Skip to main content

Adaptive Mechanisms of the Model Photosynthetic Organisms, Cyanobacteria, to Iron Deficiency

  • Chapter
  • First Online:
Microbial Photosynthesis

Abstract

Cyanobacteria are the oldest oxygen-evolving photosynthetic organisms on the Earth. They are widely distributed in marine, freshwater, and terrestrial environments and contribute about 25% of global primary productivity. They are thought to be responsible for the conversion of the Earth’s atmosphere from anaerobic to aerobic about 2.4 billion years ago. This development permitted the evolution of aerobic bacteria, algae, plants, and animals. However, due to the emergence of oxidative environments on the Earth’s surface, soluble ferrous iron (Fe2+) was almost completely oxidized to hardly soluble ferric iron (Fe3+) in aquatic environments. The extremely low bioavailability of iron in the ocean has been considered as an important factor that is limiting global primary productivity. As photosynthetic organisms, cyanobacteria have higher iron demand than other non-photosynthetic organisms to meet the needs of photosynthetic electron transport and chlorophyll synthesis. The nitrogen-fixing cyanobacteria need even more iron to fix the inert dinitrogen gas. The contradiction between the high iron demand of cyanobacteria and their iron-limiting habitats has forced them to evolve special strategies to overcome iron deficiency during the long-period evolution. In this review, we summarized the recent perspectives on the physiological responses and special strategies of cyanobacteria to overcome the changing iron bioavailability in freshwater, coastal, and open-ocean environments.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
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

Change history

  • 09 October 2020

    The original version of the book was revised with the following corrections.

References

  • Abdallah, F., Salamini, F., & Leister, D. (2000). A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. Trends in Plant Science, 5, 141–142.

    Article  CAS  PubMed  Google Scholar 

  • Andrews, S. C., Smith, J. M. A., Hawkins, C., Williams, J. M., Harrison, P. M., & Guest, J. R. (1993). Overproduction, purification and characterization of the bacterioferritin of Escherichia coli and a C-terminally extended variant. European Journal of Biochemistry, 213, 329–338.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Andrizhiyevskaya, E. G., Schwabe, T. M. E., Germano, M. D., Haene, S., Kruip, J., van Grondelle, R., & Dekker, J. P. (2002). Spectroscopic properties of PSI–IsiA supercomplexes from the cyanobacterium Synechococcus PCC 7942. Biochimica et Biophysica Acta, 1556, 265–272.

    Article  CAS  PubMed  Google Scholar 

  • Årstøl, E., & Hohmann-Marriott, M. F. (2019). Cyanobacterial siderophores-physiology, structure, biosynthesis, and applications. Marine Drugs, 17(5), 281.

    Google Scholar 

  • Baichoo, N., Wang, T., Ye, R., & Helmann, J. D. (2002). Global analysis of the Bacillus subtilis Fur regulon and the iron starvation stimulon. Molecular Microbiology, 45, 1613–1629.

    Article  CAS  PubMed  Google Scholar 

  • Bailey, S., Melis, A., Mackey, K. R. M., Cardol, P., Finazzi, G., et al. (2008). Alternative photosynthetic electron flow to oxygen in marine Synechococcus. Biochimica et Biophysica Acta, 1777, 269–276.

    Article  CAS  PubMed  Google Scholar 

  • Bakker, D. C. E., Watson, A. J., & Law, C. S. (2001). Southern Ocean iron enrichment promotes inorganic carbon drawdown. Deep Sea Research Part II, 48, 2483–2507.

    Article  CAS  Google Scholar 

  • Barber, J., Nield, J., Duncan, J., & Bibby, T. S. (2006). Accessory chlorophyll proteins in cyanobacterial photosystem l. In J. H. Golbeck (Ed.), Photosystem I (pp. 99–117). Dordrecht, Springer.

    Google Scholar 

  • Barbeau, K., Rue, E. L., Bruland, K. W., & Butler, A. (2001). Photochemical cycling of iron in the surface ocean mediated by microbial iron(III)-binding ligands. Nature, 413, 409–413.

    Article  CAS  PubMed  Google Scholar 

  • Behrenfeld, M. J., & Milligan, A. J. (2013). Photophysiological expressions of iron stress in phytoplankton. Annual Review of Marine Science, 5, 217–246.

    Article  PubMed  Google Scholar 

  • Berman-frank, I., Cullen, J. T., Shaked, Y., Sherrell, R., & Falkowski, P. G. (2001). Iron availability, cellular quotas, and nitrogen fixation in Trichodesmium. Limnology and Oceanography, 46, 1249–1260.

    Article  CAS  Google Scholar 

  • Berry, S., Schneider, D., Vermaas, W. F. J., & Rogner, M. (2002). Electron transport routes in whole cells of Synechocystis sp strain PCC 6803: The role of the cytochrome bd-type oxidase. Biochemistry, 41, 3422–3429.

    Article  CAS  PubMed  Google Scholar 

  • Bhaya, D., Bianco, N. R., Bryant, D., & Grossman, A. (2000). Type iv pilus biogenesis and motility in the cyanobacterium synechocystis sp. PCC 6803. Molecular Microbiology, 37, 941–951.

    Article  CAS  PubMed  Google Scholar 

  • Bibby, T. S., 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 

  • Bibby, T. S., Mary, I., Nield, J., Partensky, F., & Barber, J. (2003). Low-light-adapted Prochlorococcus species possess specific antennae for each photosystem. Nature, 424, 1051–1054.

    Article  CAS  PubMed  Google Scholar 

  • Binder, A. (1982). Respiration and photosynthesis in energy-transducing membranes of cyanobacteria. Journal of Bioenergetics and Biomembranes, 14, 271–286.

    Article  CAS  PubMed  Google Scholar 

  • Bishop, P. E., & Premakumar, R. (1992). Alternative nitrogen fixation systems. In G. Stacey, R. H. Burris, & D. J. Evans (Eds.), Biological nitrogen fixation (pp. 736–762). New York: Chapman & Hall.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Boyd, P., Jickells, T., Law, C. S., Blain, S., Boyle, E. A., Buesseler, K. O., et al. (2007). Mesoscale iron enrichment experiments 1993–2005: Synthesis and future directions. Science, 315, 612–617.

    Article  CAS  PubMed  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.

    Article  CAS  PubMed  Google Scholar 

  • Bruland, K. W., Franks, R. P., Kanuer, G., & Martin, J. H. (1979). Sampling and analytical methods for the determination of copper, cadmium, zinc, and nickel in seawater. Analytica Chimica Acta, 105, 233–245.

