Skip to main content
Log in

Oxidative stress responses to cadmium in the seedlings of a commercial seaweed Sargassum fusiforme

  • Published:
Acta Oceanologica Sinica Aims and scope Submit manuscript

Abstract

Cadmium (Cd) is a common heavy metal pollutant in the aquatic environment, generally toxic to plant growth and leading to growth inhibition and biomass reduction. To study the oxidation resistance in Sargassum fusiforme seedlings in response to inorganic Cd stress, we cultured the seedlings under two different Cd levels: natural seawater and high Cd stress. High Cd stress significantly inhibited the seedlings growth, and darkened the thalli color. Additionally, the pigment contents, growth rate, peroxidase (POD) activity, dehydroascorbic acid (DHA) content, and glutathione reductase (GR) activity in S. fusiforme were significantly reduced by high Cd treatment. Contrarily, the Cd accumulation, Cd2+ absorption rate, dark respiration/net photosynthetic rate (Rd/Pn), ascorbic acid (Vc) content, soluble protein (SP) content, glutathione (GSH), and the activities of superoxide dismutase (SOD) and catalase (CAT) of S. fusiforme under Cd treatment significantly increased compared to the control group. The decrease of malondialdehyde (MDA) was not significant. Although S. fusiforme seedlings increased the antioxidant activities of POD, SOD, Vc, and the AsA-GSH cycle to disseminate H2O2 and maintain healthy metabolism, high Cd stress caused Cd accumulation in the stem and leaves of S. fusiforme seedlings. The excessive Cd significantly restricted photosynthesis and reduced photosynthetic pigments in the seedlings, resulting in growth inhibition and deep morphological color, especially of the stems. High levels of Cd in seawater had toxic effects on commercial S. fusiforme seedlings, and risked this edible seaweed for human food.

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.

Similar content being viewed by others

References

  • Aebi H E. 1983. Catalase. In: Bergmeyer U S, ed. Methods of Enzymatic Analysis. 3rd ed. Weinheim: Verlag-Chemie

    Google Scholar 

  • Baumann H A, Morrison L, Stengel D B. 2009. Metal accumulation and toxicity measured by PAM—Chlorophyll fluorescence in seven species of marine macroalgae. Ecotoxicology and Environmental Safety, 72(4): 1063–1075, doi: https://doi.org/10.1016/j.ecoenv.2008.10.010

    Article  Google Scholar 

  • Bradford M M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1–2): 248–254, doi: https://doi.org/10.1016/0003-2697(76)90527-3

    Article  Google Scholar 

  • Collén J, Pinto E, Pedersén M, et al. 2003. Induction of oxidative stress in the red macroalga Gracilaria tenuistipitata by pollutant metals. Archives of Environmental Contamination and Toxicology, 45(3): 337–342

    Article  Google Scholar 

  • Contreras L, Moenne A, Correa J A. 2005. Antioxidant responses in Scytosiphon lomentaria (Phaeophyceae) inhabiting copper-enriched coastal environments. Journal of Phycology, 41(6): 1184–1195, doi: https://doi.org/10.1111/j.1529-8817.2005.00151.x

    Article  Google Scholar 

  • Costa G B, Simioni C, Pereira D T, et al. 2017. The brown seaweed Sargassum cymosum: changes in metabolism and cellular organization after long-term exposure to cadmium. Protoplasma, 254(2): 817–837, doi: https://doi.org/10.1007/s00709-016-0992-9

    Article  Google Scholar 

  • Dos Santos R W, Schmidt É C, Martins R D P, et al. 2012. Effects of cadmium on growth, photosynthetic pigments, photosynthetic performance, biochemical parameters and structure of chloroplasts in the Agarophyte Gracilaria domingensis (Rhodophyta, Gracilariales). American Journal of Plant Sciences, 3(8): 1077–1084, doi: https://doi.org/10.4236/ajps.2012.38129

    Article  Google Scholar 

  • Du Hong, Liang Honghao, Jiang Yang, et al. 2018. Proteome responses of Gracilaria lemaneiformis exposed to lead stress. Marine Pollution Bulletin, 135: 311–317, doi: https://doi.org/10.1016/j.marpolbul.2018.07.030

