Skip to main content
SpringerLink
Log in

Toxicity evaluation of iron oxide nanoparticles and accumulation by microalgae Coelastrella terrestris

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

Abstract

Uses of iron oxide nanoparticles have increased in the last decade. The increased application marked a concern regarding their fate and behavior in the environment. Especially towards the aquatic ecosystems, as the ultimate descend of these iron oxide nanoparticles are aquatic bodies. The greater surface area per mass compared with larger-sized materials of the same chemistry renders these nanoparticles biologically more active. Therefore, it is imperative to assess their eco-toxicogical impact on aquatic eco-systems. In the present study, comparative assessment of iron oxide nanoparticles and their bulk counterpart have been monitored using Coelastrella terrestris up to 40 days. Interestingly, study reveals the potential of Coelastrella terrestris as tool for the bioremediation of iron nanoparticles to combat nano-pollution. Adsorption/absorption kinetics measured after 25 days of treatments with iron oxide nanoparticle and its bulk counterpart revealed higher absorption levels in comparison to the adsorption with maximum accumulation factor (AF) of 2.984 at 50 mg L−1 in nano-form. Iron oxide absorption was found linearly related with concentration in both cases (y = 11.313x-12.165, R2 = 0.8691 in nano; y = 6.35x-5.74, R2 = 0.8128 in bulk). However, 50-mg L−1 nanoparticle concentration was perceived sub-lethal for the algae with 33.33% algal growth reduction under nano and 27.77% under bulk counterpart. Other biochemical parameters, i.e., SOD, CAT, MDA, and lipid quantification, were also quantified to correlate the state of metabolism of treated algal cells in comparison to the control and these exhibited reduction in algal growth due to oxidative stress. Morphological changes were monitored through SEM and TEM.

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

Similar content being viewed by others

Abbreviations

AAS:

Atomic absorption spectrophotometer

ANOVA:

Analysis of variance

BG-11:

Blue Green-11

BOD:

Biochemical oxygen demand

BSA:

Bovine serum albumin

CAT:

Catalase

CDH:

Central drug house

EDTA:

Ethylene diamine tetra acetic acid

FTIR:

Fourier-transform infrared spectroscopy

HClO4 :

Perchloric acid

HNO3 :

Nitric acid

IC50 :

Half maximal inhibitory concentration

MDA:

Malondialdehyde assay

NCBI:

National Center for Biotechnology Information

NP:

Nanoparticle

SD:

Standard deviation

SEM:

Scanning electron microscopy

SOD:

Superoxide dismutase

TEM:

Transmission electron microscopy

UV:

Ultraviolet

References

  • Abdal Dayem A, Hossain MK, Lee SB, Kim K, Saha SK, Yang GM, Cho SG (2017) The role of reactive oxygen species (ROS) in the biological activities of metallic nanoparticles. Int J Mol Sci 18:120

    Google Scholar 

  • Badruddoza AZM, Tay ASH, Tan PY, Hidajat K, Uddin MS (2011) Carboxymethyl-β-cyclodextrin conjugated magnetic nanoparticles as nano-adsorbents for removal of copper ions: synthesis and adsorption studies. J Hazard Mater 185:1177–1186

    CAS  Google Scholar 

  • Barhoumi L, Dewez D (2013) Toxicity of superparamagnetic iron oxide nanoparticles on green alga. Chlorella vulgaris. Biomed Res Int:2013

  • Bour A, Mouchet F, Silvestre J, Gauthier L, Pinelli E (2015) Environmentally relevant approaches to assess nanoparticles ecotoxicity: a review. J Hazard Mater 283:764–777

    CAS  Google Scholar 

  • Cattaneo AG (2018) Nanotoxicological evaluation in marine water ecosystem: a detailed review. In: Environmental Toxicity of Nanomaterials. CRC Press, Boca Raton, pp 61–90