    Article  CAS  Google Scholar 

  • Burnap, R. L., Troyan, T., & Sherman, L. A. (1993). The highly abundant chlorophyll–protein complex of iron-deficient Synechococcus sp. PCC 7942 (CP43′) is encoded by the isiA gene. Plant Physiology, 103, 893–902.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Canini, A., Civitareale, P., Marini, S., Grilli, C. A., & Rotilio, G. (1992). Purification of iron superoxide dismutase from the cyanobacterium Anabaena cylindrica Lemm and localization of the enzyme in heterocysts by immunogold labeling. Planta, 187, 438–444.

    Article  CAS  PubMed  Google Scholar 

  • Cao, H. S., Kong, F. X., Tan, J. K., Zhang, X. F., Tao, Y., & Yang, Z. (2005). Recruitment of total phytoplankton, chlorophytes and cyanobacteria from lake sediments recorded by photosynthetic pigments in a large, shallow lake (Lake Taihu, China). International Review of Hydrobiology, 90, 347–357.

    Article  CAS  Google Scholar 

  • Capone, D. G., Zehr, J. P., Paerl, H. W., Bergman, B., & Carpenter, E. J. (1997). Trichodesmium, a globally significant marine cyanobacterium. Science, 276, 1221–1229.

    Article  CAS  Google Scholar 

  • Capone, D. G., Burns, J. A., Montoya, J. P., Subramaniam, A., Mahaffey, C., Gunderson, T., Michaels, A. F., & Carpenter, E. J. (2005). Nitrogen fixation by Trichodesmium spp: An important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Global Biogeochemical Cycles, 19.

    Google Scholar 

  • Carroll, C. S., & Moore, M. M. (2018). Ironing out siderophore biosynthesis: A review of non-ribosomal peptide synthetase (NRPS)-independent siderophore synthetases. Critical Reviews in Biochemistry and Molecular Biology, 53(4), 356–381.

    Article  CAS  PubMed  Google Scholar 

  • Chereskin, B., & Castelfranco, P. (1982). Effects of iron and oxygen on the biosynthetic pathway in etiochloroplasts II observations on isolated etiochloroplasts. Plant Physiology, 69, 112–116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coy, M., & Neilands, J. B. (1991). Structural dynamics and functional domains of the Fur protein. Biochemistry, 30, 8201–8210.

    Article  CAS  PubMed  Google Scholar 

  • Croot, P. L., Bowie, A. R., Frew, R. D., Maldonado, M. T., Hall, J. A., Safi, K. A., La Roche, J., Boyd, P. W., & Law, C. S. (2001). Retention of dissolved iron and Fe-II in an iron induced Southern Ocean phytoplankton bloom. Geophysical Research Letters, 28, 3425–3428.

    Article  CAS  Google Scholar 

  • Croot, P. L., Passow, U., Assmy, P., Jansen, S., & Strass, V. H. (2007). Surface active substances in the upper water column during a Southern Ocean Iron fertilization experiment (EIFEX). Geophysical Research Letters, 34, C06015.

    Article  CAS  Google Scholar 

  • Croot, P. L., Bluhm, K., Schlosser, C., Streu, P., Breitbarth, E., Frew, R., & Van Ardelan, M. (2008). Regeneration of Fe(II) during EIFeX and SOFeX. Geophysical Research Letters, 35, L19606.

    Article  CAS  Google Scholar 

  • Dan, C., Qingfang, H., & Araujo, W. L. (2014). PfsR is a key regulator of iron homeostasis in Synechocystis PCC 6803. PLoS One, 9, e101743.

    Article  CAS  Google Scholar 

  • de Lorenzo, V., Giovannini, F., Herrero, M., & Neilands, J. B. (1988). Metal ion regulation of gene expression. Fur repressor-operator interaction at the promoter region of the aerobactin system of pColV-K30. Journal of Molecular Biology, 203, 875–884.

    Article  PubMed  Google Scholar 

  • de los Ríos, A., Grube, M., Sancho, L. G., & Ascaso, C. (2007). Ultrastructural and genetic characteristics of endolithic cyanobacterial biofilms colonizing Antarctic granite rocks. FEMS Microbial Ecology, 2, 386–395.

    Google Scholar 

  • Decho, A. (1990). Microbial exopolymer secretions in ocean environments: Their role(s) in food webs and marine processes. Oceanography and Marine Biology. Annual Review, 28, 73–153.

    Google Scholar 

  • Delany, I., Spohn, G., Rappuoli, R., et al. (2001). The fur repressor controls transcription of iron-activated and-repressed gene in Helicobacter pylori. Molecular Microbiology, 42, 1297–1309.

    Google Scholar 

  • Dufresne, A., Salanoubat, M., Partensky, F., et al. (2003). Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proceedings of the National Academy of Sciences of the United States of America, 100, 10020–10025.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dühring, U., Axmann, I. M., Hess, W. R., & Wilde, A. (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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dwivedi, K., Sen, A., & Bullerjahn, G. S. (1997). Expression and mutagenesis of the dpsA gene of Synechococcus sp. PCC 7942, encoding a DNA-binding protein involved in oxidative stress protection. FEMS Microbiology Letters, 155, 85–91.

    Google Scholar 

  • Eitinger, T. (2004). In vivo production of active nickel superoxide dismutase from Prochlorococcus marinus MIT9313 is dependent on its cognate peptidase. Journal of Bacteriology, 186, 7821.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Entsch, B., & Smillie, R. M. (1972). Oxidation-reduction properties of phytoflavin, a flavoprotein from blue-green algae. Archives of Biochemistry and Biophysics, 151, 378–386.

    Article  CAS  PubMed  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Escolar, L., Perez-Martin, J., & De Lorenzo, V. (2000). Evidence of an unusually long operator for the Fur repressor in the aerobactin promoter of Escherichia coli[J]. Journal of Biological Chemistry, 275, 24709–24714.

    Article  CAS  Google Scholar 

  • Falk, S., Samson, G., Bruce, D., Huner, N. P. A., & Laudenbach, D. E. (1995). Functional analysis of the iron-stress induced CP43’ polypeptide of PSII in the cyanobacterium Synechococcus sp.PCC 7942. Photosynthesis Research, 45, 51–60.

    Article  CAS  PubMed  Google Scholar 

  • Falkowski, P. G., Barber, R. T., & Smetacek, V. (1998). Biogeochemical controls and feedbacks on ocean primary production. Science, 281, 200–207.

    Article  CAS  PubMed  Google Scholar 

  • Feely, R. A., Doney, S. C., & Cooley, S. R. (2009). Ocean acidification: Present conditions and future changes in a high-CO2 world. Oceanography, 22, 36–47.

    Article  Google Scholar 

  • Field, C. B., Behrenfeld, M. J., Randerson, J. T., & Falkowski, P. (1998). Primary production of the biosphere: Integrating terrestrial and oceanic components. Science, 281, 237–240.

