Skip to main content
SpringerLink
Log in

Iron

  • Chapter
  • First Online:
The Physiology of Microalgae

Part of the book series: Developments in Applied Phycology ((DAPH,volume 6))

Abstract

Iron is essential for algal growth, metabolism and function. Numerous proteins and enzymes require iron, including those involved in photosynthesis, respiration, as well as nitrogen assimilation and fixation. A variety of sources and sinks of iron in marine and freshwater ecosystems lead to a wide range of dissolved iron concentrations, from iron-limiting to iron-replete, for microalgal growth. Decades of physiological and molecular research, in combination with recent genomic advances, have made way for breakthroughs in our understanding of the critical roles iron plays in microalgal metabolism and how iron is acquired in aqueous environments. Herein, we review and integrate these studies to compare and contrast the iron requirements, acquisition abilities and strategies, as well as storage capacities of microalgae, with a particular emphasis on diatoms, green algae and cyanobacteria. These include the ability to perform substitution or the permanent replacement of iron-requiring proteins for non-iron containing functional equivalents, the presence of a high-affinity uptake system and the capacity to store iron in excess of cellular demand. We also include a discussion of iron-related topics of current significance, including iron-light co-limitation, effects of iron limitation on cellular elemental composition, large-scale iron fertilization experiments, and climate change effects on iron bioavailability. Lastly, a brief overview of some common laboratory and field techniques employed to study microalgal iron physiology is provided.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
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

Notes

  1. 1.

    Wherever possible the currently accepted names for species are used. The name used in the paper cited is also indicated. For details of names see chapter “Systematics, Taxonomy and Species Names: Do They Matter?” of this book (Borowitzka 2016).

References

  • Allen MD, del Campo JA, Kropat J, Merchant SS (2007) FEA1, FEA2, and FRE1, encoding two homologous secreted proteins and a candidate ferrireductase, are expressed coordinately with FOX1 and FTR1 in iron-deficient Chlamydomonas reinhardtii. Eukaryot Cell 6:1841–1852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allen A, LaRoche J, Maheswari U, Lommer M, Schauer N, Lopez P, Finazzi G, Fernie A, Bowler C (2008) Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc Natl Acad Sci 105:10438–10443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allnutt FCT, Bonner WD Jr (1987a) Characterization of iron uptake from ferrioxamine B by Chlorella vulgaris. Plant Physiol 85:746–750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allnutt FCT, Bonner WD (1987b) Evaluation of reductive release as a mechanism for iron uptake from ferrioxamine B by Chlorella vulgaris. Plant Physiol 85:751–756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anbar AD, Knoll AH (2002) Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297:1137–1142

    Article  CAS  PubMed  Google Scholar 

  • Andersen RA (1992) Diversity of eukaryotic algae. Biodivers Conserv 1:267–292

    Article  Google Scholar 

  • Anderson MA, Morel FMM (1982) The influence of aqueous iron chemistry on the uptake of iron by the coastal diatom Thalassiosira weissflogii. Limnol Oceanogr 27:789–813

    Article  CAS  Google Scholar 

  • Annett AL, Lapi S, Ruth TJ, Maldonado MT (2008) The effects of Cu and Fe availability on the growth and Cu: C ratios of marine diatoms. Limnol Oceanogr 53:2451–2461

    Article  CAS  Google Scholar 

  • Armbrust E (2009) The life of diatoms in the world’s oceans. Nature 459:185–192

    Article  CAS  PubMed  Google Scholar 

  • Askwith CC, de Silva D, Kaplan J (1996) Molecular biology of iron acquisition in Saccharomyces cerevisiae. Mol Microbiol 20:27–34

    Article  CAS  PubMed  Google Scholar 

  • Assmy P, Smetacek V, Montresor M, Klaas C, Henjes J, Strass VH, Arrieta JM, Bathmann U, Berg GM, Breitbarth E, Cisewski B, Friedrichs L, Fuchs N, Herndl GJ, Jansen S, Kragefsky S, Latasa M, Peeken I, Rottgers R, Scharek R, Schuller SE, Steigenberger S, Webb A, Wolf-Gladrow D (2013) Thick-shelled, grazer-protected diatoms decouple ocean carbon and silicon cycles in the iron-limited Antarctic Circumpolar Current. Proc Natl Acad Sci 110:20633–20638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baines SB, Twining BS, Vogt S, Balch WM, Fisher NS, Nelson DM (2011) Elemental composition of equatorial Pacific diatoms exposed to additions of silicic acid and iron. Deep Sea Res II 58:512–523

    Article  CAS  Google Scholar 

  • Banse K (1991) Iron availability, nitrate uptake, and exportable new production in the Subarctic Pacific. J Geophys Res Oceans 96:741–748

    Article  Google Scholar 

  • Barbeau K, Rue EL, Bruland KW, 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 

  • Barbeau K, Rue EL, Trick CG, Bruland KT, Butler A (2003) Photochemical reactivity of siderophores produced by marine heterotrophic bacteria and cyanobacteria based on characteristic Fe(III) binding groups. Limnol Oceanogr 48:1069–1078

    Article  CAS  Google Scholar 

  • Behrenfeld MJ, Milligan AJ (2013) Photophysiological expressions of iron stress in phytoplankton. Ann Rev Mar Sci 5:217–246

    Article  PubMed  Google Scholar 

  • Behrenfeld MJ, Worthington K, Sherrell RM, Chavez FP, Strutton P, McPhaden M, Shea DM (2006) Controls on tropical Pacific Ocean productivity revealed through nutrient stress diagnostics. Nature 442:1025–1028

    Article  CAS  PubMed  Google Scholar 

  • Behrenfeld MJ, Westberry TK, Boss ES, O’Malley RT, Siegel DA, Wiggert JD, Franz BA, McClain CR, Feldman GC, Doney SC, Moore JK, Dall’Olmo G, Milligan AJ, Lima I, Mahowald N (2009) Satellite-detected fluorescence reveals global physiology of ocean phytoplankton. Biogeosciences 6:779–794

    Article  Google Scholar 

  • Beiderbeck H, Taraz K, Budzikiewicz H, Walsby AE (2000) Anachelin, the siderophore of the cyanobacterium Anabaena cylindrica CCAP 1403/2A. Zeitschr Naturf C 55:681–687

    CAS  Google Scholar 

  • Beja O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP, Jovanovich S, Gates CM, Feldman RA, Spudich JL, Spudich EN, DeLong EF (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289:1902–1906

    Article  CAS  PubMed  Google Scholar 

  • Berman-Frank I, Quigg A, Finkel ZV, Irwin AJ, Haramaty L (2007) Nitrogen-fixation strategies and Fe requirements in cyanobacteria. Limnol Oceanogr 52:2260–2269

    Article  Google Scholar 

  • Bertrand EM, Saito MA, Rose JM, Riesselman CR, Lohan MC, Noble AE, Lee PA, DiTullio GR (2007) Vitamin B12 and iron colimitation of phytoplankton growth in the Ross Sea. Limnol Oceanogr 52:1079–1093

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Blaby-Haas CE, Merchant SS (2012) The ins and outs of algal metal transport. Biochim Biophys Acta-Mol Cell Res 1823:1531–1552

    Article  CAS  Google Scholar 

  • Blain S, Sedwick PN, Griffiths FB, Queguiner B, Bucciarelli E, Fiala M, Pondaven P, Treguer P (2002) Quantification of algal iron requirements in the Subantarctic Southern Ocean (Indian sector). Deep-Sea Res II 49:3255–3273

    Article  CAS  Google Scholar 

  • Blain S, Queguiner B, Armand L, Belviso S, Bombled B, Bopp L, Bowie A, Brunet C, Brussaard C, Carlotti F, Christaki U, Corbiere A, Durand I, Ebersbach F, Fuda JL, Garcia N, Gerringa L, Griffiths B, Guigue C, Guillerm C, Jacquet S, Jeandel C, Laan P, Lefevre D, Lo Monaco C, Malits A, Mosseri J, Obernosterer I, Park YH, Picheral M, Pondaven P, Remenyi T, Sandroni V, Sarthou G, Savoye N, Scouarnec L, Souhaut M, Thuiller D, Timmermans K, Trull T, Uitz J, van Beek P, Veldhuis M, Vincent D, Viollier E, Vong L, Wagener T (2007) Effect of natural iron fertilization on carbon sequestration in the Southern Ocean. Nature 446:1070–U1071

    Article  CAS  PubMed  Google Scholar 

  • Bleuel C, Grosse C, Taudte N, Scherer J, Wesenberg D, Krauss GJ, Nies DH, Grass G (2005) TolC is involved in enterobactin efflux across the outer membrane of Escherichia coli. J Bacteriol 187:6701–6707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Borowitzka MA (2016) Systematics, taxonomy and species names: do they matter? In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 655–681

    Google Scholar 

  • Boukhalfa H, Crumbliss AL (2002) Chemical aspects of siderophore mediated iron transport. Biometals 15:325–339

    Article  CAS  PubMed  Google Scholar 

  • Boyd PW, Jickells T, Law CS, Blain S, Boyle EA, Buesseler KO, Coale KH, Cullen JJ, de Baar HJW, Follows M, Harvey M, Lancelot C, Levasseur M, Owens NPJ, Pollard R, Rivkin RB, Sarmiento J, Schoemann V, Smetacek V, Takeda S, Tsuda A, Turner S, Watson AJ (2007) Mesoscale iron enrichment experiments 1993–2005: synthesis and future directions. Science 315:612–617

