Skip to main content

Advertisement

SpringerLink
Log in

Toxicity effect of graphene oxide on growth and photosynthetic pigment of the marine alga Picochlorum sp. during different growth stages

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Graphene oxide (GO), a recently discovered material, has been investigated for many applications in various fields. Thus, an immense awareness should be paid on the potential effects of the material on the environment as huge quantities of GO may get to the environment. Aquatic organisms, marine algae as an example, are exposed to such material when disposed to the environment. Accordingly, it is significant to assess the probable interactions of GO with algae in evaluating its possible environmental risks. In this study, we have examined the effect of different concentrations of GO on Picochlorum sp. during the different growth phases. The results showed that the toxicity of GO increases with increasing its concentration. The lowest concentration (0.5 mg L−1) was found to improve the algae growth and pigment content of Picochlorum sp. In contrast, higher GO concentrations had a negative consequence on the growth of algae and photosynthetic pigment concentration.

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

  • Agawin NSR, Duarte CM, Agusti S (2000) Nutrient and temperature control of the contribution of picoplankton to phytoplankton biomass and production. Limnol Oceanogr 45:591–600

    Article  CAS  Google Scholar 

  • Arouja V, Dubourguier HC, Kasemets K, Kahru A (2009) Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Raphidocelis subcapitata. Sci Total Environ 407:1461–1468

    Article  Google Scholar 

  • Arvidsson R, Molander S, Sanden BA (2013) Review of potential environmental and health risks of the nanomaterial graphene. Hum Ecol Risk Assess 19:873–887

    CAS  Google Scholar 

  • Azevedo J, Campidelli S, He D, Cornut R, Bertucchi M, Sorgues S, Benattar J, Colbeau-Justin C, Derycke V (2015) Versatile wafer-scale technique for the formation of ultrasmooth and thickness-controlled graphene oxide films based on very large flakes. ACS Appl Mater Interfaces 7(38):21270–21277

    Article  CAS  Google Scholar 

  • Basiuk VA, Bassiouk M (2008) Nanoassembly of meso-tetraphenylporphines on surfaces of carbon materials: initial steps as studied by molecular mechanics and scanning tunning microscopy. J Nanotechnol 8(1):259–267

    CAS  Google Scholar 

  • Brody AL (2006) Nano and food packaging technologies converge. Food Technol 60(3):92–94

    Google Scholar 

  • Callieri C (2008) Picophytoplankton in freshwater ecosystems: the importance of small-sized phototrophs. Freshwater Rev 1:1–28

    Article  Google Scholar 

  • Chen R, Ratnikova TA, Stone MB, Lin S, Lard M, Huang G, Hudson JS, Ke PC (2010) Differential uptake of carbon nanoparticles by plant and mammalian cells. Small 6:612–617

    Article  CAS  Google Scholar 

  • Combarros RG, Collado S, Diaz M (2016) Toxicity of grpahen oxide on grwoth and metabolism of Pseudomonas putida. J Hazard Mater 310: 246–252

  • Deng XJ, Lu LL, Li HW, Luo F (2010) The adsorption properties of Pb(II) and Cd(II) on functionalized graphene prepared by electrolysis method. J Hazard Mater 183:923–930

    Article  CAS  Google Scholar 

  • Fellahi O, Das MR, Coffinier Y, Szunerits S, Hadjersi T, Maamache M, Boukherroub R (2011) Silicon nanowire arrays-induced graphene oxide reduction under UV irradiation. Nanoscale 3:4662–4669

    Article  CAS  Google Scholar 

  • Graf D, Molitor F, Ensslin K, Stampfer C, Jungen A, Hierold C, Wirtz L (2007) Spatially resolved Raman spectroscopy of single- and few-layer graphene. Nano Lett 7:238–242

    Article  CAS  Google Scholar 

  • Hazeem L, AbdulWaheed F, Rashdan S, Bououdina M, Brunet L, Slomianny C, Boukherroub R, Elmeselmani W (2015) Effect of magnetic iron oxide (Fe3O4) nanoparticles on the growth and photosynthetic pigment content of Picochlorum sp. Environ Sci Pollut Res 22:11728–11739. doi:10.1007/s11356-015-4370-5