    Article  Google Scholar 

  • Giannopolitis C N, Ries S K. 1977. Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology, 59(2): 309–314, doi: https://doi.org/10.1104/pp.59.2.309

    Article  Google Scholar 

  • Guo Jiajia, Qin Shiyu, Rengel Z, et al. 2019. Cadmium stress increases antioxidant enzyme activities and decreases endogenous hormone concentrations more in Cd-tolerant than Cd-sensitive wheat varieties. Ecotoxicology and Environmental Safety, 172: 380–387, doi: https://doi.org/10.1016/j.ecoenv.2019.01.069

    Article  Google Scholar 

  • Hall J L. 2002. Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany, 53(366): 1–11

    Article  Google Scholar 

  • He Shanying, Yang Xiaoe, He Zhenli, et al. 2017. Morphological and physiological responses of plants to cadmium toxicity: a review. Pedosphere, 27(3): 421–438, doi: https://doi.org/10.1016/S1002-0160(17)60339-4

    Article  Google Scholar 

  • Heath R L, Packer L. 1968. Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 125(1): 189–198, doi: https://doi.org/10.1016/0003-9861(68)90654-1

    Article  Google Scholar 

  • Hernández-Candelario I D C, Lares M L, Camacho-Ibar V F, et al. 2019. Dissolved cadmium and its relation to phosphate in the deep region of the Gulf of Mexico. Journal of Marine Systems, 193: 27–45, doi: https://doi.org/10.1016/j.jmarsys.2019.01.005

    Article  Google Scholar 

  • Kacperska A. 2004. Sensor types in signal transduction pathways in plant cells responding to abiotic stressors: do they depend on stress intensity?. Physiologia Plantarum, 122(2): 159–168, doi: https://doi.org/10.1111/j.0031-9317.2004.00388.x

    Article  Google Scholar 

  • Khatun S, Ali M B, Hahn E J, et al. 2008. Copper toxicity in Withania somnifera: Growth and antioxidant enzymes responses of in vitro grown plants. Environmental and Experimental Botany, 64(3): 279–285, doi: https://doi.org/10.1016/j.envexpbot.2008.02.004

    Article  Google Scholar 

  • Kieffer P, Schröder P, Dommes J, et al. 2009. Proteomic and enzymatic response of poplar to cadmium stress. Journal of Proteomics, 72(3): 379–396, doi: https://doi.org/10.1016/j.jprot.2009.01.014

    Article  Google Scholar 

  • Kováčik J, Klejdus B, Štork F, et al. 2011. Comparison of methyl jasmonate and cadmium effect on selected physiological parameters in scenedesmus quadricauda (chlorophyta, chlorophyceae). Journal of Phycology, 47(5): 1044–1049, doi: https://doi.org/10.1111/j.1529-8817.2011.01027.x

    Article  Google Scholar 

  • Küpper H, Küpper F, Spiller M. 1998. In situ detection of heavy metal substituted chlorophylls in water plants. Photosynthesis Research, 58(2): 123–133, doi: https://doi.org/10.1023/A:1006132608181

    Article  Google Scholar 

  • Küpper H, Parameswaran A, Leitenmaier B, et al. 2007. Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccu-mulator Thlaspi caerulescens. New Phytologist, 175(4): 655–674, doi: https://doi.org/10.1111/j.1469-8137.2007.02139.x

    Article  Google Scholar 

  • Lee J G, Morel F M M. 1995. Replacement of zinc by cadmium in marine phytoplankton. Marine Ecology Progress Series, 127: 305–309, doi: https://doi.org/10.3354/meps127305

    Article  Google Scholar 

  • Li Ziwei, Yang Ye, Cui Xiuming, et al. 2015. Physiological response and bioaccumulation of Panax notoginseng to cadmium under hydroponic. China Journal of Chinese Materia Medica (in Chinese), 40(15): 2903–2908

    Google Scholar 

  • Lü Fang, Ding Gang, Liu Wei, et al. 2018. Comparative study of responses in the brown algae Sargassum thunbergii to zinc and cadmium stress. Journal of Oceanology and Limnology, 36(3): 933–941, doi: https://doi.org/10.1007/s00343-018-6334-3