    Article  CAS  PubMed  Google Scholar 

  • Boyle E (1998) Pumping iron makes thinner diatoms. Nature 393:733–734

    Article  CAS  Google Scholar 

  • Boyle E, Edmond J, Sholkovitz E (1976) The mechanism of iron removal in estuaries. Geochim Cosmochim Acta 41:1313–1324

    Article  Google Scholar 

  • Breitbarth E, Bellerby RJ, Neill CC, Ardelan MV, Meyerhöfer M, Zöllner E, Croot PL, Riebesell U (2010) Ocean acidification affects iron speciation during a coastal seawater mesocosm experiment. Biogeosciences 7:1065–1073

    Article  CAS  Google Scholar 

  • Bruland KW, Orians KJ, Cowen JP (1994) Reactive trace metals in the stratified central North Pacific. Geochim Cosmochim Acta 58:3171–3182

    Article  CAS  Google Scholar 

  • Bruland KW, Lohan MC, Aguilar-Islas AM, Smith GJ, Sohst B, Baptista A (2008) Factors influencing the chemistry of the near-field Columbia River plume: nitrate, silicic acid, dissolved Fe, and dissolved Mn. J Geophys Res Oceans 113:C00B02. DOI:10.1029/2007JC004702

  • Bruland KW, Middag R, Lohan MC (2014) Controls of trace metals in seawater. In: Holland HD, Tureklan KK (eds) Treatise on geochemistry, vol 8, 2nd edn. Elsevier, Oxford, pp 19–51

    Chapter  Google Scholar 

  • Brzezinski MA, Baines SB, Balch WM, Beucher C, Chai F, Dugdale RC, Krause JW, Landry MR, Marchi A, Measures C, Nelson DM, Parker A, Poulton A, Selph KE, Strutton P, Taylor AG, Twining BS (2011) Co-limitation of diatoms by iron and silicic acid in the equatorial Pacific. Deep-Sea Res II:493–511

    Google Scholar 

  • Bucciarelli E, Pondaven P, Sarthou G (2010) Effects of an iron-light co-limitation on the elemental composition (Si, C, N) of the marine diatoms Thalassiosira oceanica and Ditylum brightwellii. Biogeosciences 7:657–669

    Article  CAS  Google Scholar 

  • Castruita M, Casero D, Karpowicz SJ, Kropat J, Vieler A, Hsieh SI, Yan W, Cokus S, Loo JA, Benning C (2011) Systems biology approach in Chlamydomonas reveals connections between copper nutrition and multiple metabolic steps. Plant Cell Online 23:1273–1292

    Article  CAS  Google Scholar 

  • Cellier MFM, Bergevin I, Boyer E, Richer E (2001) Polyphyletic origins of bacterial Nramp transporters. Trends Genet 17:365–370

    Article  CAS  PubMed  Google Scholar 

  • Chase Z, Strutton PG, Hales B (2007) Iron links river runoff and shelf width to phytoplankton biomass along the U.S. West Coast. Geophys Res Lett 34:L04607. DOI:10.1029/2006GL028069

  • Chauhan D, Folea IM, Jolley CC, Kouril R, Lubner CE, Lin S, Kolber D, Wolfe-Simon F, Golbeck JH, Boekema EJ (2011) A novel photosynthetic strategy for adaptation to low-iron aquatic environments. Biochemistry 50:686–692

    Article  CAS  PubMed  Google Scholar 

  • Chavez FP, Buck KR, Coale KH, Martin JH, Ditullio GR, Welschmeyer NA, Jacobson AC, Barber RT (1991) Growth-rates, grazing, sinking, and iron limitation of Equatorial Pacific phytoplankton. Limnol Oceanogr 36:1816–1833

    Article  CAS  Google Scholar 

  • Chimento DP, Kadner RJ, Wiener MC (2005) Comparative structural analysis of TonB-dependent outer membrane transporters: implications for the transport cycle. Proteins 59:240–251

    Article  CAS  PubMed  Google Scholar 

  • Coale KH, Fitzwater SE, Gordon RM, Johnson KS, Barber RT (1996) Control of community growth and export production by upwelled iron in the equatorial Pacific Ocean. Nature 379:621–624

    Article  CAS  Google Scholar 

  • Coale KH, Wang X, Tanner SJ, Johnson KS (2003) Phytoplankton growth and biological response to iron and zinc addition in the Ross Sea and Antarctic Circumpolar Current along 170 W. Deep Sea Res II 50:635–653

    Article  CAS  Google Scholar 

  • Coale KH, Johnson KS, Chavez FP, Buesseler KO, Barber RT, Brzezinski MA, Cochlan WP, Millero FJ, Falkowski PG, Bauer JE, Wanninkhof RH, Kudela RM, Altabet MA, Hales BE, Takahashi T, Landry MR, Bidigare RR, Wang XJ, Chase Z, Strutton PG, Friederich GE, Gorbunov MY, Lance VP, Hilting AK, Hiscock MR, Demarest M, Hiscock WT, Sullivan KF, Tanner SJ, Gordon RM, Hunter CN, Elrod VA, Fitzwater SE, Jones JL, Tozzi S, Koblizek M, Roberts AE, Herndon J, Brewster J, Ladizinsky N, Smith G, Cooper D, Timothy D, Brown SL, Selph KE, Sheridan CC, Twining BS, Johnson ZI (2004) Southern ocean iron enrichment experiment: carbon cycling in high- and low-Si waters. Science 304:408–414

    Article  CAS  PubMed  Google Scholar 

  • Cochlan WP, Bronk DA, Coale KH (2002) Trace metals and nitrogenous nutrition of Antarctic phytoplankton: experimental observations in the Ross Sea. Deep-Sea Res II 49:3365–3390

    Article  CAS  Google Scholar 

  • Conway TM, John SG (2014) Quantification of dissolved iron sources to the North Atlantic Ocean. Nature 511:212–215

    Article  CAS  PubMed  Google Scholar 

  • Crawford DW, Lipsen MS, Purdie DA, Lohan MC, Statham PJ, Whitney FA, Putland JN, Johnson WK, Sutherland N, Peterson TD, Harrison PJ, Wong CS (2003) Influence of zinc and iron enrichments on phytoplankton growth in the northeastern subarctic Pacific. Limnol Oceanogr 48:1583–1600

    Article  CAS  Google Scholar 

  • Cullen JJ (1991) Hypotheses to explain high-nutrient conditions in the open sea. Limnol Oceanogr 36:1578–1599

    Article  CAS  Google Scholar 

  • Cullen JT, Chase Z, Coale KH, Fitzwater SE, Sherrell RM (2003) Effect of iron limitation on the cadmium to phosphorus ratio of natural phytoplankton assemblages from the Southern Ocean. Limnol Oceanogr 48:1079–1087

    Article  CAS  Google Scholar 

  • Dang TC, Fujii M, Rose AL, Bligh M, Waite TD (2012) Characteristics of the freshwater cyanobacterium Microcystis aeruginosa grown in iron-limited continuous culture. Appl Environ Microbiol 78:1574–1583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Baar HJW, Boyd PW, Coale KH, Landry MR, Tsuda A, Assmy P, Bakker DCE, Bozec Y, Barber RT, Brzezinski MA, Buesseler KO, Boye M, Croot PL, Gervais F, Gorbunov MY, Harrison PJ, Hiscock WT, Laan P, Lancelot C, Law CS, Levasseur M, Marchetti A, Millero FJ, Nishioka J, Nojiri Y, van Oijen T, Riebesell U, Rijkenberg MJA, Saito H, Takeda S, Timmermans KR, Veldhuis MJW, Waite AM, Wong CS (2005) Synthesis of iron fertilization experiments: from the iron age in the age of enlightenment. J Geophys Res 110:C09S16. doi:10.1029/2004JC002601

    Google Scholar 

  • Desai DK, Desai FD, LaRoche J (2012) Factors influencing the diversity of iron uptake systems in aquatic microorganisms. Front Microbiol 3:362. doi:10.3389/fmicb.2012.00362

    PubMed  PubMed Central  Google Scholar 

  • Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192

    Article  Google Scholar 

  • Doney SC, Ruckelshaus M, Emmett Duffy J, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N, Polovina J, Rabalais NN, Sydeman WJ, Talley LD (2012) Climate change impacts on marine ecosystems. Annu Rev Mar Sci 4:11–37

    Article  Google Scholar 

  • Doucette GJ, Harrison PJ (1991) Aspects of iron and nitrogen nutrition in the red tide dinoflagellate Gymnodinium sanguineum. Mar Biol 110:165–173

    Article  CAS  Google Scholar 

  • Doucette GJ, Erdner DL, Peleato ML, Hartman JJ, Anderson DM (1996) Quantitative analysis of iron-stress related proteins in Thalassiosira weissflogii: measurement of flavodoxin and ferredoxin using HPLC. Mar Ecol Prog Ser 130:269–276

    Article  CAS  Google Scholar 

  • Droop MR (1970) Vitamin B12 and marine ecology V. Continuous culture as an approach to nutritional kinetics. Helgol Wiss Meeresun 20:629–636

    Article  CAS  Google Scholar 

  • Dugdale RC, Wilkerson FP (1991) Low specific nitrate uptake rate – a common feature of high-nutrient, low-chlorophyll marine ecosystems. Limnol Oceanogr 36:1678–1688

    Article  CAS  Google Scholar 

  • Dugdale RC, Wilkerson FP (1998) Silicate regulation of new production in the equatorial Pacific upwelling. Nature 391:270–273

    Article  CAS  Google Scholar 

  • Eckhardt U, Buckhout TJ (1998) Iron assimilation in Chlamydomonas reinhardtii involves ferric reduction and is similar to Strategy I higher plants. J Exp Bot 49:1219–1226