    Article  CAS  Google Scholar 

  • Hazeem L, Bououdina M, Rashdan S, Brunet L, Slomianny C, Boukherroub R (2016) Cumulative effect of zinc oxide and titanium oxide nanoparticles on growth and chlorophyll a content of Picochlorum sp. Environ Sci Pollut Res 23:2821–2830. doi:10.1007/s11356-015-5493-4

    Article  CAS  Google Scholar 

  • Hu X, Lu K, Mu L, Kang J, Zhou Q (2014) Interactions between graphene oxide and plant cells: regulation of cell morphology, uptake, organelle damage, oxidative effects and metabolic disorders. Carbon 80:665–676

    Article  CAS  Google Scholar 

  • Hu X, Zhou Q (2013) Health and ecosystem risks of graphene. Chem Rev 113:3815–3835

    Article  CAS  Google Scholar 

  • Hu C, Wang Q, Zhao H, Wang L, Guo S, Li X (2015a) Ecotoxicological effects of graphene oxide on the protozoan Euglena gracilis. Chemosphere 128:184–190

    Article  CAS  Google Scholar 

  • Hu X, Ouyang S, Mu L, An J, Zhou Q (2015b) Effects of graphene oxide and oxidized carbon nanotubes on the cellular division, microstructure, uptake, oxidative stress, and metabolic profiles. Environ Sci Technol 49(18):10825–10833

    Article  CAS  Google Scholar 

  • Kang S, Herzberg M, Rodrigues DF, Elimelech M (2008) Antibacterial effects of carbon nanotubes: size does matter. Langmuir 24(13):2409–6413

    Article  Google Scholar 

  • Long Z, Ji J, Yang K, Lin D, Wu F (2012) Systematic and quantitative investigation of the mechanism of carbon nanotubes’ toxicity toward algae. Environ Sci Technol 46(15):8458–8466. doi:10.1021/es301802g

    Article  CAS  Google Scholar 

  • Li WKW (1994) Primary productivity of prochlorophytes, cyanobacteria, and eukaryotic ultraphytoplankton: measurements from flow cytometric sorting. Limnol Oceanogr 39:169–175

    Article  CAS  Google Scholar 

  • Mohanty N, Fahrenholtz M, Nagaraja A, Boyle D, Berry V (2011) Impermeable graphenic encasement of bacteria. Nano Lett 11:1270–1275

    Article  CAS  Google Scholar 

  • Morlon H, Fortin C, Floriani M, Adam C, Garnier-Laplace J, Boudou AB (2005) Toxicity of selenite in the unicellular green alga Chlamydomonas reinhardtii: comparison between effects at the population and sub-cellular level. Aquat Toxicol 73:65–78

    Article  CAS  Google Scholar 

  • Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao AJ, Quigg A, Santschi PH, Sigg L (2008) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17:372–386

    Article  CAS  Google Scholar 

  • Nel A, Xia T, Madler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311:622–627

    Article  CAS  Google Scholar 

  • Nogueira PFM, Nakabayashi D, Zucolotto V (2015) The effects of graphene oxide on green algae Raphidocelis subcapitata. Aquatic Toxicol 166:29–35

    Article  CAS  Google Scholar 

  • Pavagadhi S, Tang ALL, Sathishkumar M, Loh KP, Balasubramanian R (2013) Removal of microcystin-LR and microcystin-RR by graphene oxide: adsorption and kinetic experiments. Water Res 47(13):4621–4629

    Article  CAS  Google Scholar 

  • Pretti C, Oliva M, Di Pietro R, Monni G, Cevasco G, Chiellini F, Pomelli C, Chiappe C (2014) Ecotoxicity of pristine graphene to marine organisms. Ecotox Environ Safe 101:138–145

    Article  CAS  Google Scholar 

  • Sánchez CV, Jachak A, Hurt RH, Kane AB (2012) Biological interactions of graphene-family nanomaterials: an interdisciplinary review. Chem Res Toxicol 25:15–34

