports, 5, 9480.

    PubMed  PubMed Central  Google Scholar 

  • Drechsel, H., & Winkelmann, G. (1997). Iron chelation and siderophores. In G. Winkelmann & C. J. Carrano (Eds.), Transition metals in microbial metabolism (pp. 1–49). Amsterdam: Harwood Academic Publishers.

    Google Scholar 

  • Dühring, U., Axmann, I. M., Hess, W. R., et al. (2006). An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proceedings of the National Academy of Sciences of the United States of America, 103, 7054–7058.

    PubMed  PubMed Central  Google Scholar 

  • Eldridge, M., Trick, C., Alm, M., et al. (2004). Phytoplankton community response to a manipulation of bioavailable iron in HNLC waters of the subtropical Pacific Ocean. Aquatic Microbial Ecology, 35, 79–91.

    Google Scholar 

  • Ernst, J. F., Bennett, R. L., & Rothfield, L. I. (1978). Constitutive expression of the iron-enterochelin and ferrichrome uptake systems in a mutant strain of Salmonella typhimurium. Journal of Bacteriology, 135, 928–934.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Exss-Sonne, P. J., Toelle, K. P., Bader, E. K., et al. (2000). The IdiA protein of Synechococcus sp. PCC 7942 functions in protecting photosystem II under oxidative stress. Photosynthesis Research, 63, 145–157.

    CAS  PubMed  Google Scholar 

  • Falk, S., Samson, G., Bruce, D., et al. (1995). Functional analysis of the iron-stress induced CP43P polypeptide of PSII in the cyanobacterium Synechococcus sp. PCC 7942. Photosynthesis Research, 45, 51–60.

    CAS  PubMed  Google Scholar 

  • Falkowski, P. G., & Raven, J. A. (2007). Aquatic photosynthesis (2nd ed.). Princeton: Princeton University Press.

    Google Scholar 

  • Faraldo-Gomez, J. D., & Sansom, M. S. P. (2003). Acquisition of siderophores in gram-negative bacteria. Nature Reviews. Molecular Cell Biology, 4, 105–116.

    CAS  PubMed  Google Scholar 

  • Ferreira, F., & Straus, N. A. (1994). Iron deprivation in cyanobacteria. Journal of Applied Phycology, 6, 199–210.

    CAS  Google Scholar 

  • Fillat, M. F., Sandmann, G., & Gómez-Moreno, C. (1988). Flavodoxin from the nitrogen-fixing cyanobacterium Anabaena PCC 7119. Archives of Microbiology, 150, 160–164.

    CAS  Google Scholar 

  • Fillat, M. F., Edmondson, D. E., & Gomez-Moreno, C. (1990). Structural and chemical properties of a flavodoxin from Anabaena PCC 7119. Biochimica et Biophysica Acta, 1040(2), 301–307.

    CAS  PubMed  Google Scholar 

  • Finney, L. A., & O’Halloran, T. V. (2003). Transition metal speciation in the cell: Insights fromthechemistryofmetal ionreceptors. Science, 300, 931–936.

    CAS  PubMed  Google Scholar 

  • Fulda, S., & Hagemann, M. (1995). Salt treatment induces accumulation of flavodoxin in the cyanobacterium Synechocystis sp. PCC 6803. Journal of Plant Physiology, 146(4), 520–526.

    CAS  Google Scholar 

  • Fulda, S., Huang, F., Nilsson, F., et al. (2000). Proteomics of Synechocystis sp. strain PCC 6803: Identification of periplasmic proteins in cells grown at low and high salt concentrations. European Journal of Biochemistry, 267, 5900–5907.

    CAS  PubMed  Google Scholar 

  • Geiss, U., Vinnemeier, J., Kunert, A., et al. (2001). Detection of the isiA gene across cyanobacterial strains: Potential for probing iron deficiency. Applied and Environmental Microbiology, 67(11), 5247–5253.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ghassemian, M., & Straus, N. A. (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 

  • Gonzalez, A., Bes, M. T., Barja, F., et al. (2010). Overexpression of FurA in Anabaena sp. PCC 7120 reveals new targets for this regulator involved in photosynthesis, iron uptake and cellular morphology. Plant & Cell Physiology, 51, 1900–1914.