    CAS  Google Scholar 

  • Ehrenreich IM, Waterbury JB, Webb EA (2005) Distribution and diversity of natural product genes in marine and freshwater cyanobacterial cultures and genomes. Appl Environ Microbiol 71:7401–7413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci 93:5624–5628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eldridge ML, Trick CG, Alm MB, DiTullio GR, Rue EL, Bruland KW, Hutchins DA, Wilhelm SW (2004) Phytoplankton community response to a manipulation of bioavailable iron in HNLC waters of the subtropical Pacific Ocean. Aquat Microb Ecol 35:79–91

    Article  Google Scholar 

  • Falkowski PG, Owens TG, Ley AC, Mauzerall DC (1981) Effects of growth irradiance levels on the ratio of reaction centers in 2 species of marine phytoplankton. Plant Physiol 68:969–973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360

    Article  CAS  PubMed  Google Scholar 

  • Faraldo-Gomez JD, Sansom MSP (2003) Acquisition of siderophores in gram-negative bacteria. Nat Rev Mol Cell Biol 4:105–116

    Article  CAS  PubMed  Google Scholar 

  • Faraldo-Gomez JD, Smith GR, Sansom MSP (2003) Molecular dynamics simulations of the bacterial outer membrane protein FhuA: a comparative study of the ferrichrome-free and bound states. Biophys J 85:1406–1420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finkel ZV, Quigg AS, Raven JA, Reinfelder JR, Schofield OE, Falkowski PG (2006) Irradiance and the elemental stoichiometry of marine phytoplankton. Limnol Oceanogr 51:2690–2701

    Article  CAS  Google Scholar 

  • Firme GF, Rue EL, Weeks DA, Bruland KW, Hutchins DA (2003) Spatial and temporal variability in phytoplankton iron limitation along the California coast and consequences for Si, N, and C biogeochemistry. Global Biogeochem Cycles 17:1016

    Article  CAS  Google Scholar 

  • Fitzwater SE, Coale KH, Gordon RM, Johnson KS, Ondrusek ME (1996) Iron deficiency and phytoplankton growth in the equatorial Pacific. Deep-Sea Res II 43:995–1015

    Article  CAS  Google Scholar 

  • Fuhrman JA, Schwalbach MS, Stingl U (2008) Proteorhodopsins: an array of physiological roles? Nat Rev Microbiol 6:488–494

    CAS  PubMed  Google Scholar 

  • Fujii M, Dang TC, Rose AL, Omura T, Waite TD (2011) Effect of light on iron uptake by the freshwater cyanobacterium Microcystis aeruginosa. Environ Sci Technol 45:1391–1398

    Article  CAS  PubMed  Google Scholar 

  • Gademann K, Portmann C (2008) Secondary metabolites from cyanobacteria: complex structures and powerful bioactivities. Curr Org Chem 12:326–341

    Article  CAS  Google Scholar 

  • Gaither LA, Eide DJ (2001) Eukaryotic zinc transporters and their regulation. Biometals 14:251–270

    Article  CAS  PubMed  Google Scholar 

  • Garcia NS, Sedwick PN, DiTullio GR (2009) Influence of irradiance and iron on the growth of colonial Phaeocystis antarctica: implications for seasonal bloom dynamics in the Ross Sea, Antarctica. Aquat Microb Ecol 57:203–220

    Article  Google Scholar 

  • Geider RJ (1987) Light and temperature dependence of the carbon to chlorophyll a ratio in microalgae and cyanobacteria: implications for physiology and growth of phytoplankton. New Phytol 106:1–34

    Article  CAS  Google Scholar 

  • Geider RJ, LaRoche J (1994) The role of iron in phytoplankton photosynthesis, and the potential for iron limitation of primary productivity in the sea. Photosynth Res 39:275–301

    Article  CAS  PubMed  Google Scholar 

  • Geider RJ, La Roche J, Greene R, Olaizola M (1993) Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate or iron limitation. J Phycol 29:755–766

    Article  CAS  Google Scholar 

  • Gledhill M, Buck KN (2012) The organic complexation of iron in the marine environment: a review. Front Microbiol 3:69. doi:10.3389/fmicb.2012.00069

    PubMed  PubMed Central  Google Scholar 

  • Gledhill M, van den Berg CMG (1994) Determination of complexation of iron(III) with natural organic complexing ligands in seawater using cathodic stripping voltammetry. Mar Chem 47:41–54

    Article  CAS  Google Scholar 

  • Glover HF (1977) Effects of iron deficiency on the physiology and biochemistry of Isochrysis galbana (Chrysophyceae) and Phaedactylum tricornutum (Bacillariophyceae). J Phycol 13:208–212

    CAS  Google Scholar 

  • Greene RM, Geider RJ, Falkowski PG (1991) Effect of iron limitation on photosynthesis in a marine diatom. Limnol Oceanogr 36:1772–1782

    Article  CAS  Google Scholar 

  • Greene RM, Geider RJ, Kolber Z, Falkowski PG (1992) Iron-induced changes in light harvesting and photochemical energy conversion processes in eukaryotic marine algae. Plant Physiol 100:565–575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groussman RD, Parker MS, Armbrust EV (2015) Diversity and evolutionary history of iron metabolism genes in diatoms. PLoS ONE 10:e0129081

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo J, Annett AL, Taylor RL, Lapi S, Ruth TJ, Maldonado MT (2010) Copper uptake kinetics of coastal and oceanic diatoms. J Phycol 46:1218–1228

    Article  Google Scholar 

  • Guo J, Lapi S, Ruth TJ, Maldonado MT (2012) The effects of iron and copper availability on the copper stoichiometry of marine phytoplankton. J Phycol 48:312–325

    Article  CAS  Google Scholar 

  • Guo J, Green BR, Maldonado MT (2015) Sequence analysis and gene expression of potential components of copper transport and homeostasis in Thalassiosira pseudonana. Protist 166:58–77

    Article  CAS  PubMed  Google Scholar 

  • Hamm CE, Merkel R, Springer O, Jurkojc P, Maier C, Prechtel K, Smetacek V (2003) Architecture and material properties of diatom shells provide effective mechanical protection. Nature 421:841–843

    Article  CAS  PubMed  Google Scholar 

  • Harris JE (1992) Weathering of rock, corrosion of stone and rusting of iron. Meccanica 27:233–250

    Article  Google Scholar 

  • Harrison PJ, Berges JA (2005) Marine culture media. In: Andersen RA (ed) Algal culturing techniques. Elsevier Academic Press, San Diego, pp 21–34

    Google Scholar 

  • Harrison GI, Morel FMM (1986) Response of the marine diatom Thalassiosira weissflogii to iron stress. Limnol Oceanogr 31:989–997

    Article  CAS  Google Scholar 

  • Harrison PJ, Whitney FA, Tsuda A, Saito H, Tadokoro K (2004) Nutrient and plankton dynamics in the NE and NW gyres of the subarctic Pacific Ocean. J Oceanogr 60:93–117

    Article  CAS  Google Scholar 

  • Hart TJ (1934) On the phytoplankton of the Southwest Atlantic and the Bellingshausen Sea. Discov Rep 8:1–268

    Google Scholar 

  • Hartnett A, Bottger LH, Matzanke BF, Carrano CJ (2012a) Iron transport and storage in the coccolithophore: Emiliania huxleyi. Metallomics 4:1160–1166

    Article  CAS  PubMed  Google Scholar 

  • Hartnett A, Bottger LH, Matzanke BF, Carrano CJ (2012b) A multidisciplinary study of iron transport and storage in the marine green alga Tetraselmis suecica. J Inorg Biochem 116:188–194

    Article  CAS  PubMed  Google Scholar 

  • Havens SM, Hassler CS, North RL, Guildford SJ, Silsbe G, Wilhelm SW, Twiss MR (2012) Iron plays a role in nitrate drawdown by phytoplankton in Lake Erie surface waters as observed in lake-wide assessments. Can J Fish Aquat Sci 69:369–381

    Article  CAS  Google Scholar 

  • Herbik A, Bolling C, Buckhout TJ (2002a) The involvement of a multicopper oxidase in iron uptake by the green algae Chlamydomonas reinhardtii. Plant Physiol 130:2039–2048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herbik A, Haebel S, Buckhout TJ (2002b) Is a ferroxidase involved in the high-affinity iron uptake in Chlamydomonas reinhardtii. Plant Soil 241:1–9

    Article  CAS  Google Scholar 

  • Hill KL, Merchant S (1995) Coordinate expression of coproporphyrinogen oxidase and cytochrome c6 in the green alga Chlamydomonas reinhardtii in response to changes in copper availability. EMBO J 14:857–865

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ho T-Y, Quigg A, Finkel ZV, Milligan AJ, Wyman K, Falkowski PG, Morel FMM (2003) The elemental composition of some marine phytoplankton. J Phycol 39:1145–1159

    Article  CAS  Google Scholar 

  • Hoffmann LJ, Breitbarth E, Boyd PW, Hunter KA (2012) Influence of ocean warming and acidification on trace metal biogeochemistry. Mar Ecol Prog Ser 470:191–205

    Article  CAS  Google Scholar 

  • Hopkinson B, Barbeau K (2008) Interactive influences of iron and light limitation on phytoplankton at subsurface chlorophyll maxima in the eastern North Pacific. Limnol Oceanogr 53:1303–1318

    Article  CAS  Google Scholar 

  • Hopkinson BM, Barbeau KA (2012) Iron transporters in marine prokaryotic genomes and metagenomes. Environ Microbiol 14:114–128

