Skip to main content
Log in

Effects of cobalt on spore germination, gametophyte growth and development, and juvenile sporophyte growth of Saccharina japonica (Phaeophyceae)

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

Abstract

Cobalt (Co), an essential element that is toxic in excess amounts, is a major component of wastewater that has accidentally been released from nuclear power plants. However, the effects of Co in seawater on the life cycle of macroalgae have seldom been investigated. Here, we tested the effects of different Co concentrations (1, 10, 50, 100, 200, 500, and 1000 μg L−1) on spore germination, gametophyte growth and development, and juvenile sporophyte growth of the brown alga Saccharina japonica. Sterilized natural seawater with a known Co concentration was used as the control. The spore germination percentage in the 1000 μg L−1 group was significantly reduced after 1 and 2 days of exposure. The gametophyte growth in the 1 μg L−1 group was significantly accelerated, while that of the ≥ 50 μg L−1 groups was significantly inhibited after 9 days of exposure. The relative growth rate and maximum quantum yield (Fv/Fm) of photosystem II of the juvenile sporophytes in the 1 μg L−1 group were significantly higher, while those of the ≥ 10 μg L−1 groups were significantly lower after 2 weeks of exposure. By culturing the sporophytes in the control medium, Fv/Fm values recovered from Co stress within 4 days. These results highlight the potentially severe impact of accidentally released Co from nuclear power plants on the life cycle of S. japonica. Further studies should focus on the toxic mechanism of Co in S. japonica and the phytoremediation potential of seaweeds to alleviate Co pollution.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ahmadpour A, Tahmasbi M, Bastami TR, Besharati JA (2009) Rapid removal of cobalt ion from aqueous solutions by almond green hull. J Hazard Mater 166:925–930

    Article  CAS  Google Scholar 

  • Aoyama M, Hamajima Y, Hult M, Uematsu M, Oka E, Tsumune D, Kumamoto Y (2016) 134Cs and 137Cs in the North Pacific Ocean derived from the March 2011 TEPCO Fukushima Dai-ichi Nuclear Power Plant accident, Japan. Part one: surface pathway and vertical distributions. J Oceanogr 72:53–65

    Article  CAS  Google Scholar 

  • Bartsch I, Wiencke C, Bischof 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, Weinberger F, Wiese J (2008) The genus Laminaria sensu lato: recent insights and developments. Eur J Phycol 43:1–86

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

  • Bollen M, Pilditch CA, Battershill CN, Bischof K (2016) Salinity and temperature tolerance of the invasive alga Undaria pinnatifida and native New Zealand kelps: implications for competition. Mar Biol 163:194

    Article  Google Scholar 

  • Buesseler K, Aoyama M, Fukasawa M (2011) Impacts of the Fukushima nuclear power plants on marine radioactivity. Environ Sci Tech 45:9931–9935

    Article  CAS  Google Scholar 

  • Buesseler KO, Jayne SR, Fisher NS, Rypina II, Baumann H, Baumann Z, Breier CF, Douglass EM, George J, Macdonald AM (2012) Fukushima-derived radionuclides in the ocean and biota off Japan. Proc Natl Acad Sci USA 109:5984–5988

    Article  CAS  Google Scholar 

  • Chatterjee J, Chatterjee C (2000) Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ Pollut 109:69–74

    Article  CAS  Google Scholar 

  • Chino M, Nakayama H, Nagai H, Terada H, Katata G, Yamazawa H (2011) Preliminary estimation of release amounts of 131I and 137Cs accidentally discharged from the Fukushima Daiichi Nuclear Power Plant into the atmosphere. J Nucl Sci Technol 48:1129–1134

    Article  CAS  Google Scholar 

  • Endo S, Kimura S, Takatsuji T, Nanasawa K, Imanaka T, Shizuma K (2012) Measurement of soil contamination by radionuclides due to the Fukushima Dai-ichi Nuclear Power Plant accident and associated estimated cumulative external dose estimation. J Environ Radioact 111:18–27

    Article  CAS  Google Scholar 

  • Fishery Bureau of Ministry of Agriculture of China (2018) China fishery statistical yearbook, 2018. China Agriculture Press, Beijing China, p23 (in Chinese)