    CAS  Google Scholar 

  • Gonzalez, A., Bes, M. T., Peleato, M. L., et al. (2011). Unraveling the regulatory function of FurA in Anabaena sp. PCC 7120 through 2-D DIGE proteomic analysis. Journal of Proteomics, 74, 660–671.

    CAS  PubMed  Google Scholar 

  • Gonzalez, A., Bes, M. T., Valladares, A., et al. (2012). FurA is the master regulator of iron homeostasis and modulates the expression of tetrapyrrole biosynthesis genes in Anabaena sp. PCC 7120. Environmental Microbiology, 14(12), 3175–3187.

    CAS  PubMed  Google Scholar 

  • Gonzalez, A., Angarica, V. E., Sancho, J., et al. (2014). The FurA regulon in Anabaena sp. PCC 7120: In silico prediction and experimental validation of novel target genes. Nucleic Acids Research, 42, 4833–4846.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez, A., Bes, M. T., Peleato, M. L., et al. (2016). Expanding the role of FurA as essential global regulator in cyanobacteria. PLoS One, 11(3), e0151384.

    PubMed  PubMed Central  Google Scholar 

  • Grossman, A. R., Schaefer, M. R., Chiang, G. G., & Collier, J. L. (1993). The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiological Reviews, 57, 725–749.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guerinot, M. L., & Yi, Y. (1994). Iron: Nutritious, noxious, and not readily available. Plant Physiology, 104, 815–820.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guikema, J. A., & Sherman, L. A. (1983). Organization and function of chlorophyll in membranes of cyanobacteria during iron-starvation. Plant Physiology, 73, 250–256.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guikema, J. A., & Sherman, L. A. (1984). Influence of iron deprivation on the membrane composition of Anacystis nidulans. Plant Physiology, 74, 90–95.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hagemann, M., Jeanjean, R., Fulda, S., et al. (1999). Flavodoxin accumulation contributes to enhanced cyclic electron flow around photosystem I in salt-stressed cells of Synechocystis sp strain PCC 6803. Physiologia Plantarum, 105, 670–678.

    CAS  Google Scholar 

  • Hantke, K. (1981). Regulation of ferric iron transport in Escherichia coli K12: Isolation of a constitutive mutant. Molecular & General Genetics, 182, 288–292.

    CAS  Google Scholar 

  • Hantke, K. (2001). Iron and metal regulation in bacteria. Current Opinion in Microbiology, 4, 172–177.

    CAS  PubMed  Google Scholar 

  • Hantke, K., & Braun, V. (1998). Control of bacterial iron transport by regulatory proteins. In S. Silver & W. Walden (Eds.), Metal ions in gene regulation (pp. 11–45). New York: International Thomson Publishing.

    Google Scholar 

  • Havaux, M., Guedeney, G., Hagemann, M., et al. (2005). The chlorophyllbinding protein IsiA is inducible by high light and protects the cyanobacterium Synechocystis PCC6803 from photooxidative stress. FEBS Letters, 579, 2289–2293.

    CAS  PubMed  Google Scholar 

  • Hernández, J. A., Artieda, M., Peleato, M. L., et al. (2002). Iron stress and genetic response in cyanobacteria: Fur genes from Synechococcus PCC 7942 and Anabaena PCC 7120. Annales de Limnologie, 38(1), 3–11.

    Google Scholar 

  • Hernández, J. A., Lopez-Gomollon, S., Bes, M. T., et al. (2004). Three fur homologues from Anabaena sp. PCC7120: Exploring reciprocal protein-promoter recognition. FEMS Microbiology Letters, 236(2), 275–282.

    PubMed  Google Scholar 

  • Hernández, J. A., López-Gomollón, S., Muro-Pastor, A., et al. (2006). Interaction of FurA from Anabaena sp PCC 7120 with DNA: A reducing environment and the presence of Mn2+ are positive effectors in the binding to isiB and furA promoters. Biometals, 19, 259–268.

    PubMed  Google Scholar 

  • Hopkinson, B. M., & Morel, F. M. (2009). The role of siderophores in iron acquisition by photosynthetic marine microorganisms. Biometals, 22, 659–669.

    CAS  PubMed  Google Scholar 

  • Hutber, G. N., Hutson, K. G., & Rogers, L. J. (1977). Effect of iron deficiency on levels of two ferredoxins and flavodoxin in a cyanobacterium. FEMS Microbiology Letters, 1, 193–196.