    Article  CAS  PubMed  Google Scholar 

  • Hopkinson BM, Morel FMM (2009) The role of siderophores in iron acquisition by photosynthetic marine microorganisms. Biometals 22:659–669

    Article  CAS  PubMed  Google Scholar 

  • Hopkinson BM, Xu Y, Shi D, McGinn PJ, Morel FMM (2010) The effect of CO2 on the photosynthetic physiology of phytoplankton in the Gulf of Alaska. Limnol Oceanogr 55:2011–2024

    Article  CAS  Google Scholar 

  • Hoppe CJM, Hassler CS, Payne CD, Tortell PD, Rost B, Trimborn S (2013) Iron limitation modulates ocean acidification effects on Southern Ocean phytoplankton communities. PLoS ONE 8:e79890

    Article  PubMed  PubMed Central  Google Scholar 

  • Hudson RJM, Morel FMM (1989) Distinguishing between extra- and intracellular iron in marine phytoplankton. Limnol Oceanogr 34:111–1120

    Article  Google Scholar 

  • Hudson RJM, Morel FMM (1990) Iron transport in marine phytoplankton – kinetics of cellular and medium coordination reactions. Limnol Oceanogr 35:1002–1020

    Article  CAS  Google Scholar 

  • Hudson RJM, Morel FMM (1993) Trace-metal transport by marine microorganisms – implications of metal coordination kinetics. Deep-Sea Res I 40:129–150

    Article  CAS  Google Scholar 

  • Hutchins DA (1995) Iron and the marine phytoplankton community. Phycol Res 11:1–49

    CAS  Google Scholar 

  • Hutchins DA, Bruland KW (1998) Iron-limited diatom growth and Si:N uptake ratios in a coastal upwelling regime. Nature 393:561–564

    Article  CAS  Google Scholar 

  • Hutchins DA, DiTullio GR, Zhang Y, Bruland KW (1998) An iron limitation mosaic in the California upwelling regime. Limnol Oceanogr 43:1037–1054

    Article  CAS  Google Scholar 

  • Hutchins DA, Franck VM, Brzezinski MA, Bruland KW (1999a) Inducing phytoplankton iron limitation in iron-replete coastal waters with a strong chelating ligand. Limnol Oceanogr 44:1009–1018

    Article  CAS  Google Scholar 

  • Hutchins DA, Witter AE, Butler A, Luther GW (1999b) Competition among marine phytoplankton for different chelated iron species. Nature 400:858–861

    Article  CAS  Google Scholar 

  • Hutchins DA, Hare CE, Weaver RS, Zhang Y, Firme GF, DiTullio GR, Alm MB, Riseman SF, Maucher JM, Geesey ME (2002) Phytoplankton iron limitation in the Humboldt Current and Peru Upwelling. Limnol Oceanogr 47:997–1011

    Article  Google Scholar 

  • Hyenstrand P, Rydin E, Gunnerhed M (2000) Response of pelagic cyanobacteria to iron additions – enclosure experiments from Lake Erken. J Plankton Res 22:1113–1126

    Article  CAS  Google Scholar 

  • Ito Y, Butler A (2005) Structure of synechobactins, new siderophores of the marine cyanobacterium Synechococcus sp. PCC 7002. Limnol Oceanogr 50:1918

    Article  CAS  Google Scholar 

  • Johnson KS, Gordon RM, Coale KH (1997) What controls dissolved iron concentrations in the world ocean? Mar Chem 57:137–161

    Article  CAS  Google Scholar 

  • Johnson KS, Chavez FP, Friederich GE (1999) Continental-shelf sediment as a primary source of iron for coastal phytoplankton. Nature 398:697–700

    Article  CAS  Google Scholar 

  • Jones GJ, Palenik BP, Morel FMM (1987) Trace metal reduction by phytoplankton: the role of plasmalemma redox enzymes. J Phycol 23:237–244

    Article  CAS  Google Scholar 

  • Katoh H, Hagino N, Grossman AR, Ogawa T (2001a) Genes essential to iron transport in the cyanobacterium Synechocystis sp strain PCC 6803. J Bacteriol 183:2779–2784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Klunder MB, Bauch D, Laan P, de Baar HJW, van Heuven S, Ober S (2012) Dissolved iron in the Arctic shelf seas and surface waters of the central Arctic Ocean: impact of Arctic river water and ice-melt. J Geophys Res 117:C01027

    Google Scholar 

  • Koch F, Marcoval MA, Panzeca C, Bruland KW, Sanudo-Wilhelmy SA, Gobler CJ (2011) The effect of vitamin B12 on phytoplankton growth and community structure in the Gulf of Alaska. Limnol Oceanogr 56:1023–1034

    Article  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. Environ Microbiol 13:2990–2999

    Article  CAS  PubMed  Google Scholar 

  • Kranzler C, Rudolf M, Keren N, Schleiff E (2013) Iron in cyanobacteria. Adv Bot Res 65:57–105

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krewulak KD, Vogel HJ (2011) TonB or not TonB: is that the question? Biochem Cell Biol 89:87–97

    Article  CAS  PubMed  Google Scholar 

  • Kudo I, Harrison PJ (1997) Effect of iron nutrition on the marine cyanobacterium Synechococcus grown on different N sources and irradiances. J Phycol 33:232–240

    Article  CAS  Google Scholar 

  • Kudo I, Noiri Y, Nishioka J, Taira Y, Kiyosawa H, Tsuda A (2006) Phytoplankton community response to Fe and temperature gradients in the NE (SERIES) and NW (SEEDS) subarctic Pacific Ocean. Deep Sea Res II 53:2201–2213

    Article  Google Scholar 

  • Kuma K et al (1992) Photo-reduction of Fe (III) by dissolved organic substances and existence of Fe (II) in seawater during spring blooms. Mar Chem 37:15–27

    Article  CAS  Google Scholar 

  • Kustka AB, Sanudo-Wilhemy SA, Carpenter EJ, Capone D, Burns J, Sunda WG (2003) Iron requirements for dinitrogen- and ammonium-supported growth in cultures of Trichodesmium (IMS 101): comparison with nitrogen fixation rates and iron:carbon ratios of field populations. Limnol Oceanogr 48:1869–1884

    Article  CAS  Google Scholar 

  • Kustka AB, Allen AE, Morel FMM (2007) Sequence analysis and transcriptional regulation of iron acquisition genes in two marine diatoms. J Phycol 43:715–729

    Article  CAS  Google Scholar 

  • La Fontaine S, Quinn JM, Nakamoto SS, Page MD, Gohre V, Moseley JL, Kropat J, Merchant S (2002) Copper-dependent iron assimilation pathway in the model photosynthetic eukaryote Chlamydomonas reinhardtii. Eukaryot Cell 1:736–757

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • La Roche J, Geider RJ, Graziano LM, Murray H, Lewis K (1993) Induction of specific proteins in eukaryotic algae grown under iron-deficient, phosphorus-deficient, or nitrogen-deficient conditions. J Phycol 29:767–777

    Article  Google Scholar 

  • La Roche J, Boyd P, McKay R, Geider R (1996) Flavodoxin as an in situ marker for iron stress in phytoplankton. Nature 382:802–805

    Article  Google Scholar 

  • Lane ES, Semeniuk DM, Strzepek RF, Cullen JT, Maldonado MT (2009) Effects of iron limitation on intracellular cadmium of cultured phytoplankton: implications for surface dissolved cadmium to phosphate ratios. Mar Chem 115:155–162

    Article  CAS  Google Scholar 

  • Lelong A, Bucciarelli E, Hagaret H, Soudant P (2013) Iron and copper limitations differently affect growth rates and photosynthetic and physiological parameters of the marine diatom Pseudo-nitzschia delicatissima. Limnol Oceanogr 58:613–623

    CAS  Google Scholar 

  • Lin W, Chai J, Love J, Fu D (2010) Selective electrodiffusion of zinc ions in a Zrt-, Irt-like protein, ZIPB. J Biol Chem 285:39013–39020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin H, Rauschenberg S, Hexel CR, Shaw TJ, Twining BS (2011) Free-drifting icebergs as sources of iron to the Weddell Sea. Deep Sea Res II 58:1392–1406

    Article  CAS  Google Scholar 

  • Lis H, Shaked Y (2009) Probing the bioavailability of organically bound iron: a case study in the Synechococcus-rich waters of the Gulf of Aqaba. Aquat Microb Ecol 56:241–253

    Article  Google Scholar 

  • Lis H, Shaked Y, Kranzler C, Keren N, Morel FMM (2015) Iron bioavailability to phytoplankton: an empirical approach. ISME J 9:1003–1013

    Article  CAS  PubMed  Google Scholar 

  • Liu XW, Theil EC (2005) Ferritins: dynamic management of biological iron and oxygen chemistry. Acc Chem Res 38:167–175

    Article  CAS  PubMed  Google Scholar 

  • Lohan MC, Bruland KW (2008) Elevated Fe(II) and dissolved Fe in hypoxic shelf waters off Oregon and Washington: an enhanced source of iron to coastal upwelling regimes. Environ Sci Technol 42:6462–6468

    Article  CAS  PubMed  Google Scholar 

  • Lommer M, Roy A, Schilhabel M, Schreiber S, Rosenstiel P, LaRoche J (2010) Recent transfer of an iron-regulated gene from the plastid to the nuclear genome in an oceanic diatom adapted to chronic iron limitation. BMC Genomics 11:718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lommer M, Specht M, Roy A-S, Kraemer L, Andreson R, Gutowska M, Wolf J, Bergner S, Schilhabel M, Klostermeier U, Beiko R, Rosenstiel P, Hippler M, LaRoche J (2012) Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation. Genome Biol 13:R66