    Google Scholar 

  • Chen Z, Yin JJ, Zhou YT, Zhang Y, Song L, Song M, Hu S, Gu N (2012) Dual enzyme-like activities of iron oxide nanoparticles and their implication for diminishing cytotoxicity. ACS Nano 6:4001–4012

    CAS  Google Scholar 

  • Chen PJ, Wu WL, Wu KCW (2013) The zerovalent iron nanoparticle causes higher developmental toxicity than its oxidation products in early life stages of medaka fish. Water Res 47:3899e3909

    Google Scholar 

  • Chen F, Xiao Z, Yue L, Wang J, Feng Y, Zhu X, Wang Z, Xing B (2019) Algae response to engineered nanoparticles: current understanding, mechanisms and implications. Environ Sci Nano 6:1026–1042

    CAS  Google Scholar 

  • Dhawan A, Sharma V (2010) Toxicity assessment of nanomaterials: methods and challenges. Anal Bioanal Chem 398:589–605

    CAS  Google Scholar 

  • Djearamane S, Lim YM, Wong LS, Lee PF (2018) Cytotoxic effects of zinc oxide nanoparticles on cyanobacterium Spirulina (Arthrospira) platensis. PeerJ 6:e4682

    Google Scholar 

  • Du S, Zhang P, Zhang R, Lu Q, Liu L, Bao X, Liu H (2016) Reduced graphene oxide induces cytotoxicity and inhibits photosynthetic performance of the green alga Scenedesmus obliquus. Chemosphere 164:499–507

    CAS  Google Scholar 

  • Espinasse BP, Geitner NK, Schierz A, Therezien M, Richardson CJ, Lowry GV, Ferguson L, Wiesner MR (2018) Comparative persistence of engineered nanoparticles in a complex aquatic ecosystem. Environ Sci Technol 52:4072–4078

    CAS  Google Scholar 

  • Fawley MW, Fawley KP (2004) A simple and rapid technique for the isolation of DNA from microalgae 1. J Phycol 40:223–225

    CAS  Google Scholar 

  • Gong N, Shao K, Feng W, Lin Z, Liang C, Sun Y (2011) Biotoxicity of nickel oxide nanoparticles and bio-remediation by microalgae Chlorella vulgaris. Chemosphere 83:510–516

    CAS  Google Scholar 

  • Grillo R, Rosa AH, Fraceto LF (2015) Engineered nanoparticles and organic matter: a review of the state-of-the-art. Chemosphere 119:608–619

    CAS  Google Scholar 

  • Gupta VK, Nayak A (2012) Cadmium removal and recovery from aqueous solutions by novel adsorbents prepared from orange peel and Fe2O3 nanoparticles. Chem Eng J 180:81–90

    CAS  Google Scholar 

  • Harish, Sundaramoorthy S, Kumar D, Vaijapurkar SG (2008) A new chlorophycean nickel hyperaccumulator. Bioresour Technol 99:3930–3934

    CAS  Google Scholar 

  • Harish, Gupta AK, Phulwaria M, Rai MK, Shekhawat NS (2014) Conservation genetics of endangered medicinal plant Commiphora wightii in Indian Thar Desert. Gene 535:266–272

    CAS  Google Scholar 

  • Hazeem LJ, Waheed FA, Rashdan S, Bououdina M, Brunet L, Slomianny C, Boukherroub R, Elmeselmani WA (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

    CAS  Google Scholar 

  • Herbert D, Phipps PJ, Strange RE (1971) The chemical analysis of microbial cell. In: Norris JR, Ribbons DW (eds) Methods in microbiology, Volume VB. London Academic Press, London, pp 209–344

    Google Scholar 

  • Hua M, Zhang S, Pan B, Zhang W, Lv L, Zhang Q (2012) Heavy metal removal from water/wastewater by nanosized metal oxides: a review. J Hazard Mater 211:317–331