    CAS  Google Scholar 

  • Ivanov, A. G., Park, Y. I., Miskiewicz, E., et al. (2000). Iron stress restricts photosynthetic intersystem electron transport in Synechococcus sp. PCC 7942. FEBS Letters, 485, 173–177.

    CAS  PubMed  Google Scholar 

  • Ivanov, A. G., Krol, M., Sveshnikov, D., et al. (2006). Iron deficiency in cyanobacteria causes monomerization of photosystem I trimers and reduces the capacity for state transitions and the effective absorption cross section of photosystem I in vivo. Plant Physiology, 141, 1436–1445.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jantaro, S., Ali, Q., Lone, S., et al. (2006). Suppression of the lethality of high light to a quadruple HLI mutant by the inactivation of the regulatory protein PfsR in Synechocystis PCC 6803. The Journal of Biological Chemistry, 281(41), 30865–30874.

    CAS  PubMed  Google Scholar 

  • Jeanjean, R., Zuther, E., Yeremenko, N., et al. (2003). A photosystem I psaFJ-null mutant of the cyanobacterium Synechocystis PCC 6803 expresses the isiAB operon under iron replete conditions. FEBS Letters, 549, 52–56.

    CAS  PubMed  Google Scholar 

  • Jordan, P., Fromme, P., Witt, H. T., et al. (2001). Three-dimensional structure of cyanobacterial photosystem I at 2.5 A ° resolution. Nature, 411, 909–917.

    CAS  PubMed  Google Scholar 

  • Kaneko, T., Sato, S., Kotani, H., et al. (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 Research, 3(3), 109–136.

    CAS  PubMed  Google Scholar 

  • Katoh, H., Hagino, N., & Grossman, A. R. (2001a). Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803. Journal of Bacteriology, 183, 2779–2784.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh, H., Hagino, N., & Ogawa, T. (2001b). Iron-binding of FutA1 subunit of an ABC-type iron transporter in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant & Cell Physiology, 42, 823–827.

    CAS  Google Scholar 

  • Keren, N., Aurora, R., & Pakrasi, H. B. (2004). Critical roles of bacterioferritins in iron storage and proliferation of cyanobacteria. Plant Physiology, 135, 1666–1673.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koropatkin, N., Randich, A. M., Bhattacharyya-Pakrasi, M., et al. (2007). The structure of the iron-binding protein, FutA1, from Synechocystis 6803. The Journal of Biological Chemistry, 282, 27468–27477.

    CAS  PubMed  Google Scholar 

  • KouÅ™il, R., Yeremenko D’Haene, N. S., et al. (2003). Photosystem I trimers from Synechocystis PCC 6803 lacking the PsaF and PsaJ subunits bind an IsiA ring of 17 units. Biochimica et Biophysica Acta, 1607, 1–4.

    PubMed  Google Scholar 

  • KouÅ™il, R., Arteni, A. A., Lax, J., et al. (2005). Structure and functional role of supercomplexes of IsiA and photosystem I in cyanobacterial photosynthesis. FEBS Letters, 579, 3253–3257.

    PubMed  Google Scholar 

  • Kranzler, C., Rudolf, M., Keren, N., et al. (2013). Iron in cyanobacteria. Advances in Botanical Research, 65, 57–105.

    CAS  Google Scholar 

  • Kranzler, C., Lis, H., Finkel, O. M., et al. (2014). Coordinated transporter activity shapes high-affinity iron acquisition in Cyanobacteria. ISMEJ, 8, 409–417.

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Latifi, A., Jeanjean, R., Lemeille, S., et al. (2005). Iron starvation leads to oxidative stress in Anabaena sp. strain PCC 7120. Journal of Bacteriology, 187, 6596–6598.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Latifi, A., Ruiz, M., & Zhang, C. C. (2009). Oxidative stress in cyanobacteria. FEMS Microbiology Reviews, 33(2), 258–278.

    CAS  PubMed  Google Scholar 

  • Lax, J. E. M., Arteni, A. A., Boekema, E., et al. (2007). Structural response of photosystem II to iron deficiency: Characterization of a new photosystem II-IdiA complex from the cyanobacterium Thermosynechococcus elongatus BP-1. Biochimica et Biophysica Acta, 1767, 528–534.