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahowald NM, Baker AR, Bergametti G, Brooks N, Duce RA, Jickells TD, Kubilay N, Prospero JM, Tegen I (2005) Atmospheric global dust cycle and iron inputs to the ocean. Glob Biogeochem Cycles 19:GB4025

    Google Scholar 

  • Maldonado MT, Price NM (1996) Influence of N substrate on Fe requirements of marine centric diatoms. Mar Ecol Prog Ser 141:161–172

    Article  CAS  Google Scholar 

  • Maldonado MT, Price NM (1999) Utilization of iron bound to strong organic ligands by plankton communities in the subarctic Pacific Ocean. Deep Sea Res II 46:2447–2473

    Article  CAS  Google Scholar 

  • Maldonado MT, Price NM (2000) Nitrate regulation of Fe reduction and transport by Fe-limited Thalassiosira oceanica. Limnol Oceanogr 45:814–826

    Article  CAS  Google Scholar 

  • Maldonado MT, Price NM (2001) Reduction and transport of organically bound iron by Thalassiosira oceanica (Bacillariophyceae). J Phycol 37:298–309

    Article  CAS  Google Scholar 

  • Maldonado MT, Boyd PW, Harrison PJ, Price NM (1999) Co-limitation of phytoplankton growth by light and Fe during winter in the NE subarctic Pacific Ocean. Deep Sea Res II 46:2475–2485

    Article  CAS  Google Scholar 

  • Maldonado MT, Boyd PW, LaRoche J, Strzepek R, Waite A, Bowie AR, Croot PL, Frew RD, Price NM (2001) Iron uptake and physiological response of phytoplankton during a mesoscale Southern Ocean iron enrichment. Limnol Oceanogr 46:1802–1808

    Article  CAS  Google Scholar 

  • Maldonado MT, Strzepek RF, Sander S, Boyd PW (2005) Acquisition of iron bound to strong organic complexes, with different Fe binding groups and photochemical reactivities, by plankton communities in Fe-limited subantarctic waters. Glob Biogeochem Cycles 19:GB4S23

    Article  CAS  Google Scholar 

  • Maldonado MT, Allen AE, Chong JS, Lin K, Leus D, Karpenko N, Harris SL (2006) Copper-dependent iron transport in coastal and oceanic diatoms. Limnol Oceanogr 51:1729–1743

    Article  CAS  Google Scholar 

  • Maranger R, Bird DF, Price NM (1998) Iron acquisition by photosynthetic marine phytoplankton from ingested bacteria. Nature 396:248–251

    Article  CAS  Google Scholar 

  • Marchetti A, Cassar N (2009) Diatom elemental and morphological changes in response to iron limitation: a brief review with potential paleoceanographic applications. Geobiology 7:419–431

    Article  CAS  PubMed  Google Scholar 

  • Marchetti A, Harrison PJ (2007) Coupled changes in the cell morphology and the elemental (C, N and Si) composition of the pennate diatom Pseudo-nitzschia due to iron deficiency. Limnol Oceanogr 52:2270–2284

    Article  CAS  Google Scholar 

  • Marchetti A, Maldonado MT, Lane ES, Harrison PJ (2006) Iron requirements of the pennate diatom Pseudo-nitzschia: comparison of oceanic (HNLC) and coastal species. Limnol Oceanogr 51:2092–2101

    Article  CAS  Google Scholar 

  • Marchetti A, Lundholm N, Kotaki Y, Hubbard KA, Harrison PJ, Armbrust EV (2008) Identification and assessment of domoic acid production in oceanic Pseudo-nitzschia (Bacillariophyceae) from iron-limited waters in the NE Subarctic Pacific. J Phycol 44:650–661

    Article  CAS  Google Scholar 

  • Marchetti A, Parker MS, Moccia LP, Lin EO, Arrieta AL, Ribalet F, Murphy MEP, Maldonado MT, Armbrust EV (2009) Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature 457:467–470

    Article  CAS  PubMed  Google Scholar 

  • Marchetti A, Varela DE, Lance VP, Johnson Z, Palmucci M, Giordano M, Armbrust EV (2010) Iron and silicic acid effects on phytoplankton productivity, diversity, and chemical composition in the central equatorial Pacific Ocean. Limnol Oceanogr 55:11–29

    Article  CAS  Google Scholar 

  • Marchetti A, Schruth DM, Durkin CA, Parker MS, Kodner RB, Berthiaume CT, Morales R, Allen AE, Armbrust EV (2012) Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability. Proc Natl Acad Sci 109:E317–E325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marchetti A, Catlett D, Hopkinson BM, Ellis K, Cassar N (2015) Marine diatom proteorhodopsins and their potential role in coping with low iron availability. ISME J. doi:10.1038/ismej.2015.74

    PubMed  Google Scholar 

  • Martin JH (1990) Glacial-interglacial CO2 change: the iron hypothesis. Paleoceanography 5:1–13

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Martin JH, Gordon RM, Fitzwater S, Broenkow WW (1989) Vertex – phytoplankton iron studies in the Gulf of Alaska. Deep Sea Res I 36:649–680

    Article  CAS  Google Scholar 

  • Martinez JS, Carter-Franklin JN, Mann EL, Martin JD, Haygood MG, Butler A (2003) Structure and membrane affinity of a suite of amphiphilic siderophores produced by a marine bacterium. Proc Natl Acad Sci 100:3754–3759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matz CJ, Magnus RS, Walker CN, Fink MB, Treble RG, Weger HG (2006) Differences between two green algae in biological availability of iron bound to strong chelators. Can J Bot 84:400–411

    Article  CAS  Google Scholar 

  • Mawji E, Gledhill M, Milton JA, Tarran GA, Ussher S, Thompson A, Wolff GA, Worsfold PJ, Achterberg EP (2008) Hydroxamate siderophores: occurrence and importance in the Atlantic Ocean. Environ Sci Technol 42:8675–8680

    Article  CAS  PubMed  Google Scholar 

  • McAllister CD, Parsons TR, Strickland JDH (1960) Primary productivity and fertility at Station P in the north-east Pacific Ocean. ICES J Mar Sci 25:240–259

    Article  Google Scholar 

  • Merchant SS, Allen MD, Kropat J, Moseley JL, Long JC, Tottey S, Terauchi AM (2006) Between a rock and a hard place: trace element nutrition in Chlamydomonas. Biochim Biophys Acta, Mol Cell Res 1763:578–594

    Article  CAS  PubMed  Google Scholar 

  • Middlemiss JK, Anderson AM, Stratilo CW, Weger HG (2001) Oxygen consumption associated with ferric reductase activity and iron uptake by iron-limited cells of Chlorella kessleri (Chlorophyceae). J Phycol 37:393–399

    Article  CAS  Google Scholar 

  • Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413–451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller CB, Frost BW, Wheeler PA, Landry MR, Welschmeyer N, Powell TM (1991) Ecological dynamics in the subarctic Pacific, a possibly iron-limited ecosystem. Limnol Oceanogr 36:1600–1615

    Article  CAS  Google Scholar 

  • Millero FJ, Woosley R, DiTrolio BJW (2009) Effect of ocean acidification on the speciation of metals in seawater. Oceanography 22:72–85

    Article  Google Scholar 

  • Milligan AJ, Harrison PJ (2000) Effects of non-steady-state iron limitation on nitrogen assimilatory enzymes in the marine diatom Thalassiosira weissflogii (Bacillariophyceae). J Phycol 36:78–86

    Article  CAS  Google Scholar 

  • Mills MM, Ridame C, Davey M, La Roche J, Geider RJ (2004) Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429:292–294

    Article  CAS  PubMed  Google Scholar 

  • Mirus O, Strauss S, Nicolaisen K, von Haeseler A, Schleiff E (2009) TonB-dependent transporters and their occurrence in cyanobacteria. BMC Biol 7:68

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mitchell BG, Brody EA, Holm-Hansen O, McClain C, Bishop J (1991) Light limitation of phytoplankton biomass and macronutrient utilization in the Southern Ocean. Limnol Oceanogr 36:1662–1677

    Article  Google Scholar 

  • Mock T, Samanta MP, Iverson V, Berthiaume C, Robison M, Holtermann K, Durkin C, BonDurant SS, Richmond K, Rodesch M, Kallas T, Huttlin EL, Cerrina F, Sussmann MR, Armbrust EV (2008) Whole-genome expression profiling of the marine diatom Thalassiosira pseudonana identifies genes involved in silicon bioprocesses. Proc Natl Acad Sci U S A 105:1579–1584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monod J (1942) Recherches sur la croissance des Cultures Bactériennes. Hermann, Paris

    Google Scholar 

  • Monzyk B, Crumbliss AL (1982) Kinetics and mechanism of the stepwise dissociation of iron(III) from ferrioxamine B in aqueous acid. J Am Chem Soc 104:4921–4929

    Article  CAS  Google Scholar 

  • Moore JK, Braucher O (2008) Sedimentary and mineral dust sources of dissolved iron to the world ocean. Biogeosciences 5:631–656

    Article  CAS  Google Scholar 

  • Moore JK, Doney SC, Glover DM, Fung IY (2002) Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean. Deep Sea Res II 49:463–507

    Article  CAS  Google Scholar 

  • Moore CM, Mills MM, Achterberg EP, Geider RJ, LaRoche J, Lucas MI, McDonagh EL, Pan X, Poulton AJ, Rijkenberg MJA, Suggett DJ, Ussher SJ, Woodward EMS (2009) Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability. Nat Geosci 2:867–871