    Google Scholar 

  • Hussain I, Singh NB, Singh A, Singh H, Singh SC (2016) Green synthesis of nanoparticles and its potential application. Biotechnol Lett 38:545–560

    CAS  Google Scholar 

  • Joonas E, Aruoja V, Olli K, Kahru A (2019) Environmental safety data on CuO and TiO2 nanoparticles for multiple algal species in natural water: filling the data gaps for risk assessment. Sci Total Environ 647:973–980

    CAS  Google Scholar 

  • Kurutas EB (2015) The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: current state. Nutr J 15:71

    Google Scholar 

  • Leclerc S, Wilkinson KJ (2013) Bioaccumulation of Nanosilver by Chlamydomonas reinhardtii- nanoparticle or the free ion? Environ Sci Technol 48:358–364

    Google Scholar 

  • Lei C, Zhang L, Yang K, Zhu L, Lin D (2016) Toxicity of iron-based nanoparticles to green algae: effects of particle size, crystal phase, oxidation state and environmental aging. Environ Pollut 218:505–512

    CAS  Google Scholar 

  • Lei C, Sun Y, Tsang DC, Lin D (2018) Environmental transformations and ecological effects of iron-based nanoparticles. Environ Pollut 232:10–30

    CAS  Google Scholar 

  • Li HC, Zhou QF, Wu Y, Fu JJ, Wang T, Jiang GB (2009) Effects of waterborne nano-iron on medaka (Oryzias latipes): antioxidant enzymatic activity, lipid peroxidation and histopathology. Ecotoxicol Environ Saf 72:684e692

    Google Scholar 

  • Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with folin reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Mackinney G (1941) Absorption of light by chlorophyll solution. J Biol Chem 140:315–322

    CAS  Google Scholar 

  • Manzo S, Miglietta ML, Rametta G, Buono S, Di Francia G (2013) Toxic effects of ZnO nanoparticles towards marine algae Dunaliella tertiolecta. Sci Total Environ 445:371–376

    Google Scholar 

  • Markou G, Nerantzis E (2013) Microalgae for high-value compounds and biofuels production: a review with focus on cultivation under stress conditions. Biotechnol Adv 31:1532–1542

    CAS  Google Scholar 

  • Metzler DM, Li M, Erdem A, Huang CP (2011) Responses of algae to photocatalytic nano-TiO2 particles with an emphasis on the effect of particle size. Chem Eng J 170:538–546

    CAS  Google Scholar 

  • Miao AJ, Schwehr KA, Xu C, Zhang SJ, Luo Z, Quigg A, Santschi PH (2009) The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances. Environ Pollut 157:3034–3041

    CAS  Google Scholar 

  • Mishra SK, Suh WI, Farooq W, Moon M, Shrivastav A, Park MS, Yang JW (2014) Rapid quantification of microalgal lipids in aqueous medium by a simple colorimetric method. Bioresour Technol 155:330–333

    CAS  Google Scholar 

  • Moore MN (2006) Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environ Int 32:967–976

    CAS  Google Scholar 

  • Murthy KC, Vanitha A, Rajesha J, Swamy MM, Sowmya PR, Ravishankar GA (2005) In vivo antioxidant activity of carotenoids from Dunaliella salina—a green microalga. Life Sci 76:1381–1390

    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

    CAS  Google Scholar 

  • Nguyen NH, Von Moos NR, Slaveykova VI, Mackenzie K, Meckenstock RU, Thűmmler S, Bosch J, Ševců A (2018) Biological effects of four iron-containing nanoremediation materials on the green alga Chlamydomonas sp. Ecotoxicol Environ Saf 154:36–44

    CAS  Google Scholar 

  • Oukarroum A, Bras S, Perreault F, Popovic R (2012) Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicol Environ Saf 78:80–85