    CAS  PubMed  Google Scholar 

  • Leonhardt, K., & Straus, N. A. (1992). An iron stress operon involved in photosynthetic electron transport in the marine cyanobacterium Synechococcus sp. PCC 7002. Journal of General Microbiology, 138, 1613–1621.

    CAS  PubMed  Google Scholar 

  • Leonhardt, K., & Straus, N. A. (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 Molecular Biology, 24(1), 63–73.

    CAS  PubMed  Google Scholar 

  • Li, H., Singh, A. K., McIntyre, L. M., et al. (2004). Differential gene expression in response to hydrogen peroxide and the putative PerR regulon of Synechocystis sp. strain PCC 6803. Journal of Bacteriology, 186, 3331–3345.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lodeyro, A. F., Ceccoli, R. D., Pierella Karlusich, J. J., et al. (2012). The importance of flavodoxin for environmental stress tolerance in photosynthetic microorganisms and transgenic plants. Mechanism, evolution and biotechnological potential. FEBS Letters, 586(18), 2917–2924.

    CAS  PubMed  Google Scholar 

  • Ludwig, M., Chua, T. T., Chew, C. Y., et al. (2015). Fur-type transcriptional repressors and metal homeostasis in the cyanobacterium Synechococcus sp. PCC 7002. Frontiers in Microbiology, 6, 1217.

    PubMed  PubMed Central  Google Scholar 

  • Mann, E. L., & Chisholm, S. W. (2000). Iron limits the cell division rate of Prochlorococcus in the eastern equatorial Pacific. Limnology and Oceanography, 45(5), 1067–1076.

    CAS  Google Scholar 

  • Martin, J. H., & Fitzwater, S. E. (1988). Iron deficiency limits phytoplankton growth in the north-East Pacific subarctic. Nature, 331, 341–343.

    CAS  Google Scholar 

  • Martin, J. H., Coale, K. H., Johnson, K. S., et al. (1994). Testing the iron hypothesis in ecosystems of the equatorial pacific ocean. Nature, 371, 123–129.

    CAS  Google Scholar 

  • Martin-Luna, B., Hernandez, J. A., Bes, M. T., et al. (2006). Identification of a ferric uptake regulator from Microcystis aeruginosa PCC7806. FEMS Microbiology Letters, 254(1), 63–70.

    CAS  PubMed  Google Scholar 

  • Melkozernov, A. N., Bibby, T. S., Lin, S., et al. (2003). Time-resolved absorption and emission show that the CP43’ antenna ring of iron-stressed Synechocystis sp. PCC6803 is efficiently coupled to the photosystem I reaction center core. Biochemistry, 42, 3893–3903.

    CAS  PubMed  Google Scholar 

  • Michel, K. P., & Pistorius, E. K. (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 Teil C Biochem Biophys Biol Virol, 47, 867–874.

    CAS  Google Scholar 

  • Michel, K. P., & Pistorius, E. K. (2004). Adaptation of the photosynthetic electron transport chain in cyanobacteria to iron deficiency: The function of IdiA and IsiA. Physiologia Plantarum, 119, 1–15.

    Google Scholar 

  • Michel, K. P., Thole, H. H., & Pistorius, E. K. (1996). IdiA, a 34 kDa protein in the cyanobacteria Synechococcus sp. strains PCC 6301 and PCC 7942, is required for growth under iron and manganese limitations. Microbiology, 142(Pt9), 1635–1645.

    Google Scholar 

  • Michel, K. P. P., Exss-Sonne, G., Scholten-Beck, U., et al. (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.

    CAS  PubMed  Google Scholar 

  • Michel, K. P., Pistorius, E. K., & Golden, S. S. (2001). Unusual regulatory elements for iron deficiency induction of the idiA gene of Synechococcus elongatus PCC 7942. Journal of Bacteriology, 183, 5015–5024.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miethke, M., & Marahiel, M. A. (2007). Siderophore-based iron acquisition and pathogen control. Microbiology and Molecular Biology Reviews, 71, 413.

    CAS  PubMed  Google Scholar 

  • Mirus, O., Strauss, S., Nicolaisen, K., et al. (2009). TonB-dependent transporters and their occurrence in cyanobacteria. BMC Biology, 7, 68.