    Article  CAS  Google Scholar 

  • Morel FMM (1987) Kinetics of nutrient uptake and growth in phytoplankton. J Phycol 23:137–150

    Article  CAS  Google Scholar 

  • Morel FMM, Hudson R, Price N (1991) Limitation of productivity by trace metals in the sea. Limnol Oceanogr 36:1742–1755

    Article  CAS  Google Scholar 

  • Morrissey J, Bowler C (2012) Iron utilization in marine cyanobacteria and eukaryotic algae. Front Microbiol 3:43. doi:10.3389/fmicb.2012.00043

    PubMed  PubMed Central  Google Scholar 

  • Morton SD, Lee TH (1974) Algal blooms. Possible effects of iron. Environ Sci Technol 8:673–674

    Article  CAS  Google Scholar 

  • Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, Hippler M (2002) Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J 21:6709–6720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muggli DL, Harrison PJ (1996a) EDTA suppresses the growth of oceanic phytoplankton from the Northeast subarctic Pacific. J Exp Mar Biol Ecol 205:221–227

    Article  CAS  Google Scholar 

  • Muggli DL, Harrison PJ (1996b) Effects of nitrogen source on the physiology and metal nutrition of Emiliania huxleyi grown under different iron and light conditions. Mar Ecol Prog Ser 130:255–267

    Article  CAS  Google Scholar 

  • Muggli DL, Lecourt M, Harrison PJ (1996) Effects of iron and nitrogen source on the sinking rate, physiology and metal composition of an oceanic diatom from the subarctic Pacific. Mar Ecol Prog Ser 132:215–227

    Article  CAS  Google Scholar 

  • Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726

    Article  CAS  PubMed  Google Scholar 

  • Nelson DM, Treguer P, Brzezinski MA, Leynaert A, Queguiner B (1995) Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationships to biogenic sedimentation. Glob Biogeochem Cycles 9:359–372

    Article  CAS  Google Scholar 

  • Nevo Y, Nelson N (2006) The NRAMP family of metal-ion transporters. Biochim Biophys Acta Mol Cell Res 1763:609–620

    Article  CAS  Google Scholar 

  • Nicolaisen K, Moslavac S, Samborski A, Valdebenito M, Hantke K, Maldener I, Muro-Pastor AM, Flores E, Schleiff E (2008) Alr0397 is an outer membrane transporter for the siderophore schizokinen in Anabaena sp. strain PCC 7120. J Bacteriol 190:7500–7507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicolaisen K, Hahn A, Valdebenito M, Moslavac S, Samborski A, Maldener I, Wilken C, Valladares A, Flores E, Hantke K (2010) The interplay between siderophore secretion and coupled iron and copper transport in the heterocyst-forming cyanobacterium Anabaena sp. PCC 7120. Biochim Biophys Acta Biomembr 1798:2131–2140

    Article  CAS  Google Scholar 

  • Nishioka J, Takeda S (2000) Change in the concentrations of iron in different size fractions during growth of the oceanic diatom Chaetoceros sp.: importance of small colloidal iron. Mar Biol 137:231–238

    Article  CAS  Google Scholar 

  • Noinaj N, Guillier M, Barnard TJ, Buchanan SK (2010) TonB-dependent transporters: regulation, structure, and function. I Ann Rev Microbiol 64:43–60

    Article  CAS  Google Scholar 

  • North RL, Guildford SJ, Smith REH, Havens SM, Twiss MR (2007) Evidence for phosphorus, nitrogen, and iron colimitation of phytoplankton communities in Lake Erie. Limnol Oceanogr 52:315–328

    Article  CAS  Google Scholar 

  • Nouet C, Motte P, Hanikenne M (2011) Chloroplastic and mitochondrial metal homeostasis. Trends Plant Sci 16:395–404

    Article  CAS  PubMed  Google Scholar 

  • Nuester J, Vogt S, Twining BS (2012) Localization of iron within centric diatoms of the genus Thalassiosira. J Phycol 48:626–634

    Article  CAS  Google Scholar 

  • Palenik B, Ren Q, Dupont CL, Myers GS, Heidelberg JF, Badger JH, Madupu R, Nelson WC, Brinkac LM, Dodson RJ (2006) Genome sequence of Synechococcus CC9311: insights into adaptation to a coastal environment. Proc Natl Acad Sci 103:13555–13559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palenik B, Grimwood J, Aerts A, Rouze P, Salamov A, Putnam N, Dupont C, Jorgensen R, Derelle E, Rombauts S, Zhou K, Otillar R, Merchant SS, Podell S, Gaasterland T, Napoli C, Gendler K, Manuell A, Tai V, Vallon O, Piganeau G, Sv J, Heijde M, Jabbari K, Bowler C, Lohr M, Robbens S, Werner G, Dubchak I, Pazour GJ, Ren Q, Paulsen I, Delwiche C, Schmutz J, Rokhsar D, Van de Peer Y, Moreau H, Grigoriev IV (2007) The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci 104:7705–7710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pankowski A, McMinn A (2009) Iron availability regulates growth, photosynthesis, and production of ferredoxin and flavodoxin in Antarctic sea ice diatoms. Aquat Biol 4:273–288

    Article  Google Scholar 

  • Passy SI (2010) A distinct latitudinal gradient of diatom diversity is linked to resource supply. Ecology 91:36–41

    Article  PubMed  Google Scholar 

  • Paz Y, Katz A, Pick U (2007a) Multicopper ferroxidase involved in iron binding to transferrins in Dunaliella salina plasma membranes. J Biol Chem 282:8658–8666

    Article  CAS  PubMed  Google Scholar 

  • Paz Y, Shimoni E, Weiss M, Pick U (2007b) Effects of iron deficiency on iron binding and internalization into acidic vacuoles in Dunaliella salina. Plant Physiol 144:1407–1415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peers G, Price N (2006) Copper-containing plastocyanin used for electron transport by an oceanic diatom. Nature 441:341–344

    Article  CAS  PubMed  Google Scholar 

  • Peers G, Quesnel SA, Price NM (2005) Copper requirements for iron acquisition and growth of coastal and oceanic diatoms. Limnol Oceanogr 50:1149–1158

    Article  CAS  Google Scholar 

  • Pollard RT, Salter I, Sanders RJ, Lucas MI, Moore CM, Mills RA, Statham PJ, Allen JT, Baker AR, Bakker DCE, Charette MA, Fielding S, Fones GR, French M, Hickman AE, Holland RJ, Hughes JA, Jickells TD, Lampitt RS, Morris PJ, Nedelec FH, Nielsdottir M, Planquette H, Popova EE, Poulton AJ, Read JF, Seeyave S, Smith T, Stinchcombe M, Taylor S, Thomalla S, Venables HJ, Williamson R, Zubkov MV (2009) Southern Ocean deep-water carbon export enhanced by natural iron fertilization. Nature 457:577–580

    Article  CAS  PubMed  Google Scholar 

  • Pollingher U, Kaplan B, Berman T (1995) The impact of iron and chelators on Lake Kinneret phytoplankton. J Plankton Res 17:1977–1992

    Article  CAS  Google Scholar 

  • Pondaven P, Gallinari M, Chollet S, Bucciarelli E, Sarthou G, Schultes S, Jean F (2007) Grazing-induced changes in cell wall silicification in a marine diatom. Protist 158:21–28

    Article  CAS  PubMed  Google Scholar 

  • Price NM (2005) The elemental stoichiometry and composition of an iron-limited diatom. Limnol Oceanogr 50:1159–1171

    Article  CAS  Google Scholar 

  • Price NM, Harrison GI, Hering JG, Hudson RJ, Nirel PMV, Palenik B, Morel FMM (1988/89) Preparation and chemistry of the artificial algal culture medium Aquil. Biol Oceanogr 6:443–461

    Google Scholar 

  • Price NM, Andersen LF, Morel FMM (1991) Iron and nitrogen nutrition of Equatorial Pacific plankton. Deep Sea Res II 38:1361–1378

    Article  Google Scholar 

  • Price NM, Ahner BA, Morel FMM (1994) The Equatorial Pacific Ocean – grazer-controlled phytoplankton populations in an iron-limited ecosystem. Limnol Oceanogr 39:520–534

    Article  CAS  Google Scholar 

  • Quigg A, Finkel ZV, Irwin AJ, Rosenthal Y, Ho TY, Reinfelder JR, Schofield O, Morel FMM, Falkowski PG (2003) The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature 425:291–294

    Article  CAS  PubMed  Google Scholar 

  • Quigg A, Irwin AJ, Finkel ZV (2011) Evolutionary inheritance of elemental stoichiometry in phytoplankton. Proc Roy Soc B 278:526–534

    Article  Google Scholar 

  • Raiswell R, Benning L, Tranter M, Tulaczyk S (2008) Bioavailable iron in the Southern Ocean: the significance of the iceberg conveyor belt. Geochem Trans 9:7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Raven JA (1990) Predictions of Mn and Fe use efficiencies of phototrophic growth as a function of light availability for growth and of C assimilation pathway. New Phytol 116:1–18

    Article  CAS  Google Scholar 

  • Raven JA, Waite A (2004) The evolution of silicification in diatoms: inescapable sinking and sinking as escape. New Phytol 162:45–65

    Article  Google Scholar 

  • Rose AL (2012) The influence of extracellular superoxide on iron redox chemistry and bioavailability to aquatic microorganisms. Front Microbiol 3:124. doi:10.3389/fmicb.2012.00124

