Skip to main content
SpringerLink
Log in

Effect of iron complexes with seawater extractable organic matter on oogenesis in gametophytes of a brown macroalga (Saccharina japonica)

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The phenomenon of macroalgae depletion is a serious worldwide problem in terms of the destruction of ecosystems and reducing carbon fixation capacity in coastal areas. A lack of dissolved Fe is thought to be one of reasons for this phenomenon, and attempts have been made to develop Fe fertilization techniques. This study reports on the bioavailability of Fe species that are complexed with seawater extractable organic matter (SWEOM) derived from a compost and various chelators on oogenesis in a brown macroalga (Saccharina japonica). Oogenesis is induced by Fe uptake. Oogenesis assays indicate that Fe uptake can be explained by a ligand exchange reaction, suggesting that dissolved Fe in the form of a labile complex species could be used as a fertilizer. Fifty to eighty percent of gametophytes induced oogenesis in the presence of 0.16–0.27 μM Fe species complexed with SWEOM. However, no oogenesis was observed in the presence of 1 μM Fe species complexed with N,N'-bis(2-hydroxybenzyl)ethylenediamine-N,N'-diacetic acid, an inert Fe-containing complex. These results show that SWEOM can serve as a chelator for Fe fertilization. Moreover, the concentration of SWEOM extracted from a bark compost was more than ten times higher than the corresponding values obtained from dredged soil and peat, suggesting this type of compost represents a suitable source of SWEOM. These findings extend our current knowledge of the use of Fe fertilization for the restoration of seaweed beds.

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

Similar content being viewed by others

References

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

    Article  CAS  Google Scholar 

  • Aristilde L, Xu Y, Morel FMM (2010) Weak organic ligands enhance zinc uptake in marine phytoplankton. Environ Sci Technol 46:5438–5445

    Article  Google Scholar 

  • Bartsch I, Wiencke C, Bishof K, Buchholz CM, Buck BH, Eggert A, Feuerpfeil P, Hanelt D, Jacobsen S, Karez R, Karsten U, Molis M, Roleda MY, Schubert H, Schumann R, Valentin K, Wweinberger F, Wiese J (2008) The genus Laminaria sensu lato: recent insights and development. Eur J Phycol 43:1–86

    Article  Google Scholar 

  • Böttger LH, Miller EP, Anderson C, Matzanke BF, Küpper FC, Carrano CJ (2012) Atypical iron storage in marine brown algae: a multidisciplinary study of iron transport and storage in Ectocarpus siliculosus. J Exp Bot 63:5763–5772

    Article  PubMed Central  PubMed  Google Scholar 

  • Chapman ARO (1981) Stability of sea urchin dominated barren grounds following destructive grazing of kelp in St. Margaret’s Bay, Eastern Canada. Mar Biol 62:307–311

    Article  Google Scholar 

  • Chen M, Wang WX (2001) Bioavailability of natural colloid-bound iron to marine plankton: influences of colloidal size and aging. Limnol Oceanogr 46:1956–1967

    Article  CAS  Google Scholar 

  • Chen M, Wang WX (2008) Accelerated uptake by phytoplankton of iron bound to humic acids. Aquat Biol 3:155–166

    Article  Google Scholar 

  • Chung IK, Beardall J, Mehta S, Sahoo D, Stijkovic S (2011) Using marine macroalgae for carbon sequestration: a critical appraisal. J Appl Phycol 23:877–886

    Article  CAS  Google Scholar 

  • Fujita D (2010) Current status and problems of isoyake in Japan. Bull Fish Res Agen 32:33–42

    Google Scholar 

  • Gao K, McKinley KR (1994) Use of macroalgae for marine biomass production and CO2 remediation: a review. J Appl Phycol 6:45–60

    Article  Google Scholar 

  • Gobler CJ, Donat JR, Consolvo JA III, Sañudo-Wilhelmy SA (2002) Physicochemical speciation of iron during coastal algal blooms. Mar Chem 77:71–89