    PubMed  PubMed Central  Google Scholar 

  • Morel, F. M. M., Kustka, A. B., & Shaked, Y. (2008). The role of unchelated Fe in the iron nutrition of phytoplankton. Limnology and Oceanography, 53, 400–404.

    CAS  Google Scholar 

  • Neilands, J. B. (1982). Microbial envelope proteins related to iron. Annual Review of Microbiology, 36, 285–309.

    CAS  PubMed  Google Scholar 

  • Neilands, J. B. (1995). Siderophores: Structure and function of microbial iron transport compounds. The Journal of Biological Chemistry, 270, 26723–26726.

    CAS  PubMed  Google Scholar 

  • Nicolaisen, K., Moslavac, S., Samborski, A., et al. (2008). Alr0397 is an outer membrane transporter for the siderophore schizokinen in Anabaena sp strain PCC 7120. Journal of Bacteriology, 190, 7500–7507.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nicolaisen, K., Hahn, A., Valdebenito, M., et al. (2010). The interplay between siderophore secretion and coupled iron and copper transport in the heterocyst-forming cyanobacterium Anabaena sp. PCC 7120. Biochimica et Biophysica Acta, 1798, 2131–2140.

    CAS  PubMed  Google Scholar 

  • Nodop, A., Pietsch, D., Höcker, R., et al. (2008). Transcript profiling reveals new insights into the acclimation of the emesophilic fresh-water cyanobacterium Synechococcus elongatus PCC 7942 to iron starvation. Plant Physiology, 147, 747–763.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Noinaj, N., Guillier, M., Barnard, T. J., et al. (2010). TonB-dependent transporters: Regulation, structure, and function. Annual Review of Microbiology, 64, 43–60.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Obando, S. T. A., Babykin, M. M., & Zinchenko, V. V. (2018). A cluster of five genes essential for the utilization of dihydroxamate xenosiderophores in Synechocystis sp. PCC 6803. Current Microbiology, 75, 1165–1173.

    Google Scholar 

  • Odom, W. R., Hodges, R., Chitnis, P. R., et al. (1993). Characterization of Synechocystis sp. PCC 6803 in iron-supplied and iron-deficient media. Plant Molecular Biology, 23, 1255–1264.

    CAS  PubMed  Google Scholar 

  • Öquist, G. (1971). Changes in pigment composition and photosynthesis induced by iron-deficiency in blue-green-alga Anacystis nidulans. Physiologia Plantarum, 25, 188–191.

    Google Scholar 

  • Pakrasi, H. B., Goldenberg, A., & Sherman, L. A. (1985). Membrane development in the cyanobacterium, Anacystis nidulans, during recovery from Iron starvation. Plant Physiology, 79(1), 290–295.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Park, Y. I., Sandstrom, S., Gustafsson, P., et al. (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. Molecular Microbiology, 32(1), 123–129.

    CAS  PubMed  Google Scholar 

  • Pierella Karlusich, J. J., Ceccoli, R. D., Grana, M., et al. (2015). Environmental selection pressures related to iron utilization are involved in the loss of the flavodoxin gene from the plant genome. Genome Biology and Evolution, 7(3), 750–767.

    PubMed  PubMed Central  Google Scholar 

  • Ratledge, C., & Dover, L. G. (2000). Iron metabolism in pathogenic bacteria. Annual Review of Microbiology, 54, 881–941.

    CAS  PubMed  Google Scholar 

  • Raven, J. A., Evans, M. C. W., & Korb, R. E. (1999). The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynthesis Research, 60, 111–149.

    CAS  Google Scholar 

  • Razquin, P., Schmitz, S., & Peleato, M. L. (1995). Differential activities of heterocyst ferredoxin, vegetative cell ferredoxin, and flavodoxin as electron carriers in nitrogen-fixation and photosynthesis in Anabaena sp. Photosynthesis Research, 43(1), 35–40.

    CAS  PubMed  Google Scholar 

  • Rich, H. W., & Morel, F. M. M. (1990). Availability of well-defined iron colloids to the marine diatom Thalassiosira weissflogii. Limnology and Oceanography, 35(3), 652–662.

    CAS  Google Scholar 

  • Richardson, D. J. (2000). Bacterial respiration: A flexible process for a changing environment. Microbiology, 146(Pt 3), 551–571.