    PubMed  PubMed Central  Google Scholar 

  • Rue EL, Bruland KW (1995) Complexation of iron (III) by natural organic ligands in the Central North Pacific as determined by a new competitive ligand equilibration/adsorptive cathodic stripping voltammetric method. Mar Chem 50:117–138

    Article  CAS  Google Scholar 

  • Rueter JG, Ades DR (1987) The role of iron nutrition in photosynthesis and nitrogen assimilation in Scenedesmus quadricauda (Chlorophyceae). J Phycol 23:452–457

    Article  CAS  Google Scholar 

  • Ryan-Keogh TJ, Macey AI, Cockshutt AM, Moore CM, Bibby TS (2012) The cyanobacterial chlorophyll-binding-protein isiA acts to increase the in vivo effective absorption cross-section of PSI under iron limitation. J Phycol 48:145–154

    Article  CAS  Google Scholar 

  • Saito MA, Rocap G, Moffett JW (2005) Production of cobalt binding ligands in a Synechococcus feature at the Costa Rica upwelling dome. Limnol Oceanogr 50:279–290

    Article  CAS  Google Scholar 

  • Saito MA, Goepfert TJ, Ritt JT (2008) Some thoughts on the concept of colimitation: three definitions and the importance of bioavailability. Limnol Oceanogr 53:276–290

    Article  CAS  Google Scholar 

  • Saito MA, Noble AE, Tagliabue A, Goepfert TJ, Lamborg CH, Jenkins WJ (2013) Slow-spreading submarine ridges in the South Atlantic as a significant oceanic iron source. Nat Geosci 6:775–779

    Article  CAS  Google Scholar 

  • Sandmann G, Reck H, Kessler E, Boger P (1983) Distribution of plastocyanin and soluble plastidic cytochrome c in various classes of algae. Arch Microbiol 134:23–27

    Article  CAS  Google Scholar 

  • Sandmann G, Peleato ML, Fillat MF, Lazaro MC, Gomez-Moreno C (1990) Consequences of the iron-dependent formation of ferredoxin and flavodoxin on photosynthesis and nitrogen fixation on Anabaena strains. Photosynth Res 26:119–125

    Article  CAS  PubMed  Google Scholar 

  • Schauer K, Rodionov DA, de Reuse H (2008) New substrates for TonB-dependent transport: do we only see the “tip of the iceberg”? Trends Biochem Sci 33:330–338

    Article  CAS  PubMed  Google Scholar 

  • Schenck RC, Tessier A, Campbell PGC (1988) The effect of pH on iron and manganese uptake by a green alga. Limnol Oceanogr 33:538–550

    Article  CAS  Google Scholar 

  • Sedwick PN, Garcia N, Riseman S, Marsay C, DiTullio G (2007) Evidence for high iron requirements of colonial Phaeocystis antarctica at low irradiance. Biogeochemistry 83:83–97

    Article  Google Scholar 

  • Shaked Y, Lis H (2012) Disassembling iron availability to phytoplankton. Front Microbiol 3:123. doi:10.3389/fmicb.2012.00123

    PubMed  PubMed Central  Google Scholar 

  • Shaked Y, Kustka A, Morel F (2005) A general kinetic model for iron acquisition by eukaryotic phytoplankton. Limnol Oceanogr 50:872–882

    Article  CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi D, Xu Y, Hopkinson BM, Morel FMM (2010) Effect of ocean acidification on iron availability to marine phytoplankton. Science 327:676–679

    Article  CAS  PubMed  Google Scholar 

  • Shi D, Kranz SA, Kim J-M, Morel FMM (2012) Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions. Proc Natl Acad Sci 109:E3094–E3100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva-Stenico ME, Silva CS, Lorenzi AS, Shishido TK, Etchegaray A, Lira SP, Moraes LA, Fiore MF (2011) Non-ribosomal peptides produced by Brazilian cyanobacterial isolates with antimicrobial activity. Microb Res 166:161–175

    Article  CAS  Google Scholar 

  • Simpson FB, Neilands JB (1976) Siderochromes in cyanophyceae: isolation and characterization of schizokinen from Anabaena sp. J Phycol 12:44–48

    Google Scholar 

  • Smayda TJ (1970) The suspension and sinking of phytoplankton in the sea. Oceanogr Mar Biol Ann Rev 8:353–414

    Google Scholar 

  • Smetacek V (1985) Role of sinking in diatom life history cycles: ecological, evolutionary and geological significance. Mar Biol 84:239–251

    Article  Google Scholar 

  • Smetacek V (1999) Diatoms and the ocean carbon cycle. Protist 150:25–32

    Article  CAS  PubMed  Google Scholar 

  • Smetacek V, Assmy P, Henjes J (2004) The role of grazing in structuring Southern Ocean pelagic ecosystems and biogeochemical cycles. Antarct Sci 16:541–558

    Article  Google Scholar 

  • Smetacek V, Klaas C, Strass VH, Assmy P, Montresor M, Cisewski B, Savoye N, Webb A, d’Ovidio F, Arrieta JM, Bathmann U, Bellerby R, Berg GM, Croot P, Gonzalez S, Henjes J, Herndl GJ, Hoffmann LJ, Leach H, Losch M, Mills MM, Neill C, Peeken I, Rottgers R, Sachs O, Sauter E, Schmidt MM, Schwarz J, Terbruggen A, Wolf-Gladrow D (2012) Deep carbon export from a Southern Ocean iron-fertilized diatom bloom. Nature 487:313–319

    Google Scholar 

  • Smith K, Robison B, Helly J, Kaufmann R, Ruhl H, Shaw T, Twining B, Vernat M (2007) Free-drifting icebergs: hot spots of chemical and biological enrichment in the Weddell Sea. Science 317:478–483

    Article  CAS  PubMed  Google Scholar 

  • Sohm JA, Webb EA, Capone DG (2011) Emerging patterns of marine nitrogen fixation. Nat Rev Microbiol 9:499–508

    Article  CAS  PubMed  Google Scholar 

  • Soria-Dengg S, Horstmann U (1995) Ferroxiamines B and E as iron source for the marine diatom Phaeodactylum tricornutum. Mar Ecol Prog Ser 127:269–277

    Article  CAS  Google Scholar 

  • Stearman R, Yuan DS, Yamaguchi-Iwai Y, Klausner RD, Dancis A (1996) A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 271:1552–1557

    Article  CAS  PubMed  Google Scholar 

  • Sterner RW, Smutka TM, McKay RM, Xiaoming Q, Brown ET, Sherrel R (2004) Phosphorus and trace metal limitation of algae and bacteria in Lake Superior. Limnol Oceanogr 49:495–507

    Article  CAS  Google Scholar 

  • Stevanovic M, Hahn A, Nicolaisen K, Mirus O, Schleiff E (2012) The components of the putative iron transport system in the cyanobacterium Anabaena sp. PCC 7120. Environ Microbiol 14:1655–1670

    Article  CAS  PubMed  Google Scholar 

  • Straus N (2004) Iron deprivation: physiology and gene regulation. In: Bryant D (ed) The molecular biology of cyanobacteria, Book 1. Springer, Dordrecht, pp 731–750

    Chapter  Google Scholar 

  • Strong A, Chisholm S, Miller C, Cullen J (2009) Ocean fertilization: time to move on. Nature 461:347–348

    Article  CAS  PubMed  Google Scholar 

  • Strzepek R, Harrison P (2004) Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431:689–692

    Article  CAS  PubMed  Google Scholar 

  • Strzepek RF, Price NM (2000) Influence of irradiance and temperature on the iron content of the marine diatom Thalassiosira weissflogii (Bacillariophyceae). Mar Ecol Prog Ser 206:107–117

    Article  CAS  Google Scholar 

  • Strzepek RF, Maldonado MT, Hunter KAFDR, Boyd PW (2011) Adaptive strategies by Southern Ocean phytoplankton to lessen iron limitation: uptake of organically complexed iron and reduced cellular iron requirements. Limnol Oceanogr 56:1983–2002

    Article  CAS  Google Scholar 

  • Strzepek RF, Hunter KA, Frew RD, Harrison PJ, Boyd PW (2012) Iron-light interactions in Southern Ocean phytoplankton. Limnol Oceanogr 57:1182–1200

    Article  CAS  Google Scholar 

  • Sugie K, Yoshimura T (2013) Effects of pCO2 and iron on the elemental composition and cell geometry of the marine diatom Pseudo-nitzschia pseudodelicatissima (Bacillariophyceae). J Phycol 49:475–488

    Article  CAS  Google Scholar 

  • Sugie K, Endo H, Suzuki K, Nishioka J, Kiyosawa H, Yoshimura T (2013) Synergistic effects of pCO2 and iron availability on nutrient consumption ratio of the Bering Sea phytoplankton community. Biogeosciences 10:6309–6321

    Article  CAS  Google Scholar 

  • Sunda WG, Huntsman SA (1992) Feedback interactions between zinc and phytoplankton in seawater. Limnol Oceanogr 37:25–40

    Article  CAS  Google Scholar 

  • Sunda W, Huntsman SA (1995) Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar Chemy 50:189–206

    Article  CAS  Google Scholar 

  • Sunda WG, Huntsman SA (1997) Interrelated influence of iron, light and cell size on marine phytoplankton growth. Nature 390:389–392

    Article  CAS  Google Scholar 

  • Sunda W, Huntsman S (2003) Effect of pH, light, and temperature on Fe-EDTA chelation and Fe hydrolysis in seawater. Mar Chem 84:35–47

