Skip to main content
SpringerLink
Log in

Effects of Mn and Fe on growth of a coastal marine diatom Talassiosira weissflogii in the presence of precipitated Fe(III) hydroxide and EDTA-Fe(III) complex

  • Original Article
  • Chemistry and Biochemistry
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

The significance of Mn and Fe for the growth of the coastal marine diatom Thalassiosira weissflogii was investigated by culture experiments in the presence of precipitated Fe(III) hydroxide [am-Fe(III)] and EDTA-Fe(III) complex with or without Mn addition. The culture experiments in all media without any added Mn(II) resulted in the very low phytoplankton growth for cell density and chlorophyll a (Chl a) concentration. In contrast, sufficient Mn addition (25 nM) induced the maximum growth both for cell generation and Chl a production. By using an approach in which further iron uptake by T. weissflogii from external iron in the culture media is prevented by adding hydroxamate siderophore desferrioxamine B (DFB) during cultivation, we examined the ability of T. weissflogii to grow on intracellularly stored Fe after the DFB addition. The addition of DFB after 3- and 5-days of cultivation resulted in the lower growth rate and lower maximum yields for cell density and Chl a concentration in solid 7-day-aged am-Fe(III) medium than in freshly precipitated am-Fe(III) medium. The longer aging time of am-Fe(III) in medium reduced the supply of bioavailable iron in the medium by the slower dissolution rate of am-Fe(III) with the longer aging time. In addition, phytoplankton growth for cell generation in EDTA-Fe(III) complex media in the presence of insufficient Mn (0 and 5 nM) is strongly influenced by the bioavailable iron supply through the dissociation of EDTA-Fe(III). These results may suggest that T. weissflogii in longer aged am-Fe(III) medium and in EDTA-Fe(III) medium with a higher ratio of EDTA:Fe(III) is in Fe-limitation of growth, which probably increases the production rate of the reactive oxygen species (ROS), and the corresponding up-regulation of the superoxide dismuting enzyme Mn-SOD increases the requirement for Mn.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Weinberg ED (1989) Cellular regulation of iron assimilation. Q Rev Biol 64:261–290

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  3. Stumm W, Morgan JJ (1996) Aquatic Chemistry, 3rd edn. Wiley, New York

    Google Scholar 

  4. Waite TD (2001) Thermodynamics of the iron system in sweater. In: Turner DR, Hunter KA (eds) The biogeochemistry of iron in seawater. Wiley, New York, pp 291–342

    Google Scholar 

  5. Kuma K, Nishioka J, Matsunaga K (1996) Controls on iron(III) hydroxide solubility in seawater: the influence of pH and natural organic chelators. Limnol Oceanogr 41:396–407

    Article  CAS  Google Scholar 

  6. Nakabayashi S, Kusakabe M, Kuma K, Kudo I (2001) Vertical distributions of iron(III) hydroxide solubility and dissolved iron in the northwestern North Pacific Ocean. Geophys Res Lett 28:4611–4614

    Article  CAS  Google Scholar 

  7. Liu X, Millero FJ (2002) The solubility of iron in seawater. Mar Chem 77:43–54

    Article  CAS  Google Scholar 

  8. Chen M, Wang W-X, Guo L (2004) Phase partitioning and solubility of iron in natural seawater controlled by dissolved organic matter. Global Biogeochem Cycles 18:GB4013. doi:10.1029/2003GB002160

  9. Takata H, Kuma K, Iwade S, Isoda Y, Kuroda H, Senjyu T (2005) Comparative vertical distributions of iron in the Japan Sea, the Bering Sea and the western North Pacific Ocean. J Geophys Res 110:C07004. doi:10.1029/2004J002783

    Article  Google Scholar 

  10. van den Berg CMG (1995) Evidence for organic complexation of iron in seawater. Mar Chem 50:139–157