    CAS  Google Scholar 

  • Pereira FF, Paris EC, Bresolin JD, Foschini MM, Ferreira MD, Corrêa DS (2017) Investigation of nanotoxicological effects of nanostructured hydroxyapatite to microalgae Pseudokirchneriella subcapitata. Ecotoxicol Environ Saf 144:138–147

    CAS  Google Scholar 

  • Phenrat T, Long TC, Lowry GV, Veronesi B (2008) Partial oxidation (“aging”) and surface modification decrease the toxicity of nanosized zerovalent iron. Environ Sci Technol 43:195–200

    Google Scholar 

  • Rippka R, Derelies J, Waterbury JB, Herdman M, Stainer RV (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Roy R, Parashar A, Bhuvaneshwari M, Chandrasekaran N, Mukherjee A (2016) Differential effects of P25 TiO2 nanoparticles on freshwater green microalgae: Chlorella and Scenedesmus species. Aquat Toxicol 176:161–171

    CAS  Google Scholar 

  • Rui M, Ma C, Hao Y, Guo J, Rui Y, Tang X, Zhao Q, Fan X, Zhang Z, Hou T, Zhu S (2016) Iron oxide nanoparticles as a potential iron fertilizer for peanut (Arachis hypogaea). Front Plant Sci 7:815

    Google Scholar 

  • Rui M, Ma C, White JC, Hao Y, Wang Y, Tang X, Yang J, Jiang F, Ali A, Rui Y, Cao W (2018) Metal oxide nanoparticles alter peanut (Arachis hypogaea L.) physiological response and reduce nutritional quality: a life cycle study. Environ Sci Nano 5(9):2088–2102

    CAS  Google Scholar 

  • Sadiq IM, Pakrashi S, Chandrasekaran N, Mukherjee A (2011) Studies on toxicity of aluminum oxide (Al2O3) nanoparticles to microalgae species: Scenedesmus sp. and Chlorella sp. J Nanopart Res 13:3287–3299

    CAS  Google Scholar 

  • Saison C, Perreault F, Daigle JC, Fortin C, Claverie J, Morin M, Popovic R (2010) Effect of core–shell copper oxide nanoparticles on cell culture morphology and photosynthesis (photosystem II energy distribution) in the green alga, Chlamydomonas reinhardtii. Aquat Toxicol 96:109–114

    CAS  Google Scholar 

  • Salas P, Odzak N, Echegoyen Y, Kägi R, Sancho MC, Navarro E (2019) The role of size and protein shells in the toxicity to algal photosynthesis induced by ionic silver delivered from silver nanoparticles. Sci Total Environ 692:233–239

    CAS  Google Scholar 

  • Santhosh C, Velmurugan V, Jacob G, Jeong SK, Grace AN, Bhatnagar A (2016) Role of nanomaterials in water treatment applications: a review. Chem Eng J 306:1116–1137

    CAS  Google Scholar 

  • Saxena P, Harish (2018) Nanoecotoxicological reports of engineered metal oxide nanoparticles on algae. Curr Pollut Rep:1–15

  • Sharma YC, Srivastava V, Singh VK, Kaul SN, Weng CH (2009) Nano-adsorbents for the removal of metallic pollutants from water and wastewater. Environ Technol 30:583–609

    CAS  Google Scholar 

  • Siddiqi KS, Rahman A, Husen A (2016) Biogenic fabrication of iron/iron oxide nanoparticles and their application. Nanoscale Res Lett 11:498

    Google Scholar 

  • Simonsen G, Strand M, Øye G (2018) Potential applications of magnetic nanoparticles within separation in the petroleum industry. J Pet Sci Eng 165:488–495

    CAS  Google Scholar 

  • Sridharan K, Kuriakose T, Philip R, Park TJ (2014) Transition metal (Fe, Co and Ni) oxide nanoparticles grafted graphitic carbon nitrides as efficient optical limiters and recyclable photocatalysts. Appl Surf Sci 308:139–147