    CAS  PubMed  Google Scholar 

  • Richier, S., Macey, A. I., Pratt, N. J., et al. (2012). Abundances of iron-binding photosynthetic and nitrogen-fixing proteins of trichodesmium both in culture and in situ from the North Atlantic. PLoS One, 7, e35571.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riethman, H. C., & Sherman, L. A. (1988). Purification and characterization of an iron stress-induced chlorophyll-protein from the cyanobacterium Anacystis nidulans R2. Biochimica et Biophysica Acta, 935, 141–151.

    CAS  PubMed  Google Scholar 

  • Rocap, G., Larimer, F. W., Lamerdin, J., et al. (2003). Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature, 424(6952), 1042–1047.

    CAS  PubMed  Google Scholar 

  • Rudolf, M., Kranzler, C., Lis, H., et al. (2015). Multiple modes of iron uptake by the filamentous, siderophore-producing cyanobacterium, Anabaena sp. PCC 7120. Molecular Microbiology, 97, 577–588.

    CAS  PubMed  Google Scholar 

  • Rueter, J. G., Ohki, K., & Fujita, Y. (1990). The effect of iron nutrition on photosynthesis and nitrogen fixation in cultures of Trichodesmium (cyanophyceae) 1. Journal of Phycology, 26, 30–35.

    CAS  Google Scholar 

  • Sandmann, G. (1985). Consequences of iron deficiency on photosynthetic and respiratory electron transport in blue-green algae. Photosynthesis Research, 6, 261–271.

    CAS  PubMed  Google Scholar 

  • Sandmann, G., & Malkin, R. (1983). Iron-sulfur centers and activities of the photosynthetic electron transport chain in iron-deficient cultures of the blue-green alga Aphanocapsa. Plant Physiology, 73, 724–728.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sandström, S., Park, Y. I., Oquist, G., et al. (2001). CP43’, the isiA gene product, functions as an excitation energy dissipator in the cyanobacterium Synechococcus sp. PCC 7942. Photochemistry and Photobiology, 74, 431–437.

    PubMed  Google Scholar 

  • Sandström, S., Ivanov, A. G., Park, Y. I., et al. (2002). Iron stress responses in the cyanobacterium Synechococcus sp. PCC 7942. Physiologia Plantarum, 116, 255–263.

    PubMed  Google Scholar 

  • Schrader, P. S., Milligan, A. J., & Behrenfeld, M. J. (2011). Surplus photosynthetic antennae complexes underlie diagnostics of iron limitation in a cyanobacterium. PLoS One, 6, e18753.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shcolnick, S., & Keren, N. (2006). Metal homeostasis in cyanobacteria and chloroplasts. Balancing benefits and risks to the photosynthetic apparatus. Plant Physiology, 141, 805–810.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shcolnick, S., Summerfield, T. C., Reytman, L., et al. (2009). The mechanism of iron homeostasis in the unicellular cyanobacterium synechocystis sp. PCC 6803 and its relationship to oxidative stress. Plant Physiology, 150, 2045–2056.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sherman, D. M., & Sherman, L. A. (1983). Effect of iron deficiency and iron restoration on ultrastructure of Anacystis nidulans. Journal of Bacteriology, 156, 393–401.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi, T., Sun, Y., & Falkowski, P. G. (2007). Effects of iron limitation on the expression of metabolic genes in the marine cyanobacterium Trichodesmium erythraeum IMS101. Environmental Microbiology, 9, 2945–2956.

    CAS  PubMed  Google Scholar 

  • Simpson, F. B., & Nielands, J. B. (1976). Siderochromes in cyanophyceae: Isolation and characterization of schizokinen from Anabaena sp. Journal of Phycology, 12(44), 48.

    Google Scholar 

  • Straus, N. A. (1994). Iron deprivation: Physiology and gene regulation. In D. A. Bryant (Ed.), The molecular biology of cyanobacteria (Advances in photosynthesis) (Vol. 1, pp. 731–750). Dordrecht: Springer.

    Google Scholar 

  • Sun, J., & Golbeck, J. H. (2015). The presence of the IsiA-PSI supercomplex leads to enhanced photosystem I electron throughput in iron-starved cells of Synechococcus sp. PCC 7002. The Journal of Physical Chemistry. B, 119(43), 13549–13559.