    Article  Google Scholar 

  11. 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 

  12. 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 

  13. Archer DE, Johnson KS (2000) A model of the iron cycle in the ocean. Global Biogeochem Cycles 14:269–279

    Article  CAS  Google Scholar 

  14. Kuma K, Isoda Y, Nakabayashi S (2003) Control on dissolved iron concentrations in deep waters in the western North Pacific: iron(III) hydroxide solubility. J Geophys Res 108(C9):3289. doi:10.1029/2002JC001481

    Article  Google Scholar 

  15. Hiemstra T, van Riemsdijk WH (2006) Biogeochemical speciation of Fe in ocean water. Mar Chem 102:181–197

    Article  CAS  Google Scholar 

  16. Kitayama S, Kuma K, Manabe E, Sugie K, Takata H, Isoda Y, Toya K, Saitoh S, Takagi S, Kamei Y, Sakaoka K (2009) Controls on iron distributions in the deep water column of the North Pacific Ocean: iron(III) hydroxide solubility and marine humic-type dissolved organic matter. J Geophys Res 114:C08019. doi:10.1029/2008JC004754

    Article  Google Scholar 

  17. Laglera LM, van den Berg CMG (2009) Evidence for geochemical control of iron by humic substances in seawater. Limnol Oceanogr 54:610–619

    Article  CAS  Google Scholar 

  18. Wu J, Boyle E, Sunda WG, Wen L-S (2001) Soluble and colloidal iron in the oligotrophic North Atlantic and North Pacific. Science 293:847–849

    Article  PubMed  CAS  Google Scholar 

  19. Wells ML, Zorkin NG, Lewis AG (1983) The role of colloid chemistry in providing a source of iron to phytoplankton. J Mar Res 41:731–746

    Article  CAS  Google Scholar 

  20. Rich HW, Morel FMM (1990) Availability of well-defined iron colloids to the marine diatom Thalassiosira weissflogii. Limnol Oceanogr 35:652–662

    Article  CAS  Google Scholar 

  21. Kuma K, Matsunaga K (1995) Availability of colloidal ferric oxides to coastal marine phytoplankton. Mar Biol 122:1–11

    Article  CAS  Google Scholar 

  22. 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. Mar Biol 149:379–392

    Article  CAS  Google Scholar 

  23. Iwade S, Kuma K, Isoda Y, Yoshida M, Kudo I, Nishioka J, Suzuki K (2006) Effect of high iron concentrations on iron uptake and growth of a coastal diatom Chaetoceros sociale. Aquat Microb Ecol 43:177–191

    Article  Google Scholar 

  24. Moffett JW (2001) Transformations among different forms of iron in the ocean. In: Tuner DR, Hunter KA (eds) The biogeochemistry of iron in seawater. Wiley, New York, pp 343–372

    Google Scholar 

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

    Article  CAS  Google Scholar 

  26. 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 

  27. 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 

  28. Sunda WG (2001) Bioavailability and bioaccumulation of iron in the sea. In: Turner DR, Hunter KA (eds) The biogeochemistry of iron in seawater. Wiley, New York, pp 41–84

    Google Scholar 

  29. Ringbom A (1963) Complexation in analytical chemistry. Wiley, New York

    Google Scholar 

  30. Hudson RJM, Covault DT, Morel FMM (1992) Investigations of iron coordination and redox reactions in seawater using 59Fe radiometry and ion-pair solvent extraction of amphiphilic iron complexes. Mar Chem 38:209–235

    Article  CAS  Google Scholar 

  31. Sunda WG, Price NM, Morel FMM (2005) Trace metal ion buffers and the use in culture studies. In: Andersen RA (ed) Algal culturing techniques. Elsevier, New York, pp 35–63

    Chapter  Google Scholar 

  32. Fujii M, Rose AL, Wait TD, Omura T (2008) Effect of divalent cations on the kinetics of Fe(III) complexation by organic ligands in natural waters. Geochim Cosmochim Acta 72:1335–1349

    Article  CAS  Google Scholar 

  33. Kuma K, Tanaka J, Matsunaga K (1999) Effect of natural and synthetic organic-Fe(III) complexes in an estuarine mixing model on iron uptake and growth of a coastal marine diatom, Chaetoceros sociale. Mar Biol 134:761–769