    Article  CAS  PubMed  Google Scholar 

  • Flombaum, P., Gallegos, J. L., Gordillo, R. A., Rincón, J., Zabala, L. L., Jiao, N., et al. (2013). Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. Proceedings of the National Academy of Sciences of the United States of America, 110(24), 9824–9829.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fraser, J. M., Tulk, S. E., Jeans, J. A., Campbell, D. A., Bibby, T. S., & Cockshutt, A. M. (2013). Photophysiological and photosynthetic complex changes during iron starvation in Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942. PLoS ONE, 8(3), e59861.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii, M., Rose, A. L., Omura, T., & Waite, T. D. (2010). Effect of Fe(II) and Fe(III) transformation kinetics on iron acquisition by a toxic strain of Microcystis aeruginosa. Environmental Science & Technology, 44, 1980–1986.

    Article  CAS  Google Scholar 

  • Fujii, M., Dang, T. C., Rose, A. L., Omura, T., & Waite, T. D. (2011). Effect of light on iron uptake by the freshwater cyanobacterium microcystis aeruginosa. Environmental Science & Technology, 45, 1391–1398.

    Article  CAS  Google Scholar 

  • Fulda, S., Huang, F., Nilsson, F., Hagemann, M., & Norling, B. (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.

    Article  CAS  PubMed  Google Scholar 

  • Garnerin, T., Dassonville-Klimpt, A., & Sonnet, P. (2017). (2017) Fungal hydroxamate siderophores: Biosynthesis, chemical synthesis and potential medical applications. In A. Méndez-Vilas (Ed.), Antimicrobial Research: Novel Bioknowledge and Educational Programs. Badajoz, Spain: Formatex Research Center.

    Google Scholar 

  • Geider, R. J., & La Roche, J. (1994). The role of iron in phytoplankton photosynthesis, and the potential for iron-limitation of primary productivity in the sea. Photosynthesis Research, 39, 275–301.

    Article  CAS  PubMed  Google Scholar 

  • Georg, J., Kostova, G., Vuorijoki, L., et al. (2017). Acclimation of oxygenic photosynthesis to iron starvation is controlled by the sRNA IsaR1[J]. Current Biology, 27, 1425–1436. e7.

    Article  CAS  PubMed  Google Scholar 

  • Gledhill, M., & Buck, K. N. (2012). The organic complexation of iron in the marine environment: A review. Frontiers in Microbiology, 3, 128–144.

    Google Scholar 

  • Gledhill, M., & van den Berg, C. M. G. (1994). Determination of complexation of iron(III) with natural organic complexing ligands in seawater using cathodic stripping voltammetry. Marine Chemistry, 47, 41–54.

    Article  CAS  Google Scholar 

  • Goldman, S. J., Lammers, P. J., Berman, M. S., & Sanders-Loehr, J. (1983). Siderophore-mediated iron uptake in different strains of Anabaena sp. Journal of Bacteriology, 156, 1144–1150.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • González, 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.

    Google Scholar 

  • Gordon, R. M., Marin, J. H., & Knauer, G. A. (1982). Iron in north-east Pacific waters. Nature, 299, 611–612.

    Article  CAS  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hantkel, K. (2003). Is the bacterial ferrous iron transporter FeoB a living fossil? Trends in Microbiology, 11, 192–195.

    Article  CAS  Google Scholar 

  • Hart, S. E., Schlarb-Ridley, B. G., Bendall, D. S., & Howe, C. J. (2005). Terminal oxidases of cyanobacteria. Biochemical Society Transactions, 33, 832–835.

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Hernández-Prieto, M. A., Schön, V., Georg, J., Barreira, L., Varela, J., Hess, W. R., & Futschik, M. E. (2012). Iron deprivation in Synechocystis: Inference of pathways, non-coding RNAs, and regulatory elements from comprehensive expression profiling. G3, 2, 175–195.

    Google Scholar 

  • Hider, R. C., & Kong, X. (2010). Chemistry and biology of siderophores. Natural Product Reports, 27, 637–657.

    Article  CAS  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.

    Article  CAS  PubMed  Google Scholar 

  • Horsburgh, M. J., Clements, M. O., Crossley, H., Ingham, E., & Foster, S. J. (2001). PerR controls oxidative stress resistance and iron storage proteins and is required for virulence in Staphylococcus aureus. Infection and Immunity, 69, 3744–3754.

    Google Scholar 

  • Hudson, R. J. M., & Morel, F. M. M. (1993). Trace metal transport by marine microorganisms: Implications of metal coordination kinetics. Deep Sea Research, 140, 129–150.

    Article  Google Scholar 

  • Hutchins, D. A., Fe, F.-X., Zhang, Y., Warner, M. E., Feng, Y., et al. (2007). CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: Implications for past, present, and future ocean biogeochemistry. Limnology and Oceanography, 52, 1293–1304.

    Article  CAS  Google Scholar 

  • Ibisanmi, E., Sander, S. G., Boyd, P. W., Bowie, A. R., & Hunter, K. A. (2011). Vertical distributions of iron-(III) complexing ligands in the Southern Ocean. Deep Sea Research Part II: Topical Studies Oceanography, 58, 2113–2125.

    Article  CAS  Google Scholar 

  • Ito, Y., & Butler, A. (2005). Structure of synechobactins, new siderophores of the marine cyanobacterium Synechococcus sp. PCC 7002. Limnology and Oceanography, 50, 1918–1923.

    Google Scholar 

  • James, A., Guikema, S., & L. A. (1983). Organization and function of chlorophyll in membranes of cyanobacteria during iron starvation. Plant Physiology, 73, 250–225.

    Article  Google Scholar 

  • Jiang, H. B., Lou, W. J., Du, H. Y., Price, N. M., & Qiu, B. S. (2012). Sll1263, a unique cation diffusion facilitator protein that promotes iron uptake in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant and Cell Physiology, 53, 1404–1417.

    Google Scholar 

  • Jiang, H. B., Lou, W. J., Ke, W. T., Song, W. Y., Price, N. M., & Qiu, B. S. (2015). New insights into iron acquisition by cyanobacteria: An essential role for ExbB-ExbD complex in inorganic iron uptake. The ISME Journal, 9, 297–309.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, H. B., Fu, F. X., et al. (2018). Ocean warming alleviates iron limitation of marine nitrogen fixation. Nature Climate Change, 8(8), 709–712.

    Article  CAS  Google Scholar 

  • Jordan, P., Fromme, P., Witt, H. T., Klukas, O., Saenger, W., & Krauss, N. (2001). Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature, 411, 909–917.

    Article  CAS  PubMed  Google Scholar 

  • Kakhlon, O., & Cabantchik, Z. I. (2002). The labile iron pool: Characterization, measurement, and participation in cellular processes[J]. Free Radical Biology and Medicine, 33, 1037–1046.