    Article  CAS  Google Scholar 

  • Sunda WG, Huntsman SA (2011) Interactive effects of light and temperature on iron limitation in a marine diatom: implications for marine productivity and carbon cycling. Limnol Oceanogr 56:1475–1488

    Article  CAS  Google Scholar 

  • Sunda WG, Huntsman SA (2015) High iron requirement for growth, photosynthesis, and low-light acclimation in the coastal cyanobacterium Synechococcus bacillaris. Front Microbiol 6:561

    PubMed  PubMed Central  Google Scholar 

  • Sunda WG, Swift D, Huntsman S (1991) Low iron requirement for growth in oceanic phytoplankton. Nature 351:55–57

    Article  CAS  Google Scholar 

  • Sunda W, Kieber DJ, Kiene RP, Huntsman S (2002) An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–320

    Article  CAS  PubMed  Google Scholar 

  • Sunda WG, Price NM, Morel FMM (2005) Trace metal ion buffers and their use in culture studies. In: Anderson RA (ed) Algal culturing techniques. Elsevier Academic Press, London, pp 35–64

    Google Scholar 

  • Tagliabue A, Bopp L, Dutay J-C, Bowie AR, Chever F, Jean-Baptiste P, Bucciarelli E, Lannuzel D, Remenyi T, Sarthou G, Aumont O, Gehlen M, Jeandel C (2010) Hydrothermal contribution to the oceanic dissolved iron inventory. Nat Geosci 3:252–256

    Article  CAS  Google Scholar 

  • Takeda S (1998) Influence of iron availability on nutrient consumption ratio of diatoms in oceanic waters. Nature 393:774–777

    Article  CAS  Google Scholar 

  • Tang D, Morel FMM (2006) Distinguishing between cellular and Fe-oxide-associated trace elements in phytoplankton. Mar Chem 98:18–30

    Article  CAS  Google Scholar 

  • Taylor RL, Semeniuk DM, Payne CD, Zhou J, Tremblay J-E, Cullen JT, Maldonado MT (2013) Colimitation by light, nitrate, and iron in the Beaufort Sea in late summer. J Geophys Res 118:3260–3277

    Article  Google Scholar 

  • Tilzer M, Elbrachter M, Gieskes WWC, Beese B (1986) Light-temperature interactions in the control of photosynthesis in Antarctic phytoplankton. Polar Biol 5:105–112

    Article  Google Scholar 

  • Timmermans KR, Gerringa LJA, de Baar HJW, van der Wagt B, Veldhuis MJW, de Jong JTM, Croot PL, Boye M (2001) Growth rates of large and small Southern Ocean diatoms in relation to availability of iron in natural seawater. Limnol Oceanogr 46:260–266

    Article  Google Scholar 

  • Timmermans KR, van der Wagt B, de Baar HJW (2004) Growth rates, half-saturation constants, and silicate, nitrate, and phosphate depletion in relation to iron availability of four large, open-ocean diatoms from the Southern Ocean. Limnol Oceanogr 49:2141–2151

    Article  CAS  Google Scholar 

  • Timmermans KR, van der Wagt B, Veldhuis MJW, Maatman A, de Baar HJW (2005) Physiological responses of three species of marine pico-phytoplankton to ammonium, phosphate, iron and light limitation. J Sea Res 53:109–120

    Article  CAS  Google Scholar 

  • Trick CG, Bill BD, Cochlan WP, Wells ML, Trainer VL, Pickell LD (2010) Iron enrichment stimulates toxic diatom production in high-nitrate, low-chlorophyll areas. Proc Natl Acad Sci 107:5887–5892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Twining BS, Baines SB (2013) The trace metal composition of marine phytoplankton. Ann Rev Mar Sci 5:191–215

    Article  PubMed  Google Scholar 

  • Twining BS, Baines SB, Fisher NS, Maserr J, Vogt S, Jacobsen C, Tovar-Sanchez A, Sañudo-Wilhelmy SA (2003) Quantifying trace elements in individual aquatic protist cells with a synchrotron X-ray fluorescence microprobe. Anal Chem 75:3806–3816

    Article  CAS  PubMed  Google Scholar 

  • Twining BS, Baines SB, Fisher NS, Landry MR (2004) Cellular iron contents of plankton during the Southern Ocean Iron Experiment (SOFeX). Deep Sea Res I 51:1827–1850

    Article  CAS  Google Scholar 

  • Twining BS, Baines SB, Bozard JB, Vogt S, Walker EA, Nelson DM (2011) Metal quotas of plankton in the equatorial Pacific Ocean. Deep Sea Res II 58:325–341

    Article  CAS  Google Scholar 

  • Twiss MR, Auclair J-C, Charlton MN (2000) An investigation into iron-stimulated phytoplankton productivity in epipelagic Lake Erie during thermal stratification using trace metal clean techniques. Can J Fish Aquat Sci 57:86–95

    Article  CAS  Google Scholar 

  • Van Ho A, Ward DM, Kaplan J (2002) Transition metal transport in yeast. Annu Rev Microbiol 56:237–261

    Article  PubMed  CAS  Google Scholar 

  • van Oijen T, van Leeuwe MA, Gieskes WWC, de Baar HJW (2004) Effects of iron limitation on photosynthesis and carbohydrate metabolism in the Antarctic diatom Chaetoceros brevis (Bacillariophyceae). Eur J Phycol 39:161–171

    Article  CAS  Google Scholar 

  • Varsano T, Wolf SG, Pick U (2006) A chlorophyll a/b-binding protein homolog that is induced by iron deficiency is associated with enlarged photosystem I units in the eucaryotic alga Dunaliella salina. J Biol Chem 281:10305–10315

    Article  CAS  PubMed  Google Scholar 

  • Waite TD, Morel FMM (1984) Photoreductive dissolution of colloidal iron oxides in natural waters. Environ Sci Technol 18:860–868

    Article  CAS  PubMed  Google Scholar 

  • Weger HG (1999) Ferric and cupric reductase activities in the green alga Chlamydomonas reinhardtii: experiments using iron-limited chemostats. Planta 207:377–384

    Article  CAS  Google Scholar 

  • Weger HG, Middlemiss JK, Petterson CD (2002) Ferric chelate reductase activity as affected by the iron- limited growth rate in four species of unicellular green algae (Chlorophyta). J Phycol 38:513–519

    Article  CAS  Google Scholar 

  • Wells ML, Goldberg ED (1994) The distribution of colloids in the North Atlantic and Southern Oceans. Limnol Oceanogr 39:286–302

    Article  Google Scholar 

  • Wells ML, Price NM, Bruland KW (1995) Iron chemistry in seawater and its relationship to phytoplankton – a workshop report. Mar Chem 48:157–182

    Article  CAS  Google Scholar 

  • Weng H-X, Sun X-W, Qin Y-C, Chen J-F (2007) Effect of irradiance on Fe and P uptake by Cryptomonas sp. Geochimica 4:008

    Google Scholar 

  • Wetz MS, Hales B, Chase Z, Wheeler PA, Whitney MM (2006) Riverine input of macronutrients, iron, and organic matter to the coastal ocean off Oregon, USA, during the winter. Limnol Oceanogr 51:2221–2231

    Article  CAS  Google Scholar 

  • Whitney L, Lins J, Hughes M, Wells M, Chappell P, Jenkins B (2011) Characterization of putative iron responsive genes as species-specific indicators of iron stress in Thalassiosiroid diatoms. Front Microbiol 2:234. doi:10.3389/fmicb.2011.00234

    PubMed  PubMed Central  Google Scholar 

  • Wilhelm SW (1995) Ecology of iron-limited cyanobacteria: a review of physiological responses and implications for aquatic systems. Aquat Microb Ecol 9:295–303

    Article  Google Scholar 

  • Wolfe-Simon F, Grzebyk D, Schofield O, Falkowski PG (2005) The role and evolution of superoxide dismutases in algae. J Phycol 41:453–465

    Article  CAS  Google Scholar 

  • Zehr JP, Kudela RM (2009) Photosynthesis in the open ocean. Science 326:945–946

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Eide D (1996a) The yeast ZRT1 gene encodes the zinc transporter protein of a high-affinity uptake system induced by zinc limitation. Proc Natl Acad Sci 93:2454–2458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao H, Eide D (1996b) The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J Biol Chem 271:23203–23210

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank W.G. Sunda, P.J. Harrison and J.A. Raven for their helpful comments and insights on the manuscript. Supported by NSF-OCE 1334935 (A.M.).

Author information

Authors and Affiliations

  1. Department of Marine Sciences, University of North Carolina at Chapel Hill, Campus Box 3300, Chapel Hill, NC, 27599, USA

    Adrian Marchetti

  2. Department of Earth, Ocean and Atmospheric Sciences, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

    Maria T. Maldonado

Authors
  1. Adrian Marchetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria T. Maldonado
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adrian Marchetti .

Editor information

Editors and Affiliations

  1. School of Veterinary and Life Sciences, Murdoch University, Algae R&D Centre, Murdoch, West Australia, Australia

    Michael A. Borowitzka

  2. School of Biological Sciences, Monash University, Clayton, Victoria, Australia

    John Beardall

  3. Division of Plant Biology, University of Dundee at the James Hutton, Dundee, United Kingdom

    John A. Raven

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Marchetti, A., Maldonado, M.T. (2016). Iron. In: Borowitzka, M., Beardall, J., Raven, J. (eds) The Physiology of Microalgae. Developments in Applied Phycology, vol 6. Springer, Cham. https://doi.org/10.1007/978-3-319-24945-2_11

Download citation

Publish with us

Policies and ethics

Search

Navigation