    Article  CAS  Google Scholar 

  34. Kuma K, Tanaka J, Matsunaga K, Matsunaga K (2000) Effect of hydroxamate ferrisiderophore complex (ferrichrome) on iron uptake and growth of a coastal marine diatom, Chaetoceros sociale. Limnol Oceanogr 45:1235–1244

    Article  CAS  Google Scholar 

  35. Sunda WG, Huntsman SA (1988) Effect of sunlight on redox cycles of manganese in the southwestern Sargasso Sea. Deep Sea Res 35:1297–1317

    Article  CAS  Google Scholar 

  36. Emerson S, Kalhorn S, Jacobs L, Tebo BM, Nealson KH, Rosson RA (1982) Environmental oxidation rate of manganese(II): bacterial catalysis. Geochim Cosmochim Acta 46:1073–1079

    Article  CAS  Google Scholar 

  37. Bruland KW, Donat JR, Hutchins DA (1991) Interractive influences of bioactive trace metals on biological production in oceanic waters. Limnol Oceanogr 36:1555–1577

    Article  CAS  Google Scholar 

  38. Obata H, Doi T, Hongo Y, Alibo DS, Minami H, Kato Y, Maruo M (2007) Manganese, cerium and iron in the Sulu, Celebes and Phillipine Seas. Deep Sea Res II 54:38–49

    Article  CAS  Google Scholar 

  39. Noble AE, Saito MA, Maiti K, Benitez-Nelson CR (2008) Cobalt, manganese, and iron near the Hawaiian Islands: a potential concentrating mechanism for cobalt within a cyclonic eddy and implications for the hybrid-type trace metals. Deep Sea Res II 55:1473–1490

    Article  Google Scholar 

  40. Johnson KS, Berelson WM, Coale KH, Coley TL, Elrod VA, Fairey WR, Lams HD, Kilgore TE, Nowicki JL (1992) Manganese flux from continental margin sediments in a transect through the oxygen minimum. Science 257:1242–1245

    Article  PubMed  CAS  Google Scholar 

  41. Bucciarelli E, Blain S, Treguer P (2001) Iron and manganese in the wake of the Kerguelen Islands (Southern Ocean). Mar Chem 73:21–36

    Article  CAS  Google Scholar 

  42. Delgadillo-Hinojosa F, Segovia-Zavala JA, Huerta-Diaz MA, Atilano-Silva H (2006) Influence of geochemical and physical processes on the vertical distribution of manganese in Gulf of California waters. Deep Sea Res I 53:1301–1319

    Article  CAS  Google Scholar 

  43. Burnell JN (1988) The biochemistry of manganese in plants. In: Graham RG, Hannam RJ, Uren NC (eds) Manganese in soils and plants. Kluwer, New York, pp 125–137

    Google Scholar 

  44. Brand LE, Sunda WG, Guillard RRL (1983) Limitation of marine phytoplankton reproductive rates by zinc, manganese, and iron. Limnol Oceanogr 28:1182–1198

    Article  CAS  Google Scholar 

  45. Coale KH (1991) Effects of iron, manganese, copper, and zinc enrichments on productivity and biomass in the subarctic Pacific. Limnol Oceaogr 36:1851–1864

    Article  CAS  Google Scholar 

  46. Obata H, Karatani H, Nakayama E (1993) Automated determination of iron in seawater by chelating resin concentration and chemiluminescence detection. Anal Chem 65:1524–1528

    Article  CAS  Google Scholar 

  47. Sohrin Y, Urushihara S, Nakatsuka S, Kono T, Higo E, Minami T, Norisuye K, Umetani S (2008) Multielemental determination of GEOTRACES key trace metals in seawater by ICPMS after preconcentration using an ethylenediaminetriacetic acid chelating resin. Anal Chem 80:6267–6273

    Article  PubMed  CAS  Google Scholar 

  48. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Gleve) Gran. Can J Microbiol 8:229–239