    Article  CAS  PubMed  Google Scholar 

  • Kamiya, N., & Shen, J. R. (2003). Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution. Proceedings of the National Academy of Sciences of the United States of America, 100, 98–103.

    Article  CAS  PubMed  Google Scholar 

  • Katoh, H., Hagino, N., Grossman, A. R., & Ogawa, T. (2001). Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803. Journal of Bacteriology, 183(9), 2779–2784.

    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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kessler, N., Armoza-Zvuloni, R., Wang, S., Basu, S., Weber, P., Stuart, R., & Shaked, Y. (2019). Selective collection of iron-rich dust particles by natural Trichodesmium colonies. The ISME Journal, 14, 1–13.

    Google Scholar 

  • Khan, A., Singh, P., & Srivastava, A. (2017). Synthesis, nature and utility of universal iron chelator – Siderophore: A review. Microbiological Research, S0944501317306730.

    Google Scholar 

  • Khan, A., Singh, P., & Srivastava, A. (2018). Synthesis, nature and utility of universal iron chelator—Siderophore: A review. Microbiological Research, 212–213, 103–111.

    Article  PubMed  CAS  Google Scholar 

  • Kim, K. S., Chang, Y. J., Chung, Y. J., Park, C. U., & Seo, H. Y. (2007). Enhanced expression of high-affinity iron transporters via H-ferritin production in yeast. Journal of Biochemistry and Molecular Biology, 40, 82–87.

    CAS  PubMed  Google Scholar 

  • Kim, H., Lee, H., & Shin, D. (2015). Lon-mediated proteolysis of the FeoC protein prevents Salmonella enterica from accumulating the Fe(II) transporter FeoB under highoxygen conditions. Journal of Bacteriology, 197, 92–98.

    Article  PubMed  CAS  Google Scholar 

  • Klausner, R. D., Rouault, T. A., & Harford, J. B. (1993). Regulating the fate of mRNA: The control of cellular iron metabolism. Cell, 72, 19–28.

    Article  CAS  PubMed  Google Scholar 

  • Koedding, J., Polzer, P., Killig, F., Howard, S. P., Gerber, K., Seige, P., Diederichsand, K., & Weltea, W. (2004). Crystallization and preliminary X-ray analysis of a C-terminal TonB fragment from Escherichia coli. Acta Crystallographica Section D, 1281–1283.

    Google Scholar 

  • Kouřil, R., Arteni, A. A., Lax, J., Yeremenko, N., Haene, S. D., Rögner, M., Matthijs, H. C. P., Dekker, J. P., & Boekema, E. J. (2005). Structure and functional role of supercomplexes of IsiA and photosystem I in cyanobacterial photosynthesis. FEBS Letters, 579, 3253–3257.

    Article  PubMed  CAS  Google Scholar 

  • Kranzler, C., Lis, H., Shaked, Y., & Keren, N. (2011). The role of reduction in iron uptake processes in a unicellular, planktonic cyanobacterium. Environmental Microbiology, 13, 2990–2999.

    Article  CAS  PubMed  Google Scholar 

  • Kranzler, C., Lis, H., Finkel, O. M., Schmetterer, G., Shaked, Y., & Keren, N. (2014). Coordinated transporter activity shapes high-affinity iron acquisition in cyanobacteria. The ISME Journal, 8, 409–417.

    Article  CAS  PubMed  Google Scholar 

  • Krieger, A., & Rutherford, A. W. (1998). The involvement of H2O2 produced by photosystem II in photoinhibition. In G. Garab (Ed.), Photosynthesis: Mechanisms and effects (Vol. 3, pp. 2135–2213). Dordrecht: Kluwer Academic Publishers.

    Chapter  Google Scholar 

  • Kuma, K., Katsumoto, A., Kawakami, H., Takatori, F., & Matsunaga, K. (1998). Spatial variability of Fe(III) hydroxide solubility in the water column of the northern North Pacific Ocean. Deep Sea Research Part I: Oceanographic Research Papers, 45, 91–113.

    Article  CAS  Google Scholar 

  • Küpper, H., Šetlík, I., Seibert, S., Prášil, O., Šetlikova, E., Strittmatter, M., Levitan, O., Lohscheider, J., Adamska, I., & Berman-Frank, I. (2008). Iron limitation in the marine cyanobacterium Trichodesmium reveals new insights into regulation of photosynthesis and nitrogen fixation. The New Phytologist, 179, 784–798.

    Article  PubMed  Google Scholar 

  • Kurisu, G., Zhang, H.-m., Smith, J. L., & Cramer, W. A. (2003). Structure of the cytochrome b6f complex of oxygenic photosynthesis: Tuning the cavity. Science, 302, 1009–1114.

    Article  CAS  PubMed  Google Scholar 

  • Kustka, A., Carpenter, E. J., & Sanudo-Wilhelmy, S. A. (2002). Iron and marine nitrogen fxation: Progress and future directions. Research in Microbiology, 153, 255–262.

    Article  CAS  PubMed  Google Scholar 

  • Kustka, A. B., Saňudo-Wilhelmy, S. A., & Carpenter, E. J. (2003). Iron requirement for dinitrogen and ammonium-supported growth in cultures of Trichodesmium (IMI 101): Comparison with nitrogen fixation rate and iron: Carbon ratios of field populations. Limnology and Oceanography, 48, 1869–1884.

    Article  CAS  Google Scholar 

  • Lamb, J. J., Hill, R. E., Eaton-Rye, J. J., & Hohmann-Marriott, M. F. (2014). Functional role of pila in iron acquisition in the cyanobacterium Synechocystis sp. PCC 6803. PLOS ONE, 9.

    Google Scholar 

  • Landry, M. R., Constantinou, J., Latasa, M., Brown, S. L., Bidigare, R. R., & Ondrusek, M. E. (2000). Biological response to iron fertilization in the eastern equatorial Pacific (IronEx II). III.Dynamics of phytoplankton growth and microzooplankton grazing. Marine Ecology Progress Series, 201, 57–72.

    Article  CAS  Google Scholar 

  • Lane, N. (2010). First breath: Earth’s billion-year struggle for oxygen. New Science, 36–39.

    Google Scholar 

  • Latifi, A., Jeanjean, R., Lemeille, S., Havaux, M., & Zhang, C. C. (2005). Iron starvation leads to oxidative stress in Anabaena sp. Strain PCC 7120. Journal of Bacteriology, 187, 6596–6598.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, J. W., & Helmann, J. D. (2007). Functional specialization within the Fur family of metalloregulators[J]. Biometals, 20, 485.

    Article  CAS  PubMed  Google Scholar 

  • Leynaert, A., Bucciarelli, E., Claquin, P., Dugdale, R. C., Martin-Jézéquel, V., Pondaven, P., & Ragueneau, O. (2004). Effect of iron deficiency on diatom cell size and silicic acid uptake kinetics. Limnology and Oceanography, 49, 1134–1143.