    Article  CAS  Google Scholar 

  • Hassler CS, Schoemann V (2009) Bioavailability of organically bound Fe to model phytoplankton of the Southern Ocean. Biogeosci Discuss 6:1677–1712

    Article  Google Scholar 

  • Hassler CS, Twiss MR (2006) Bioavailability of iron sensed by a phytoplanktonic Fe-bioreporter. Environ Sci Technol 40:2544–2551

    Article  CAS  PubMed  Google Scholar 

  • Hirose K (2007) Metal-organic matter interaction: ecological roles of ligands in oceanic DOM. Appl Geochem 22:1636–1645

    Article  CAS  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 

  • Iwai H, Fukushima M, Yamamoto M (2012) Binding characteristics and dissociation kinetics for iron(II) complexes with seawater extractable organic matter and humic substances in a compost. Anal Sci 28:819–821

    Article  CAS  PubMed  Google Scholar 

  • Iwai H, Fukushima M, Yamamoto M (2013a) Determination of labile Fe(II) species complexed with seawater extractable organic matter under seawater conditions based on the kinetics of ligand-exchange reactions with ferrozine. Anal Sci 29:723–728

    Article  CAS  PubMed  Google Scholar 

  • Iwai H, Fukushima M, Yamamoto M, Komai T, Kawabe Y (2013b) Characterization of seawater extractable organic matter from bark compost by TMAH-py-GC/MS. J Anal Appl Pyrolysis 99:9–15

    Article  CAS  Google Scholar 

  • Kawachi M, Noël MH (2005) Sterilization and sterile technique. In: Anderson RA (ed) Algal culturing technique. Elsevier Academic Press, Burlington, pp 65–81

    Google Scholar 

  • Kuma K, Suzuki Y, Matsunaga K (1993) Solubility and dissolution rate of colloidal γ-FeOOH in seawater. Water Res 27:651–657

    Article  CAS  Google Scholar 

  • Lobban CS, Harrison PJ (2000) Seaweed ecology and physiology. Cambridge University Press, Cambridge

    Google Scholar 

  • Lüning K (1981) Egg release in gametophytes of Laminaria saccharina: induction by darkness and inhibition by blue light and u.v. Br Phycol J 16:379–393

    Article  Google Scholar 

  • Lüning K, Neushul M (1978) Light and temperature demands for growth and reproduction of Laminarian gametophytes in southern and central California. Mar Biol 45:297–309

    Article  Google Scholar 

  • Macrellis MM, Trick CG, Rue EL, Smith G, Bruland KW (2001) Collection and detection of natural iron-binding ligands from seawater. Mar Chem 76:175–187

    Article  CAS  Google Scholar 

  • Mann KH (1977) Destruction of kelp-beds by sea-urchins: a cyclical phenomenon or irreversible degradation? Helgol Wiss Meeresunters 30:455–467

    Article  Google Scholar 

  • Matsunaga K, Kawaguchi T, Suzuki Y, Nigi G (1999) The role of terrestrial humic substances on the shift of kelp community to crustose coralline algae community of the southern Hokkaido Island in the Japan Sea. J Exp Mar Biol Ecol 241:193–205

    Article  Google Scholar 

  • Matsunaga K, Suzuki Y, Kuma K, Kudo I (1994) Diffusion of Fe(II) from an iron propagation cage and its effect on tissue iron and pigments of macroalgae on the cage. J Appl Phycol 6:397–403

    Article  CAS  Google Scholar 

  • Millar AJK (2003) The world’s first recorded extinction of a seaweed. In: Chapman ARO, Anderson RJ, Vreeland VJ, Davison IR (eds) Proceedings of the 17th International Seaweed Symposium. Oxford University Press, Oxford, pp 313–318

    Google Scholar 

  • Morel FMM, Kustka AB, Shaked Y (2008) The role of unchelated Fe in the iron nutrition of phytoplankton. Limnol Oceanogr 53:400–404