    CAS  PubMed  Google Scholar 

  • Tognetti, V. B., Zurbriggen, M. D., Morandi, E. N., et al. (2007). Enhanced plant tolerance to iron starvation by functional substitution of chloroplast ferredoxin with a bacterial flavodoxin. Proceedings of the National Academy of Sciences of the United States of America, 104(27), 11495–11500.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tolle, J., Michel, K. P., Kruip, J., et al. (2002). Localization and function of the IdiA homologue Slr1295 in the cyanobacterium Synechocystis sp. strain PCC 6803. Microbiology, 148, 3293–3305.

    CAS  PubMed  Google Scholar 

  • Trick, C. G., & Kerry, A. (1992). Isolation and purification of siderophores produced by cyanobacteria, Synechococcus sp. PCC 7942 and Anabaena variabilis ATCC 29413. Current Microbiology, 24, 241–245.

    CAS  Google Scholar 

  • Vigara, A. J., Inda, L. A., & Vega, J. M. (1998). Flavodoxin as an electronic donor in photosynthetic inorganic nitrogen assimilation by iron-deficient Chlorella fusca cells. Photochemistry and Photobiology, 67(4), 446–449.

    CAS  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. Archives of Microbiology, 172, 377–386.

    CAS  PubMed  Google Scholar 

  • Waldron, K. J., Tottey, S., Yanagisawa, S., et al. (2007). A periplasmic iron-binding protein contributes toward inward copper supply. The Journal of Biological Chemistry, 282, 3837–3846.

    CAS  PubMed  Google Scholar 

  • Walworth, N. G., Fu, F. X., Webb, E. A., et al. (2016). Mechanisms of increased Trichodesmium fitness under iron and phosphorus co-limitation in the present and future ocean. Nature Communications, 7, 12081.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Q., Hall, C. L., Al-Adami, M. Z., et al. (2010). IsiA is required for the formation of photosystem I supercomplexes and for efficient state transition in Synechocystis PCC 6803. PLoS One, 5, e10432.

    PubMed  PubMed Central  Google Scholar 

  • Webb, E. A., Moffett, J. W., & Waterbury, J. B. (2001). Iron stress in open-ocean cyanobacteria (Synechococcus, Trichodesmium, and Crocosphaera spp.): Identification of the IdiA protein. Applied and Environmental Microbiology, 67, 5444–5452.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilhelm, S. W. (1995). Ecology of iron-limited cyanobacteria: A review of physiological responses and implications for aquatic systems. Aquatic Microbial Ecology, 9, 295–303.

    Google Scholar 

  • Xu, W., Jeanjean, R., Liu, Y., et al. (2003). pkn22 (alr2502) encoding a putative Ser/Thr kinase in the cyanobacterium Anabaena sp. PCC 7120 is induced by both iron starvation and oxidative stress and regulates the expression of isiA. FEBS Letters, 553(1–2), 179–182.

    CAS  PubMed  Google Scholar 

  • Yeremenko, N., Kouril, R., Ihalainen, J. A., et al. (2004). Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria. Biochemistry, 43, 10308–10313.

    CAS  PubMed  Google Scholar 

  • Yousef, N., Pistorius, E. K., & Michel, K. P. (2003). Comparative analysis of idiA and isiA transcription under iron starvation and oxidative stress in Synechococcus elongatus PCC 7942 wild-type and selected mutants. Archives of Microbiology, 180, 471–483.

    CAS  PubMed  Google Scholar 

  • Yu, C., & Genco, C. A. (2012). Fur-mediated global regulatory circuits in pathogenic Neisseria species. Journal of Bacteriology, 194, 6372–6381.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. NCI, NIH, Bethesda, MD, USA

    Dan Cheng

  2. Department of Biology, University of Arkansas at Little Rock, Little Rock, AR, USA

    Qingfang He

Authors
  1. Dan Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qingfang He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qingfang He .

Editor information

Editors and Affiliations

  1. Key laboratory of Plant Stress Biology, State Key Laboratory of Cotton Biology, School of Life Sciences, Henan University, Kaifeng, Henan, China

    Qiang Wang

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Cheng, D., He, Q. (2020). Iron Deficiency in Cyanobacteria. In: Wang, Q. (eds) Microbial Photosynthesis. Springer, Singapore. https://doi.org/10.1007/978-981-15-3110-1_10

Download citation

Publish with us

Policies and ethics

Search

Navigation