    Article  CAS  Google Scholar 

  • Li, T., Huang, X., Zhou, R., Liu, Y., Li, B., Nomura, C., & Zhao, J. (2002). Differential expression and localization of Mn and Fe superoxide dismutases in the heterocystous cyanobacterium Anabaena sp. strain PCC 7120. Journal of Bacteriology, 184, 5096–5103.

    Article  CAS  PubMed  PubMed Central  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[J]. Journal of Bacteriology, 186, 3331–3345.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, Z. K., Dai, G. Z., Juneau, P., Qiu, B. S., & Post, A. (2016). Capsular polysaccharides facilitate enhanced iron acquisition by the colonial cyanobacterium Microcystis sp. isolated from a freshwater lake. Journal of Phycology, 52(1), 105–115.

    Google Scholar 

  • Liberton, M., Berg, R. H., Heuser, J., Roth, R., & Pakrasi, H. B. (2006). Ultrastructure of the membrane systems in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. Protoplasma, 227, 129–138.

    Article  PubMed  Google Scholar 

  • Lis, H., Kranzler, C., Keren, N., & Shaked, Y. (2015). A comparative study of iron uptake rates and mechanisms amongst marine and fresh water cyanobacteria: Prevalence of reductive iron uptake. Life, 5(1), 841–860.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lodeyro, A. F., Ceccoli, R. D., Karlusich, J. J. P., & Carrillo, N. (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.

    Article  CAS  PubMed  Google Scholar 

  • López-Gomollón, S., Hernández, J. A., Wolk, C. P., Peleato, M. L., & Fillat, M. F. (2007). Expression of furA is modulated by NtcA and strongly enhanced in heterocysts of Anabaena sp. PCC 7120. Microbiology, 153, 42–50.

    Article  PubMed  CAS  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[J]. Frontiers in Microbiology, 6, 1217.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahowald, N. M., Baker, A. R., Bergametti, G., Brooks, N., Duce, R. A., Jickells, T. D., et al. (2015). Atmospheric global dust cycle and iron inputs to the ocean. Global Biogeochemical Cycles, 19, 1–15.

    Google Scholar 

  • Marlovits, T. C., Haase, W., Herrmann, C., Aller, S. G., & Unger, V. M. (2002). The membrane protein FeoB contains an intramolecular G protein essential for Fe(II) uptake in bacteria. Proceedings of the National Academy of Sciences of the United States of America, 99, 16243–16248.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin, J. H. (1990). Glacial interglacial CO2 change: The iron hypothesis. Paleoceanography, 5, 12–13.

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Martinez, A., & Kolter, R. (1997). Protection of DNA during oxidative stress by the non-specific DNA- binding protein Dps. Journal of Bacteriology, 179, 5188–5194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin-Luna, B., Hernandez, J. A., Bes, M. T., Fillat, M. F., & Peleato, M. L. (2006). Identification of a Ferric uptake regulator from Microcystis aeruginosa PCC 7806. FEMS Microbiology Letters, 254, 63–70.

    Article  CAS  PubMed  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, 120, 36–50.

    Article  CAS  PubMed  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, 2635–2645.

    Article  CAS  PubMed  Google Scholar 

  • Michel, K. P., Exss-Sonne, P., Scholten-Beck, G., Kahmann, U., Ruppel, H. G., & Pistorius, E. K. (1998). Immunocytochemical localization of IdiA, a protein expressed under iron or manganese limitation in the mesophilic cyanobacterium Synechococcus PCC 6301and the thermophilic cyanobacterium Synechococcus elongatus. Planta, 205, 73–81.

    Article  CAS  PubMed  Google Scholar 

  • Michel, K.-P., Berry, S., Hifney, A., & Kruip, J. (2003). 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.

    Article  CAS  PubMed  Google Scholar 

  • Miethke, M., & Marahiel, M. A. (2007). Siderophore-based iron acquisition and pathogen control. Microbiology and Molecular Biology Reviews, 71, 413–451.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mikheyskaya, L. V., Ovodova, R. G., & Ovodova, Y. S. (1977). Isolation and characterization of lipopolysaccharides from cell walls of blue-green algae of the genus Phormidium. Journal of Bacteriology, 130, 1–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller, G. W., Denney, A., Pushnik, J., & Yu, M.-H. (1982). The formation of delta-aminolevulinate, a precursor of chlorophyll, in barley and the role of iron. Journal of Plant Nutrition, 5, 289–300.

    Article  CAS  Google Scholar 

  • Moeck, G. S., & Coulton, J. W. (1998). TonB-dependent iron acquisition: mechanisms of siderophore-mediated active transport. Molecular Microbiology, 28(4), 675–81

    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.

    Article  CAS  Google Scholar 

  • Morrissey, J., & Bowler, C. (2012). Iron utilization in marine cyanobacteria and eukaryotic algae. Frontiers in Microbiology, 3, 43.

    Article  PubMed  PubMed Central  Google Scholar 

  • Müller, G., Isowa, Y., & Raymond, K. N. (1985). Stereospecificity of siderophore-mediated iron uptake in Rhodotorula pilimanae as probed by Enantiorhodotoruli acid and isomers of chromic Rhodotorulate. The Journal of Biological Chemistry, 260, 13921–13926.

    Article  PubMed  Google Scholar 

  • Myers, J. (1987). Is there significant cyclic electron flow around photosystem I in cyanobacteria. Photosynthesis Research, 14, 55–69.

    Article  CAS  PubMed  Google Scholar 

  • Nicolaisen, K., & Schleiff, E. (2010). Iron dependency of and transport by cyanobacteria. In S. Andrews & P. Cornelis (Eds.), Iron uptake in microorganisms (pp. 203–229). Norfolk: Caister Academic Press.

    Google Scholar 

  • Nicolaisen, K., Moslavac, S., Samborski, A., Valdebenito, M., Hantke, K., Maldener, I., et al. (2008). Alr0397 is an outer membrane transporter for the siderophore schizokinen in Anabaena sp. strain PCC 7120. Journal of Bacteriology, 190(22), 7500–7507.

    Google Scholar 

  • Nield, J., Morris, E. P., Bibby, T. S., & Barber, J. (2003). Structural analysis of the photosystem I supercomplex of cyanobacteria induced by iron deficiency. Biochemistry, 42, 3180–3188.

    Article  CAS  PubMed  Google Scholar 

  • Nishioka, J., Takeda, S., Wong, C. S., & Johnson, W. K. (2001). Size-fractionated iron concentrations in the Northeast Pacific Ocean: Distribution of soluble and small colloidal iron. Marine Chemistry, 74, 157–179.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ovescostales, D., Kadi, N., & Challis, G. L. (2009). The long-overlooked enzymology of a nonribosomal peptide synthetase-independent pathway for virulence-conferring siderophore biosynthesis. ChemInform, 41, 6530–6541.