    Article  Google Scholar 

  • Moreno-Jiménez E, Fernández J M, Puschenreiter M, et al. 2016. Availability and transfer to grain of As, Cd, Cu, Ni, Pb and Zn in a barley agri-system: Impact of biochar, organic and mineral fertilizers. Agriculture, Ecosystems & Environment, 219: 171–178

    Article  Google Scholar 

  • Panda S K, Choudhury S. 2005. Chromium stress in plants. Brazilian Journal of Plant Physiology, 17(1): 95–102, doi: https://doi.org/10.1590/S1677-04202005000100008

    Article  Google Scholar 

  • Parsons T R, Strickland J D H. 1963. Discussion of spectrophotometric determination of marine plant pigments, with revised equations for ascertaining chlorophylls and carotenoids. Journal of Marine Research, 21(3): 155–163

    Google Scholar 

  • Patrón-Prado M, Casas-Valdez M, Serviere-Zaragoza E, et al. 2011. Biosorption capacity for cadmium of brown seaweed Sargassum sinicola and Sargassum lapazeanum in the gulf of California. Water, Air, & Soil Pollution, 221(1–4): 137–144

    Article  Google Scholar 

  • Porra R J. 2002. The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynthesis Research, 73(1–3): 149–156

    Article  Google Scholar 

  • Ramus J. 1992. Productivity of seaweeds. In: Falkowski P G, Wood-head A D, eds. Primary Productivity and Biogeochemical Cycles in the Sea. New York: Plenum Press

    Google Scholar 

  • Rihab B A, Sabrine B O, Lina C, et al. 2017. Cadmium effect on physiological responses of the tolerant chlorophyta specie picocystis sp. isolated from tunisian wastewaters. Environmental Science and Pollution Research, 24(2): 1803–1810, doi: https://doi.org/10.1007/s11356-016-7950-0

    Article  Google Scholar 

  • Rizwan M, Ali S, Abbas T, et al. 2016. Cadmium minimization in wheat: a critical review. Ecotoxicology and Environmental Safety, 130: 43–53, doi: https://doi.org/10.1016/j.ecoenv.2016.04.001

    Article  Google Scholar 

  • Ruangsomboon S, Wongrat L. 2006. Bioaccumulation of cadmium in an experimental aquatic food chain involving phytoplankton (Chlorella vulgaris), zooplankton (Moina macrocopa), and the predatory catfish Clarias macrocephalus×C. gariepinus. Aquatic Toxicology, 78(1): 15–20, doi: https://doi.org/10.1016/j.aquatox.2006.01.015

    Article  Google Scholar 

  • Shao Guosheng, Muhammad J H, Zhang Xiufu, et al. 2004. Effects of cadmium stress on plant growth and antioxidative enzyme system in different rice genotypes. Chinese Journal of Rice Science (in Chinese), 8(3): 239–244

    Google Scholar 

  • Simioni C, Schmidt É C, Rover T, et al. 2015. Effects of cadmium metal on young gametophytes of Gelidium floridanum: metabolic and morphological changes. Protoplasma, 252(5): 1347–1359, doi: https://doi.org/10.1007/s00709-015-0768-7

    Article  Google Scholar 

  • Souza O P, Ferreira R L, Pires N R X, et al. 2012. Algae of economic importance that accumulate cadmium and lead: a review. Revista Brasileira de Farmacognosia, 22(4): 825–837, doi: https://doi.org/10.1590/S0102-695X2012005000076

    Article  Google Scholar 

  • Stobart A K, Griffiths W T, Ameen-Bukhari I, et al. 1985. The effect of Cd2+ on the biosynthesis of chlorophyll in leaves of barley. Physiologia Plantarum, 63(3): 293–298, doi: https://doi.org/10.1111/j.1399-3054.1985.tb04268.x

    Article  Google Scholar 

  • Sun Yongdi, Chao Jianguo, Gu Wei, et al. 2018. Effect of cadmium stress on physiological and biochemical characteristics of Atractylodes lancea. Plant Physiology Journal (in Chinese), 54(12): 1857–1864

    Google Scholar 

  • Tian Jiyuan, Yu Juan. 2009. Changes in ultrastructure and responses of antioxidant systems of algae (Dunaliella salina) during acclimation to enhanced ultraviolet-B radiation. Journal of Photochemistry and Photobiology B: Biology, 97(3): 152–160, doi: https://doi.org/10.1016/j.jphotobiol.2009.09.003