  • Fukuda SY, Iwamoto K, Atsumi M, Yokoyama A, Nakayama T, Ishida K, Inouye I, Shiraiwa Y (2014) Global searches for microalgae and aquatic plants that can eliminate radioactive cesium, iodine and strontium from the radio-polluted aquatic environment: a bioremediation strategy. J Plant Res 127:79–89

    Article  CAS  Google Scholar 

  • Hosono Y, Takahashi H (2013) Radioactive contamination by the accident of the Fukushima Daiichi nuclear power plant, and the transition of the radioactive concentration-measurement of the tea leaf etc. of Bunkyo-ku Hongo and Tokorozawa. Radioisotopes 62:21–25

    Article  Google Scholar 

  • Karuppanapandian T, Kim W (2013) Cobalt-induced oxidative stress causes growth inhibition associated with enhanced lipid peroxidation and activates antioxidant responses in Indian mustard (Brassica juncea L.) leaves. Acta Physiol Plant 35:2429–2443

    Article  CAS  Google Scholar 

  • Kawai H, Kitamura A, Mimura M, Mimura T, Tahara T, Aida D, Sato K, Sasaki H (2014) Radioactive cesium accumulation in seaweeds by the Fukushima 1 Nuclear Power Plant accident-two years’ monitoring at Iwaki and its vicinity. J Plant Res 127:23–42

    Article  CAS  Google Scholar 

  • Kudesia VP (1990) Water pollution. Pregatiprakashan Publications, Meerut

    Google Scholar 

  • Lewis RJ, Green MK, Afzal ME (2013) Effects of chelated iron on oogenesis and vegetative growth of kelp gametophytes (Phaeophyceae). Phycol Res 61:46–51

    Article  CAS  Google Scholar 

  • Li L, Wang D, He J, Dai W, Zeng C, Chen L (2015) Research of germination characteristics and cobalt accumulation abilities of nine kinds of plant seeds under the cobalt stress. J Anhui Agri Sci 43:246–249 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Li M, Jin XU, Liu ZL, Jun XU (2004) Strontium stress on marine microalgae Dicrateria inornata growth and antioxidant enzymes activities. Oceanol Limnol Sinica 35:467–472

    CAS  Google Scholar 

  • Linna (2004) Exposure to cobalt in the production of cobalt and cobalt compounds and its effect on the heart. Occup Environ Med 61:877–885

    Article  CAS  Google Scholar 

  • Lwalaba JL, Zvobgo G, Fu L, Zhang X, Mwamba TM, Muhammad N, Mundende RP, Zhang G (2017) Alleviating effects of calcium on cobalt toxicity in two barley genotypes differing in cobalt tolerance. Ecotoxicol Environ Saf 139:488–495

    Article  CAS  Google Scholar 

  • Manohar VDM, Noeline BF, Anirudhan TS (2006) Adsorption performance of Al-pillared bentonite clay for the removal of cobalt (II) from aqueous phase. Appl Clay Sci 31:194–206

    Article  CAS  Google Scholar 

  • Musapatika ET, Singh R, Moodley K, Charles N, Onyango M, Ochieng A (2012) Cobalt removal from wastewater using pine sawdust. Afr J Biotechnol 11:9407–9415

    CAS  Google Scholar 

  • Nonova T, Tosheva Z (2014) Cesium and strontium in Black Sea macroalgae. J Environ Radioact 129:48–56

    Article  CAS  Google Scholar 

  • Öquist G, Hagström Å, Alm P, Samuelsson G, Richardson K (1982) Chlorophyll a fluorescence, an alternative method for estimating primary production. Mar Biol 68:71–75

    Article  Google Scholar 

  • Plekhanov SE, Chemeris YK (2003) Early toxic effects of zinc, cobalt, and cadmium on photosynthetic activity of the green alga Chlorella pyrenoidosa Chick S-39. Biol Bull Rus Acad Sci 30:506–511

    Article  CAS  Google Scholar 

  • Provasoli L (1968) Media and prospects for the cultivation of marine algae. In Cultures and Collections of Algae. Proceedings of the US-Japan Conference, Hakone, September 1966, pp 63-75. Japanese Society for Plant Physiology

  • Sree KS, Keresztes A, Mueller-Roeber B, Brandt R, Eberius M, Fischer W, Appenroth KJ (2015) Phytotoxicity of cobalt ions on the duckweed Lemna minor - morphology, ion uptake, and starch accumulation. Chemosphere 131:149–156