    Google Scholar 

  • Oliveira, P., Martins, N. M., Santos, M., Pinto, F., Büttel, Z., Couto, N. A. S., et al. (2016). The versatile tolc-like slr1270 in the cyanobacterium Synechocystis sp. PCC 6803. Environmental Microbiology, 18.

    Google Scholar 

  • Palenik, B., Brahamsha, B., Larimer, F. W., Land, M., Hauser, L., Chain, P., Lamerdin, J., Regala, W., Allen, E. E., McCarren, J., Paulsen, I., Dufresne, A., Partensky, F., Webb, E. A., & Waterbury, J. (2003). The genome of a motile marine Synechococcus. Nature, 424, 1037–1042.

    Article  CAS  PubMed  Google Scholar 

  • Palenik, B., Ren, Q., Dupont, C. L., Myers, G. S., Heidelberg, J. F., Badger, J. H., et al. (2006). Genome sequence of Synechococcus PCC 9311: Insights into adaptation to a coastal environment. Proceedings of the National Academy of Sciences of the United States of America, 103, 13555–13559.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parent, A., Caux-Thang, C., Signor, L., et al. (2013). Single glutamate to aspartate mutation makes ferric uptake regulator (Fur) as sensitive to H2O2 as peroxide resistance regulator (PerR)[J]. Angewandte Chemie, 125, 10529–10533.

    Google Scholar 

  • Parker, D. L., Mihalick, J. E., Plude, J. L., Plude, M. J., Clark, T. P., Egan, L., et al. (2000). Sorption of metals by extracellular polymers from the cyanobacterium Microcystis aeruginosa fo. flos-aquae strain c3-40. Journal of Applied Phycology, 12, 219–224.

    Google Scholar 

  • Passow, U. (2002). Transparent exopolymer particles (TEP) in aquatic environments. Progress in Oceanography, 55, 287–333.

    Article  Google Scholar 

  • Pils, D., & Schmetterer, G. (2001). Characterization of three bioenergetically active respiratory terminal oxidases in the cyanobacterium Synechocystis sp strain PCC 6803. FEMS Microbiology Letters, 203, 217–222.

    Article  CAS  PubMed  Google Scholar 

  • Pospisil, P., Arato, A., & Krieger-Liszkay, A. (2004). Hydroxyl radical generation by photosystem II. Biochemistry, 43, 6783–6792.

    Article  CAS  PubMed  Google Scholar 

  • Qiu, G. W., Lou, W. J., Sun, C. Y., Yang, N., & Qiu, B. S. (2018). Characterization of outer membrane iron uptake pathways in the model cyanobacterium Synechocystis sp. PCC 6803. Applied and Environmental Microbiology, 84(19), AEM.01512-18.

    Google Scholar 

  • Raven, J. A. (1988). The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. The New Phytologist, 109, 279–287.

    Article  CAS  Google Scholar 

  • Raven, J. A. (1990). Predictions of Mn and Fe use efficiencies of phototrophic growth as a function of light availability for growth and of C assimilation pathway. The New Phytologist, 116, 1–18.

    Article  CAS  Google Scholar 

  • Raven, J. A. (1999). The size of cells and organisms in relation to the evolution of embryophytes. Plant Biology, 1, 2–12.

    Article  Google Scholar 

  • Raven, J. A., & Richard, J. G. (1988). Temperature and Algal Growth. The New Phytologist, 110, 411–461.

    Article  Google Scholar 

  • Raven, J. A., Evans, M. C., & Korb, R. E. (1999). The role of trace metals in photosynthetic electron transport in O2-evolving organism. Photosynthesis Research, 60, 111–150.

    Article  CAS  Google Scholar 

  • Regelsberger, G., Laaha, U., Dietmann, D., Rüker, F., Grilli-Caiola, A. C. M., Furtmuüller, P. G., Jakopitsch, C., Peschek, G. A., & Obinger, C. (2004). The iron superoxide dismutase from the filamentous cyanobacterium nostoc PCC 7120. The Journal of Biological Chemistry, 279, 44384–44393.

    Article  CAS  PubMed  Google Scholar 

  • Ren, X. X., Jiang, H., Leng, X., & An, S. Q. (2013). Ecological significance and industrial application of extracellular polysaccharides from cyanobacteria: A review. Chinese Journal of Ecology, 291, 428–435.

    Google Scholar 

  • Řezanka, T., Palyzová, A., & Sigler, K. (2018). Isolation and identification of siderophores produced by cyanobacteria. Folia Microbiologica, 63(5), 569–579.

    Article  PubMed  CAS  Google Scholar 

  • Rivers, A. R. (2009). Iron limitation and the role of siderophores in marine Synechococcus. New College of Florida. Papper for the degree of Doctor. pp. 3.

    Google Scholar 

  • Rocap, G. (2003). Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature, 424, 1042–1047.

    Article  CAS  PubMed  Google Scholar 

  • Romheld, V., & Marschner, H. (1983). Mechanism of iron uptake by peanut plants: I. Fe reduction, chelate splitting, and release of phenolics. Plant Physiology, 71, 949–954.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rose, A. L., Salmon, T. P., Lukondeh, T., Neilan, B., & Waite, T. D. (2005). Use of superoxide as an electron shuttle for iron acquisition by the marine cyanobacterium Lyngbya majuscule. Environmental Science & Technology, 39, 3708–3715.

    Google Scholar 

  • Roy, E. G., Wells, M. L., & King, D. W. (2008). Persistence of iron(II) in surface waters of the western subarctic Pacific. Limnology and Oceanography, 53, 89–98.

    Article  CAS  Google Scholar 

  • Rusch, D. B., Martiny, A. C., Dupont, C. L., & Venter, A. L. H. C. (2010). Characterization of prochlorococcus clades from iron-depleted oceanic regions. Proceedings of the National Academy of Sciences of the United States of America, 107, 16184–16189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rubin, M., Bermanfrank, I., & Shaked, Y. (2011). Dust- and mineral-iron utilization by the marine dinitrogen-fixer Trichodesmium. Nature Geoscience, 4, 529–534.

    Google Scholar 

  • Rudolf, M., Kranzler, C., Lis, H., Margulis, K., Stevanovic, M., Keren, N., & Schleiff, E. (2015). Multiple modes of iron uptake by the filamentous, siderophore producing cyanobacterium, Anabaena sp. PCC 7120. Molecular Microbiology.

    Google Scholar 

  • Ryan-Keogh, T. J., Macey, A. I., Cockshutt, A. M., Moore, C. M., & Bibby, T. S. (2012). The cyanobacterial chlorophyll-binding-protein IsiA acts to increase the in vivo effective absorption cross-section of PSI under iron limitation. Journal of Phycology, 48, 145–154.