    Article  CAS  Google Scholar 

  • Motomura T, Sakai Y (1981) Effect of chelated iron in culture media on oogenesis in Laminaria angustata. Bull Japan Soc Sci Fish 47:1535–1540

    Article  CAS  Google Scholar 

  • Motomura T, Sakai Y (1984) Regulation of gametogenesis of Laminaria and Desmarestia (Pheaophyta) by iron and boron. Jpn J Phycol 32:209–215

    CAS  Google Scholar 

  • Naito K, Imai I, Nakahara H (2008) Complexation of iron by microbial siderophores and effects of iron chelates on the growth of marine microalgae causing red tides. Phycol Res 56:58–67

    Article  CAS  Google Scholar 

  • Okuda K (2008) Coastal environment and seaweed-bed ecology in Japan. Kuroshio Sci 2:15–20

    Google Scholar 

  • Pettit G, Pettit LD (1999) SC-Database. IUPAC, Academic Software

  • Provasoli L (1963) Growing marine seaweeds. In: DeVirville D, Feldmann J (eds) Proceeding of the 4th International Seaweed Symposium. Pergamon Press, New York, pp 9–17

    Google Scholar 

  • Rico JM, Guiry MD (1997) Life history and reproduction of Gelidium maggsiae sp. nov. (Rhodophyta, Gelidiales) from Ireland. Eur J Phycol 32:267–277

    Article  Google Scholar 

  • Schneider R, Hartmann A, Braun V (1981) Transport of the iron ionophore ferrichrome in Escherichia coli K-12 and Salmonella typhimurium LT2. FEMS Microbiol Lett 11:115–119

    Article  CAS  Google Scholar 

  • 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 

  • Suzuki Y, Kuma K, Matsunaga K (1994) Effect of iron on oogonium formation, growth rate and pigment synthesis of Laminaria japonica (Phaeophyta). Fish Sci 60:373–378

    CAS  Google Scholar 

  • Suzuki Y, Kuma K, Matsunaga K (1995) Bioavailable iron species in seawater measured by macroalga (Laminaria japonica) uptake. Mar Biol 123:173–178

    Article  CAS  Google Scholar 

  • Tegner MJ, Dayton PK (1991) Sea urchins, El Niños, and the long term stability of southern California kelp forest communities. Mar Ecol Prog Ser 77:49–63

    Article  Google Scholar 

  • Tipping E (2002) Cation binding by humic substances. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Yamamoto M, Fukushima M, Kiso E, Kato T, Shibuya M, Otsuka K, Nishida A, Komai T (2010) Application of iron-humates to a coastal areas of barren ground for restoring seaweed bed. J Chem Eng Jpn 43:627–634

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Marine System Engineering, Graduate School of Engineering, Osaka Prefecture University, Sakai, 599-8531, Japan

    Hisanori Iwai

  2. Division of Sustainable Resource Engineering, Graduate School of Engineering, Hokkaido University, Sapporo, 060-8628, Japan

    Masami Fukushima

  3. Muroran Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, Muroran, 051-0013, Japan

    Taizo Motomura

  4. R & D Laboratories, Nippon Steel & Sumitomo Metal Corporation, Futtsu, 293-8511, Japan

    Toshiaki Kato & Chika Kosugi

Authors
  1. Hisanori Iwai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masami Fukushima
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Taizo Motomura
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Toshiaki Kato
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chika Kosugi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hisanori Iwai.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 222 kb)

ESM 2

(PDF 188 kb)

ESM 3

(PDF 148 kb)

ESM 4

(PDF 345 kb)

ESM 5

(PDF 298 kb)

ESM 6

(PDF 283 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Iwai, H., Fukushima, M., Motomura, T. et al. Effect of iron complexes with seawater extractable organic matter on oogenesis in gametophytes of a brown macroalga (Saccharina japonica). J Appl Phycol 27, 1583–1591 (2015). https://doi.org/10.1007/s10811-014-0479-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-014-0479-z

Keywords

Search

Navigation