    Article  CAS  Google Scholar 

  • Shan TF, Liu F, Liu QS, Pang SJ (2011) Review and prospect of “Summer Sporeling” technique of Saccharina japonica in China. J Agric Sci Technol 13:129–134 (in Chinese with English abstract)

    Google Scholar 

  • Su L, Pang SJ, Shan TF, Li X (2017) Large-scale hatchery of the kelp Saccharina japonica: a case study experience at Lvshun in northern China. J Appl Phycol 29:3003–3013

    Article  Google Scholar 

  • TEPCO (The Tokyo Electric Power Co., Inc.) (2012) About the estimation of the total amount of radioactive materials released to the atmosphere by the accident of the Fukushima Daiichi nuclear power plant. Press Release: 2012 (in Japanese)

  • Terada H, Katata G, Chino M, Nagai H (2012) Atmospheric discharge and dispersion of radionuclides during the Fukushima Dai-ichi Nuclear Power Plant accident. Part II: verification of the source term and analysis of regional-scale atmospheric dispersion. J Environ Radioact 112:141–154

    Article  CAS  Google Scholar 

  • Tseng CK, Sun KY, Wu CY (1955) On the cultivation of Haitai (Laminaria japonica Aresch.) by summering young sporophytes at low temperature. Acta Bot Sin 4:255–264

    Google Scholar 

  • Tseng CK (2001) Algal biotechnology industries and research activities in China. J Appl Phycol 13:375–380

    Article  Google Scholar 

  • Tsushima I (2017) Behavior of radioactive materials and safety stock of contaminated sludge. Environ Lett 52:158–165

    CAS  Google Scholar 

  • Wang J, Tang Y, Xu J, Xu G, Zou Y, Chen H (2015) Accumulation and distribution of cobalt in broad bean and its effects on the photosynthesis and antioxidant enzyme activities. Acta Bot Boreal – Occident Sin 35:963–970 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Wang WJ, Sun XT, Wang GC, Xu P, Wang XY, Lin ZL, Wang FJ (2010) Effect of blue light on indoor seedling culture of Saccharina japonica (Phaeophyta). J Appl Phycol 22:737–744

    Article  Google Scholar 

  • Wang XM, Shan TF, Pang SJ (2018) Phytoremediation potential of Saccharina japonica and Sargassum horneri (Phaeophyceae): biosorption study of strontium. Bull Environ Contam Toxicol 101:501–505

    Article  CAS  Google Scholar 

  • Wang XM, Shan TF, Pang SJ (2019) Effects of cobalt on spore germination, gametophyte growth and gametogenesis of Undaria pinnatifida (Phaeophyceae). Bull Environ Contam Toxicol 102:784–788

    Article  CAS  Google Scholar 

  • Wu C, Lin G (1987) Progress in the genetics and breeding of economic seaweeds in China. Hydrobiologia 151:57–61

    Google Scholar 

  • Xiao HQ, Zhu S, Wang HW (2011) Risk assessment on the Japan Fukushima nuclear accident. J Inspect Quarant 21:68–71 (in Chinese with English abstract)

    Google Scholar 

  • Zhuang ST, Yin YN, Wang JL (2018) Simultaneous detection and removal of cobalt ions from aqueous solution by modified chitosan beads. Int J Environ Sci Te 15:385–394

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Natalie Kim, PhD, from Liwen Bianji, Edanz Editing China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript. We are grateful to Suqin Gao and Cuimei Zhang for their assistance in algal culture in the laboratory.

Funding

This research was supported by grants from the State’s Key Project of Research and Development Plan (2016YFC1402507), National Key Technology Support Program (2015BAD13B05), China Agriculture Research System (CARS-50), the Taishan Scholar Program of Shandong Province, and the Foundation for Huiquan Scholar of Institute of Oceanology, Chinese Academy of Sciences.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Tifeng Shan or Shaojun Pang.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 38 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Shan, T. & Pang, S. Effects of cobalt on spore germination, gametophyte growth and development, and juvenile sporophyte growth of Saccharina japonica (Phaeophyceae). J Appl Phycol 32, 511–518 (2020). https://doi.org/10.1007/s10811-019-01955-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-019-01955-x

Keywords

Navigation