    Article  CAS  PubMed  Google Scholar 

  • Saha, M., Sarkar, S., Sarkar, B., Sharma, B. K., Bhattacharjee, S., & Tribedi, P. (2016). Microbial siderophores and their potential applications: A review. Environmental Science and Pollution Research, 23, 3984–3999.

    Article  CAS  PubMed  Google Scholar 

  • Saito, M. A., Bertrand, E. M., Dutkiewicz, S., Bulygin, V. V., Moran, D. M., Monteiro, F. M., Follows, M. J., Valois, F. W., & Waterbury, J. B. (2011). Iron conservation by reduction of metal-loenzyme inventories in the marine diazotroph Crocosphaera watsonii. Proceedings of the National Academy of Sciences of the United States of America, 108, 2184–2189.

    Google Scholar 

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

    Article  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saňudo-Wilhelmy, S. A., Kustka, A. B., Gobler, C. J., Hutchins, D. A., Yang, M., Lwiza, K., Burns, J., Capone, D. G., Ravenk, J. A., & Carpenter, E. J. (2001). Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature, 411, 66–69.

    Article  PubMed  Google Scholar 

  • Schmidt, W., Drews, G., Weckesser, J., Fromme, J., & Borowiak, D. (1980). Characterization of the lipopolysaccharides from eight Synechococcus strains. Archives of Microbiology, 127, 217–222.

    Article  CAS  Google Scholar 

  • Schneider, D., Berry, S., Volkmer, T., Seidler, A., & Rogner, M. (2004). PetC1 is the major rieske iron-sulfur protein in the cytochrome b6f complex of Synechocystis sp. PCC 6803. The Journal of Biological Chemistry, 279, 39383–39388.

    Article  CAS  PubMed  Google Scholar 

  • Schopf, J. W. (2012). Springer Netherlands the fossil record of cyanobacteria. In B. A. Whitton & B. A. Whitton (Eds.), Ecology of cyanobacteria II (pp. 15–36). Dordrecht: Springer.

    Chapter  Google Scholar 

  • Schrader, M., Drews, G., & Weckesser, J. (1981). Chemical analyses on cell wall constituents of the thermophilic cyanobacterium Synechococcus PCC 6716. FEMS Microbiology Letters, 11, 37–40.

    Article  CAS  Google Scholar 

  • Schuergers, N., & Wilde, A. (2015). Appendages of the cyanobacterial cell. Life, 5, 700–715.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sen, A., Dwivedi, K., Rice, K. A., & Bullerjahn, G. S. (2000). Growth phase and metal-dependent regulation of the dpsa gene in Synechococcus sp. strain PCC 7942. Archives of Microbiology, 173, 352–357.

    Google Scholar 

  • Shaked, Y., & Lis, H. (2012). Disassembling iron availability to phytoplankton. Frontiers in Microbiology, 3, 1–25.

    Article  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shcolnick, S., Summerfield, T. C., Reytman, L., Sherman, L. A., & Keren, N. (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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi, D., Xu, Y., Hopkinson, B. M., & Morel, F. M. M. (2010). Effect of ocean acidification on iron availability to marine phytoplankton. Science, 327, 676–679.

    Article  CAS  PubMed  Google Scholar 

  • Shih, P. M., Wu, D., Latifi, A., Axen, S. D., Fewer, D. P., Talla, E., et al. (2013). Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proceedings of the National Academy of Sciences, 110, 1053–1058.

    Article  CAS  Google Scholar 

  • Simpson, F. B., & Neilands, J. B. (1976). Siderochromes in cyanophyceae: isolation and characterization of schizokinen from Anabaena sp. 1. Journal of Phycology, 12, 44–48.

    Article  Google Scholar 

  • Singh, A. K., & Sherman, L. A. (2006). Iron-independent dynamics of IsiA production during the transition to stationary phase in the cyanobacterium Synechocystis sp. PCC 6803. EMS Microbiol Letters, 256, 159–164.

    Article  CAS  Google Scholar 

  • Singh, A. K., McIntyre, L. M., & Sherman, L. A. (2003). Microarray analysis of the genome-wide response to iron deficiency and iron reconstitution in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiology, 132, 1825–1839.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh, A. K., Li, H., & Sherman, L. A. (2004). Microarray analysis and redox control of gene expression in the cyanobacterium Synechocystis sp. PCC 6803. Physiologia Plantarum, 120, 27–35.

    Article  CAS  PubMed  Google Scholar 

  • Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., et al. (2007). Climate change 2007: The physical science basis: Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. New York: Cambridge University Press.

    Google Scholar 

  • Stockel, J., Welsh, E. A., Liberton, M., Kunnvakkam, R., Aurora, R., & Pakrasi, H. B. (2008). Global transcriptomic analysis of Cyanothece 51142 reveals robust diurnal oscillation of central metabolic processes. Proceedings of the National Academy of Sciences of the United States of America, 105, 6156–6161.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stroebel, D., Choquet, Y., Popot, J.-L., & Picot, D. (2003). An atypical haem in the cytochrome b6f complex. Nature, 426, 413–418.

    Article  CAS  PubMed  Google Scholar 

  • Stumm, W., & Sulzberger, B. (1992). The cycling of iron in natural environments: Considerations based on laboratory studies of heterogeneous redox processes. Geochimica et Cosmochimica Acta, 56, 3233–3257.

    Article  CAS  Google Scholar 

  • Sunda, W. G. (2001). Bioavailability and bioaccumulation of iron in the sea. In K. Hunter & D. Turner (Eds.), Biogeochemistry of Fe in seawater (pp. 41–84). West Sussex: Wiley.

    Google Scholar 

  • Sunda, W. G., & Huntsman, S. A. (1997). Interrelated influence of iron, light and cell size on marine phytoplankton growth. Nature, 390, 389–392.

    Article  CAS  Google Scholar 

  • Tagliabue, A., Bowie, A. R., Boyd, P. W., Buck, K. N., Johnson, K. S., & Saito, M. A. (2017). The integral role of iron in ocean biogeochemistry. Nature, 543, 51–59.

    Article  CAS  PubMed  Google Scholar 

  • Teresa, B. M., Hernández, J. A., Luisa, P. M., 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.

    Google Scholar 

  • Terry, N., & Low, G. (1982). Leaf chlorophyll content and its relation to the intracellular location of iron. Journal of Plant Nutrition, 5, 301–310.

    Article  CAS  Google Scholar 

  • Tichy, M., & Vermaas, W. (1999). In vivo role of catalase-peroxidase in Synechocystis sp. strain PCC 6803. Journal of Bacteriology, 181, 1875–1882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tölle, J., Michel, K. P., Kruip, J., Kahmann, U., Preisfeld, A., & Pistorius, E. K. (2002). Localization and function of the IdiA homologue Slr1295 in the cyanobacterium Synechocystis sp. strain PCC 6803. Microbiology, 148, 3293–3305.