    Article  PubMed  CAS  Google Scholar 

  49. Morel FMM, Rueter JG, Andersen DM, Guillard RRL (1979) Aquil: a chemistry defined phytoplankton culture medium for trace metal studies. J Phycol 15:135–141

    Article  CAS  Google Scholar 

  50. Wells ML, Price NM, Bruland KW (1994) Iron limitation and the cyanobacterium Synechococcus in equatorial Pacific waters. Limnol Oceanogr 39:1481–1486

    Article  CAS  Google Scholar 

  51. Wells ML (1999) Manipulating iron availability in nearshore waters. Limnol Oceanogr 44:1002–1008

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  53. Wells ML, Trick CG (2004) Controlling iron availability to phytoplankton in iron-replete coastal waters. Mar Chem 86:1–13

    Article  CAS  Google Scholar 

  54. Suzuki R, Ishimaru T (1990) An improved method for the determination of phytoplankton chlorophyll using N,N-dimethylformamide. J Oceanogr Soc Jpn 46:190–194

    Article  CAS  Google Scholar 

  55. Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the present of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–1992

    Article  CAS  Google Scholar 

  56. 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 Res I 45:91–113

    Article  CAS  Google Scholar 

  57. Fraust da Silva JJR, Williams RJP (2001) The biological chemistry of the elements: the inorganic chemistry of life, 2nd edn. Oxford University Press, New York

    Google Scholar 

  58. Chrichton RR (2001) Inorganic biochemistry of iron metabolism: from molecular mechanisms to clinical consequences, 2nd edn. Wiley, New York

    Google Scholar 

  59. Wolfe-Simon F, Starovoytov V, Reinfelder JR, Schofield O, Falkowski PG (2006) Localization and role of manganese superoxide dismutase in a marine diatom. Plant Physiol 142:1701–1709

    Article  PubMed  CAS  Google Scholar 

  60. Qiu B, Price NM (2009) Different physiological responses of four marine Synechococcus strains (Cyanophyceae) to nickel starvation under iron-replete and iron-deplete conditions. J Phycol 45:1062–1071

    Article  CAS  Google Scholar 

  61. Ushizaka S, Sugie K, Yamada M, Kasahara M, Kuma K (2008) Significance of Mn and Fe for growth of coastal marine diatom Thalassiosira weissflogii. Fish Sci 74:1137–1145

    Article  CAS  Google Scholar 

  62. Peers G, Price NM (2004) A role for manganese in superoxide dismutases and growth of iron-deficient diatoms. Limnol Oceanogr 49:1774–1783

    Article  CAS  Google Scholar 

  63. Sunda WG, Huntsman SA (1995) Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar Chem 50:189–206

    Article  CAS  Google Scholar 

  64. 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 

  65. Hudson RJM, Morel FMM (1989) Distinguishing between extra- and intracellular iron in marine phytoplankton. Limnol Oceanogr 34:1113–1120

    Article  CAS  Google Scholar 

  66. 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 

Download references

Acknowledgments

We thank Dr. H. Takata for technical assistance. We are grateful to two anonymous reviewers for their constructive and helpful comments on this work. This study was partially supported by a grant for Scientific Research (no. 22510001) from the Ministry of Education, Culture, Sports, Science and Technology, Japan.

Author information

Authors and Affiliations

  1. Graduate School of Environmental Science, Hokkaido University, Kita 10, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan

    Satomi Ushizaka, Kenshi Kuma & Koji Suzuki

  2. Faculty of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate, Hokkaido, 041-8611, Japan

    Kenshi Kuma

  3. Faculty of Environmental Earth Science, Hokkaido University, Kita 10, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan

    Koji Suzuki

Authors
  1. Satomi Ushizaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kenshi Kuma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Koji Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kenshi Kuma.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ushizaka, S., Kuma, K. & Suzuki, K. Effects of Mn and Fe on growth of a coastal marine diatom Talassiosira weissflogii in the presence of precipitated Fe(III) hydroxide and EDTA-Fe(III) complex. Fish Sci 77, 411–424 (2011). https://doi.org/10.1007/s12562-011-0339-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-011-0339-6

Keywords

Search

Navigation