    Article  Google Scholar 

  • Schwab F, Bucheli TD, Lukhele LP (2011) Are carbon nanotube effects on green algae caused by shading and agglomeration? Environ Sci Technol 45:6136–6144

    Article  CAS  Google Scholar 

  • Tang Y, Tian J, Li S, Xue C, Xue Z, Yin D, Yu S (2015) Combined effects of graphene oxide and Cd on the photosynthetic capacity and survival of Microcystis aeruginosa. Sci Total Environ 532:154–161

    Article  CAS  Google Scholar 

  • Van Den Hoek C, Mann DG, Jahn MM (1995) Algae: an introduction to phycology. Cambridge University Press, Cambridge Science 623 pages

    Google Scholar 

  • Vohra FC (1966) Determination of photosynthetic pigment in seawater. Monographs on oceanographic methodology. UNESCO, France

    Google Scholar 

  • Wahid MH, Eroglu E, Chen X, Smith SM, Raston CL (2013) Entrapment of Chlorella vulgaris cells within graphene oxide layers. RSC Adv 3:8180–8183

    Article  CAS  Google Scholar 

  • Wang K, Ruan J, Song H (2011) Biocompatibility of graphene oxide. Nanoscale Res Lett 6:1–8

    Google Scholar 

  • Wang J, Zhang X, Chen Y, Sommerfeld M, Hu Q (2008) Toxicity assessment of manufactured nanomaterials using the unicellular green alga Chlamydomonas reinhardtii. Chemosphere 73:1121–1128

    Article  CAS  Google Scholar 

  • Wei I, Thakkar M, Chen Y, Ntim SA, Mitra S, Zhang X (2010) Cytotoxicity effects of water dispersible oxidized multiwalled carbon nanotubes on marine alga Dunaliella teriolecta. Aquat Toxicol 100:194–201

    Article  CAS  Google Scholar 

  • Zhao J, Wang Z, White JC, Xing B (2014) Graphene in the aquatic environment: adsorption, dispersion, toxicity, and transformation. Environ Sci Technol 48:9995–10009

    Article  CAS  Google Scholar 

  • Zhang K, Dwivedi V, Chi C, Wu J (2010) Graphene oxide/ ferric hydroxide composites for efficient arsenate removal from drinking water. J Hazard Mater 182:162–168

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grant number (11/2012) funded by the Deanship of Scientific Research, University of Bahrain. We would like to extend our appreciation to the reviewers for taking the time and effort to provide insightful comments to improve the quality of the article. This work was partly supported by the french RENATECH network (French national nanofabrication platform).

Author information

Authors and Affiliations

  1. Department of Biology, College of Science, University of Bahrain, P.O. Box 32038, Zallaq, Kingdom of Bahrain

    Layla J. Hazeem

  2. Department of Physics, College of Science, University of Bahrain, P.O. Box 32038, Zallaq, Kingdom of Bahrain

    Mohamed Bououdina

  3. Laboratoire de Physiologie Cellulaire, INSERM U.1003, Université de Lille 1, Rue Paul Langevin, 59655, Villeneuve d’Ascq, France

    Etienne Dewailly & Christian Slomianny

  4. Univ. Lille, CNRS, Centrale Lille, ISEN, Univ. Valenciennes, UMR 8520-IEMN, F-59000, Lille, France

    Alexandre Barras, Yannick Coffinier, Sabine Szunerits & Rabah Boukherroub

Authors
  1. Layla J. Hazeem
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohamed Bououdina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Etienne Dewailly
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christian Slomianny
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alexandre Barras
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yannick Coffinier
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sabine Szunerits
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rabah Boukherroub
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Layla J. Hazeem.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hazeem, L.J., Bououdina, M., Dewailly, E. et al. Toxicity effect of graphene oxide on growth and photosynthetic pigment of the marine alga Picochlorum sp. during different growth stages. Environ Sci Pollut Res 24, 4144–4152 (2017). https://doi.org/10.1007/s11356-016-8174-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-8174-z

Keywords

Search

Navigation