    Article  PubMed  Google Scholar 

  • Toulzal, E., Tagliabue, A., Blain, S., & Piganeau, G. (2012). Analysis of the Global Ocean Sampling (GOS) project for trends in iron uptake by surface ocean microbes. PLoS One, 7(2), e30931.

    Article  CAS  Google Scholar 

  • Tronnet, S., Garcie, C., Brachmann, A. O., et al. (2017). High iron supply inhibits the synthesis of the genotoxin colibactin by pathogenic Escherichia coli through a non-canonical Fur/RyhB-mediated pathway[J]. Pathogens and Disease, 75, ftx066.74.

    Article  CAS  Google Scholar 

  • Trujillo, A. (2011). The iron hypothesis. http://www.homepages.ed.ac.uk/shs/Climatechange/Carbon%20sequestration/Martin%20iron.htm

  • Tuit, C., Waterbury, J., & Ravizza, G. (2004). Diel variation of molybdenum and iron in marine diazotrophic cyanobacteria. Limnology and Oceanography, 49, 978–990.

    Article  CAS  Google Scholar 

  • Vassiliev, L. R., Kolber, Z., Wyman, K. D., Mauzerall, D., Shukla, V. K., & Falkowsk, P. C. (1995). Effects of iron limitation on photosystem II composition and light utilization in Dunaliella tertiolecta. Plant Physiology, 109, 963–972.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Velayudhan, J., Hughes, N. J., Mccolm, A. A., Bagshaw, J., Clayton, C. L., Andrews, S. C., et al. (2000). Iron acquisition and virulence in Helicobacter pylori: A major role for FeoB, a high-affinity ferrous iron transporter. Molecular Microbiology, 37, 274–286.

    Article  CAS  PubMed  Google Scholar 

  • Vermaas, W. F. (2001). Photosynthesis an respiration in cyanobacteria (Encyclopedia of Life Sciences, pp. 1–7). London: Nature Publishing Group.

    Google Scholar 

  • Violaine, J., Céline, R., Stéphane, L.’. H., Fanny, K., Alain, S., & Andrew, C. D. (2014). Response of the unicellular diazotrophic cyanobacterium crocosphaera watsonii to iron limitation. PLoS ONE, 9(1), e86749.

    Article  CAS  Google Scholar 

  • Volk, T., & Hoffert, M. I. (1985). In the carbon cycle and atmospheric CO2: Natural variations Archean to present. American Geophysical Union, 32, 99–110.

    Google Scholar 

  • Wandersman, C., & Delepelaire, P. (2004). Bacterial iron sources: From siderophores to hemophores[J]. Annual Review of Microbiology, 58, 611.

    Article  CAS  PubMed  Google Scholar 

  • Westberry, T. K., & Siegel, D. A. (2006). Spatial and temporal distribution of Trichodesmium blooms in the worlds oceans. Global Biogeochemical Cycles, 20.

    Google Scholar 

  • Wilson, A., Boulay, C., Wilde, A., Kerfeld, C. A., & Kirilovsky, D. (2007). Light-induced energy dissipation in Iron-starved cyanobacteria: Roles of OCP and IsiA proteins. Plant Cell, 19, 656–672.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolf, S. G., Frenkiel, D., Arad, T., Finkel, S. E., Kolter, R., & Minsky, A. (1999). DNA protection by stress-induced biocrystallization. Nature, 400, 83–85.

    Article  CAS  PubMed  Google Scholar 

  • Wotton, R. S. (2004). The ubiquity and many roles of exopolymers (EPS) in aquatic systems. Scientia Marina, 68, 13–21.

    Article  CAS  Google Scholar 

  • Wu, J. F., Boyle, E., Sunda, W., & Wen, L. S. (2001). Soluble and colloidal iron in the oligotrophic North Atlantic and North Pacific. Science, 293, 847–849.

    Article  CAS  PubMed  Google Scholar 

  • Xing, W., Huang, W. M., Li, D. H., & Liu, Y. D. (2007). Effects of iron on growth, pigment content, photosystem II efficiency, and siderophores production of Microcystis aeruginosa and Microcystis wesenbergii. Current Microbiology, 55, 94–98.

    Google Scholar 

  • Xu, D., Liu, X., Zhao, J., & Zhao, J. (2005). FesM, a membrane iron-sulfur protein, is required for cyclic electron flow around Photosystem I and photoheterotrophic growth of the cyanobacterium Synechococcus sp. PCC 7002. Plant Physiology, 138, 1586–1595.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu, N., Qiu, G. W., Lou, W. J., Li, Z. K., Jiang, H. B., Price, N. M., et al. (2016). Identification of an iron permease, cftr1, in cyanobacteria involved in the iron reduction/re-oxidation uptake pathway. Environmental Microbiology., 18, 5005–5017.

    Article  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.

    Article  CAS  PubMed  Google Scholar 

  • Yoshida, M., Kuma, K., Iwade, S., Isoda, Y., Takata, H., & Yamada, M. (2006). Effect of aging time on the availability of freshly precipitated ferric hydroxide to coastal marine diatoms. Marine Biology, 149, 379–392.

    Article  CAS  Google Scholar 

  • Yoshihara, S., Geng, X. X., Okamoto, S., Yura, K., Murata, T., Go, M., Ohmori, M., & Ikeuchi, M. (2001). Mutational analysis of genes involved in pilus structure, motility and transformation competency in the unicellular motile cyanobacterium Synechocystis sp. PCC 6803. Plant and Cell Physiology, 42, 63–73.

    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.

    Article  CAS  PubMed  Google Scholar 

  • Yu, L., Zhao, J., Muhlenhoff, U., Bryant, D. A., & Golbeck, J. H. (1993). PsaE is required for in vivo cyclic electron flow around photosystem I in the cyanobacterium Synechococcus sp. PCC 7002. Plant Physiology, 103, 171–180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zouni, A., Witt, H. T., Kern, J., Fromme, P., Krauss, N., Saenger, W., & Orth, P. (2001). Crystal structure of photosystem II from Synechococcus elongatus at 3.8 A resolution. Nature, 409, 739–743.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hai-Bo Jiang .

Editor information

Editors and Affiliations

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

Jiang, HB., Lu, XH., Deng, B., Liu, LM., Qiu, BS. (2020). Adaptive Mechanisms of the Model Photosynthetic Organisms, Cyanobacteria, to Iron Deficiency. In: Wang, Q. (eds) Microbial Photosynthesis. Springer, Singapore. https://doi.org/10.1007/978-981-15-3110-1_11

Download citation

Publish with us

Policies and ethics