    CAS  Google Scholar 

  • Stone V, Nowack B, Baun A, van den Brink N, von der Kammer F, Dusinska MM, Handy R, Hankin S, Hassellöv M, Joner E, Fernandes TF (2010) Nanomaterials for environmental studies: classification, reference material issues, and strategies for physico-chemical characterisation. Sci Total Environ 408:1745–1754

    CAS  Google Scholar 

  • Suman TY, Rajasree SR, Kirubagaran R (2015) Evaluation of zinc oxide nanoparticles toxicity on marine algae Chlorella vulgaris through flow cytometric, cytotoxicity and oxidative stress analysis. Ecotoxicol Environ Saf 113:23–30

    CAS  Google Scholar 

  • Tripathi DK, Tripathi A, Shweta SS, Singh Y, Vishwakarma K, Yadav G, Sharma S, Singh VK, Mishra RK, Upadhyay RG, Dubey NK, Lee Y, Chauhan DK (2017) Uptake, accumulation and toxicity of silver nanoparticle in autotrophic plants, and heterotrophic microbes: a concentric review. Front Microbiol 8:7

    Google Scholar 

  • Turhani D, Cvikl B, Watzinger E, Weißenböck M, Yerit K, Thurnher D et al (2005) In vitro growth and differentiation of osteoblast-like cells on hydroxyapatite ceramic granule calcified from red algae. J Oral Maxillofac Surg 63(6):793–799

    Google Scholar 

  • Van Koetsem F, Verstraete S, Wallaert E, Verbeken K, Van der Meeren P, Rinklebe J, Du Laing G (2017) Use of filtration techniques to study environmental fate of engineered metallic nanoparticles: factors affecting filter performance. J Hazard Mater 322:105–117

    Google Scholar 

  • Van Nhan L, Ma C, Rui Y, Cao W, Deng Y, Liu L, Xing B (2016) The effects of Fe2O3 nanoparticles on physiology and insecticide activity in non-transgenic and Bt-transgenic cotton. Front Plant Sci 6:1263

    Google Scholar 

  • Vance ME, Kuiken T, Vejerano EP, McGinnis SP, Hochella MF Jr, Rejeski D, Hull MS (2015) Nanotechnology in the real world: redeveloping the nanomaterial consumer products inventory. Beilstein J Nanotechnol 6:1769–1780

    CAS  Google Scholar 

  • von Moons N, Slaveykova VI (2014) Oxidative stress induced by inorganic nanoparticles in bacteria and aquatic microalgaeestate of the art and knowledge gaps. Nanotoxicology 8:605e630

    Google Scholar 

  • Wang G, Hao Z, Huang Z, Chen L, Li X, Hu C, Liu Y (2010) Raman spectroscopic analysis of a desert cyanobacterium Nostoc sp. in response to UVB radiation. Astrobiology 10:783–788

    CAS  Google Scholar 

  • Wang L, Min Y, Xu D, Yu F, Zhou W, Cuschieri A (2014) Membrane lipid peroxidation by the peroxidase-like activity of magnetite nanoparticles. Chem Commun 50:11147–11150

    CAS  Google Scholar 

  • Wang Y, Jiang F, Ma C, Rui Y, Tsang DC, Xing B (2019) Effect of metal oxide nanoparticles on amino acids in wheat grains (Triticum aestivum) in a life cycle study. J Environ Manag 241:319–327

    Google Scholar 

  • Woodrow Wilson International Center for Scholars (2010) Nanotechnology Consumer Products Inventory. http://www.nanotechproject.org/inventories/consumer

  • Wu HH, Yin JJ, Wamer WG, Zeng MY, Lo YM (2014) Reactive oxygen speciesrelated activities of nano-iron metal and nano-iron oxides. J Food Drug Anal 22:86e94

    Google Scholar 

  • Wu H, Jiang H, Liu C, Deng Y (2015) Growth, pigment composition, chlorophyll fluorescence and antioxidant defenses in the red alga Gracilaria lemaneiformis (Gracilariales, Rhodophyta) under light stress. S Afr J Bot 100:27–32