    Article  Google Scholar 

  • Wang Shuzhi, Zhang Daoyong, Pan Xiangliang. 2013. Effects of cadmium on the activities of photosystems of Chlorella pyrenoidosa and the protective role of cyclic electron flow. Chemosphere, 93(2): 230–237, doi: https://doi.org/10.1016/j.chemosphere.2013.04.070

    Article  Google Scholar 

  • Wójcik M, Tukiendorf A. 2011. Glutathione in adaptation of Arabidopsis thaliana to cadmium stress. Biologia Plantarum, 55(1): 125–132, doi: https://doi.org/10.1007/s10535-011-0017-7

    Article  Google Scholar 

  • Wójcik M, Vangronsveld J, D’Haen J, et al. 2005. Cadmium tolerance in Thlaspi caerulescens: II. Localization of cadmium in Thlaspi caerulescens. Environmental and Experimental Botany, 53(2): 163–171

    Google Scholar 

  • Xia J R, Li Y J, Lu J, et al. 2004. Effects of copper and cadmium on growth, photosynthesis, and pigment content in Gracilaria lemaneiformis. Bulletin of Environmental Contamination and Toxicology, 73(6): 979–986, doi: https://doi.org/10.1007/s00128-004-0522-x

    Article  Google Scholar 

  • Xiao Qingtie, Wang Jingyuan, Zheng Xinyu, et al. 2015. Analysis of the differently expressed proteins in rice roots in response to cadmium stress. Acta Ecologica Sinica (in Chinese), 35(24): 8276–8283

    Google Scholar 

  • Xie Yang, Ye Shan, Wang Yan, et al. 2015. Transcriptome-based gene profiling provides novel insights into the characteristics of radish root response to Cr stress with next-generation sequencing. Frontiers in Plant Science, 6: 202

    Google Scholar 

  • Xu Yan, Tang Degui, Shaked Y, et al. 2007. Zinc, cadmium, and cobalt interreplacement and relative use efficiencies in the coccolithophore Emiliania huxleyi. Limnology and Oceanography, 52(5): 2294–2305, doi: https://doi.org/10.4319/lo.2007.52.5.2294

    Article  Google Scholar 

  • Yu Jiang, Yang Yufeng, Nie Xiangping. 2007. Response of seaweed Gracilaria Lemaneiformis to Cadmium stress. Journal of Sichuan University (Engineering Science Edition) (in Chinese), 39(3): 83–90

    Google Scholar 

  • Zhang Aiqin, Xu Tao, Zou Huixi, et al. 2015. Comparative proteomic analysis provides insight into cadmium stress responses in brown algae Sargassum fusiforme. Aquatic Toxicology, 163: 1–15, doi: https://doi.org/10.1016/j.aquatox.2015.03.018

    Article  Google Scholar 

  • Zhao Tianhong, Sun Jiawei, Fu Yu. 2008. Advances of research on metabolism of plant reactive oxygen species and exogenous regulation under abiotic stresses. Crops (in Chinese), (3): 10–13

  • Zhu Xifeng, Zou Dinghui, Du Hong. 2011. Physiological responses of Hizikia fusiformis to copper and cadmium exposure. Botanica Marina, 54(5): 431–439

    Article  Google Scholar 

  • Zou Dinghui. 2005. Effects of elevated atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in the economic brown seaweed, Hizikia fusiforme (Sargassaceae, Phaeophyta). Aquaculture, 250(3–4): 726–735

    Article  Google Scholar 

Download references

Acknowledgements

We appreciate all staffs for their helpful assistance during this research.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Binbin Chen or Zengling Ma.

Additional information

Foundation item

The National Key R&D Program of China under contract No. 2018YFD0901500; the National Natural Science Foundation of China under contract Nos 41706147 and 41876124.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, T., Hong, M., Wu, M. et al. Oxidative stress responses to cadmium in the seedlings of a commercial seaweed Sargassum fusiforme. Acta Oceanol. Sin. 39, 147–154 (2020). https://doi.org/10.1007/s13131-020-1630-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13131-020-1630-0

Key words

Navigation