    CAS  Google Scholar 

  • Xu P, Zeng GM, Huang DL, Feng CL, Hu S, Zhao MH, Lai C, Wei Z, Huang C, Xie GX, Liu ZF (2012) Use of iron oxide nanomaterials in wastewater treatment: a review. Sci Total Environ 424:1–10

    CAS  Google Scholar 

  • Yang H, Liu C, Yang D, Zhang H, Xi Z (2009) Comparative study of cytotoxicity, oxidative stress and genotoxicity induced by four typical nanomaterials: the role of particle size, shape and composition. J Appl Toxicol 29:69–78

    Google Scholar 

  • Yilancioglu K, Cokol M, Pastirmaci I, Erman B, Cetiner S (2014) Oxidative stress is a mediator for increased lipid accumulation in a newly isolated Dunaliella salina strain. PLoS One 9:e91957

    Google Scholar 

  • Yoon SY, Lee CG, Park JA, Kim JH, Kim SB, Lee SH, Choi JW (2014) Kinetic, equilibrium and thermodynamic studies for phosphate adsorption to magnetic iron oxide nanoparticles. Chem Eng J 236:341–347

    CAS  Google Scholar 

  • Yunus IS, Harwin, Kurniawan A, Adityawarman D, Indarto A (2012) Nanotechnologies in water and air pollution treatment. Environ Technol 1:136–148

    CAS  Google Scholar 

  • Zhang L, Liao C, Yang Y, Wang YZ, Ding K, Huo D, Hou C (2019) Response of lipid biosynthesis in Chlorella pyrenoidosa to intracellular reactive oxygen species level under stress conditions. Bioresour Technol 287:121414

    CAS  Google Scholar 

  • Zhao J, Cao X, Liu X, Wang Z, Zhang C, White JC, Xing B (2016) Interactions of CuO nanoparticles with the algae Chlorella pyrenoidosa: adhesion, uptake, and toxicity. Nanotoxicology 10:1297–1305

    CAS  Google Scholar 

  • Zhong LS, Hu JS, Liang HP, Cao AM, Song WG, Wan LJ (2006) Self-assembled 3D flowerlike iron oxide nanostructures and their application in water treatment. Adv Mater 18:2426–2431

    CAS  Google Scholar 

  • Zion Market Research (2016) Nanomaterials market (metal oxide, metals, chemicals & polymers and others) for construction, chemical products, packaging, consumer goods, electrical and electronics, energy, healthcare, transportation and other applications: Global market perspective, comprehensive analysis and forecast, 2022.2017

Download references

Acknowledgments

We are thankful to the editors and anonymous reviewers for the critical reading of the manuscript and improvement. We wish to acknowledge SAIF, New Delhi for Electron Microscopy Facility.

Funding

Contribution of Pallavi Saxena and Vishambhar Sangela to this study was financially supported by University Grants Commission (UGC), New Delhi, India, in the form of BSR meritorious fellowship [F.25-a/2013-14(BSR)/7-125/2007(BSR)] and [F.25-a/2014-15(BSR)/7-125/2007(BSR)].

Author information

Authors and Affiliations

  1. Plant Biotechnology Laboratory, Department of Botany, Mohanlal Sukhadia University, Udaipur, Rajasthan, 313001, India

    Pallavi Saxena, Vishambhar Sangela &  Harish

Authors
  1. Pallavi Saxena
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vishambhar Sangela
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Harish
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Harish.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Gangrong Shi

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saxena, P., Sangela, V. & Harish Toxicity evaluation of iron oxide nanoparticles and accumulation by microalgae Coelastrella terrestris. Environ Sci Pollut Res 27, 19650–19660 (2020). https://doi.org/10.1007/s11356-020-08441-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-08441-9

Keywords

Search

Navigation