Skip to main content

Advertisement

SpringerLink
Log in

Does the photocatalytic activity of nanoparticles protect the marine mussel Mytilus galloprovincialis from polycyclic aromatic hydrocarbon toxicity?

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

Abstract

In the present study, five NPs (containing ZnO, Au-ZnO, Cu-ZnO, TiO2, and Au-TiO2) were characterized using dynamic light scattering and transmission electron microscopy, in order to observe their behavior under environmental change. The applicability of NPs for degradation of three polycyclic aromatic hydrocarbons (PAHs), including benzo(a)pyrene, fluoranthene, and benzanthracene, using UV irradiation showed the high photocatalytic efficiency of doped NPs for the removal of the study pollutants. To predict the environmental impact and interaction between NPs and PAHs on marine organisms, Mytilus galloprovincialis mussels were exposed to concentrations of each chemical (50 and 100 μg/L) for 14 days. The mussel’s response was determined using the oxidative stress biomarker approach. Measured biomarkers in the mussel’s digestive gland showed possible oxidative mechanisms in a concentration-dependent manner occurring after exposure to PAHs and NPs separately. Overall, this finding provides an interesting combination to remove PAHs in water, and the incorporation of chemical element into the crystallographic structure of NPs and the combination of two different NPs to form a binary hybrid NPs are promising materials.

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
Fig. 7

Similar content being viewed by others

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Aebi H (1974) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press, London, pp 671–684

    Google Scholar 

  • Andersson JT, Achten C (2015) Time to say goodbye to the 16 EPA PAHs? Toward an up-to-date use of PACs for environmental purposes. Polycycl Aromat Compd 35:330–354

    Article  CAS  Google Scholar 

  • Anyakora C, Ogbeche A, Palmer P, Coker H (2005) Determination of polynuclear aromatic hydrocarbons in marine samples of Siokolo Fishing Settlement. J Chromatogr A 1073:323–330

    Article  CAS  Google Scholar 

  • Ayala A, Muñoz MF, Argüelles S (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Med Cell Longev:360–438

  • Babaranti O, Horn S, Jowett T, Frew R (2019) Isotopic signatures in Mytilus galloprovincialis and Ulva lactuca as bioindicators for assessing discharged sewage effluent in coastal waters along Otago Peninsula, New Zealand. Geol Ecol Landsc 3(1):53–64

    Article  Google Scholar 

  • Banni M, Negri A, Dagnino A, Jebali J, Ameur S, Boussetta H (2010) Acute effects of benzo [a] pyrene on digestive gland enzymatic biomarkers and DNA damage on mussel Mytilus galloprovincialis. Ecotoxicol Environ Saf 73(5):842–848

    Article  CAS  Google Scholar 

  • Barata C, Varo I, Navarro JC, Arun S, Porte C (2005) Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds. Comp Biochem Physiol C 140:175–186

    Google Scholar 

  • Bat L (2019) Concentrations of toxic elements in mussels Mytilus galloprovincialis as bio-indicator of coastal pollution. In International Biodiverstiy & Ecology Sciences Symposium. E-book on 22.10. 2019

  • Batley GE, Kirby JK, McLaughlin MJ (2013) Fate and risks of nanomaterials in aquatic and terrestrial environments. Acc Chem Res 46(3):854–862

    Article  CAS  Google Scholar 

  • Behera BK, Das A, Sarkar DJ, Weerathunge P, Parida PK, Das BK, Thavamani P, Ramanathan R, Bansal V (2018) Polycyclic Aromatic Hydrocarbons (PAHs) in inland aquatic ecosystems: Perils and remedies through biosensors and bioremediation. Environ Pollut 241:212–233

    Article  CAS  Google Scholar 

  • Bellas J, Saco-Alvarez L, Nieto O, Beiras R (2008) Ecotoxicological evaluation of polycyclic aromatic hydrocarbons using marine invertebrate embry-elarval bioassays. Mar Pollut Bull 57:493–502

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    Article  CAS  Google Scholar 

  • Caliani I, Porcelloni S, Mori G, Frenzilli G, Ferraro M, Marsili L, Casini S, Fossi MC (2009) Genotoxic effects of produced waters in mosquito fish (Gambusia affinis). Ecotoxicology 18:75–80

    Article  CAS  Google Scholar 

  • Canesi L, Ciacci C, Lorusso LC, Betti M, Gallo G, Pojana G, Marcomini A (2007) Effects of triclosan on Mytilus galloprovincialis hemocyte function and digestive gland enzyme activities: possible modes of action on non target organisms. Comp Biochem Physiol C 145:464–472

    Google Scholar 

  • Canesi L, Fabbri R, Gallo G, Vallotto D, Marcomini A, Pojana GJAT (2010) Biomarkers in Mytilus galloprovincialis exposed to suspensions of selected nanoparticles (Nano carbon black, C60 fullerene, Nano-TiO2, Nano-SiO2). Aquat Toxicol 100:168–177

    Article  CAS  Google Scholar 

  • Canesi L, Frenzilli G, Balbi T, Bernardeschi M, Ciacci C, Corsolini S, Della Torre C, Fabbri R, Faleri C, Focardi S, Guidi P, Kocan A, Marcomini A, Mariottini M, Nigro M, Pozo-Gallardo K, Rocco L, Scarcelli V, Smerilli A, Corsi I (2014) Interactive effects of n-TiO2 and 2,3,7,8-TCDD on the marine bivalve Mytilus galloprovincialis. Aquat Toxicol 153:53–65

    Article  CAS  Google Scholar 

  • Cheung CCC, Zheng GJ, Li AMY, Richardson BJ, Lam PKS (2001) Relationships between tissue concentrations of polycyclic aromatic hydrocarbons and antioxidative responses of marine mussels, Perna viridis. Aquat Toxicol 52(3-4):189–203

    Article  CAS  Google Scholar 

  • EC (2002) Opinion of the Scientific Committee on Food on the Risks to Human Health of Polycyclic Aromatic Hydrocarbons in Food. European Commission, Health and Consumer Protection Directorate-General, Scientific Community on Food, Brussels, Belgium. SCF/CS/CNTM/PAH/29 Final

  • Farkas J, Bergum S, Nilsen EW, Olsen AJ, Salaberria I, Ciesielski TM, Jenssen BM (2015) The impact of TiO2 nanoparticles on uptake and toxicity of benzo(a)pyrene in the blue mussel (Mytilus edulis). Sci Total Environ 511(469):476

    Google Scholar 

  • Farré M, Gajda-Schrantz K, Kantiani L, Barceló D (2009) Ecotoxicity and analysis of nanomaterials in the aquatic environment. Anal Bioanal Chem 393:81–95

    Article  CAS  Google Scholar 

  • Feng J, Guo X, Chen Y, Lu D, Niu Z, Tou F, Hou L, Xu J, Liu M, Yang Y (2020) Time-dependent effects of ZnO nanoparticles on bacteria in an estuarine aquatic environment. Sci Total Environ 698:134298

    Article  CAS  Google Scholar 

  • Fkiri A, Santacruz MR, Mezni A, Smiri LS, Keller V, Keller N (2017) One-pot synthesis of lightly doped Zn 1− x Cu x O and Au–Zn 1− x Cu x O with solar light photocatalytic activity in liquid phase. Environ Sci Pollut Res 24(18):15622–15633

    Article  CAS  Google Scholar 

  • Giannapas M, Karnis L, Dailianis S (2012) Generation of free radicals in haemocytes of mussels after exposure to low molecular weight PAH components: immune activation, oxidative and genotoxic effects. Comp Biochem Physiol C 155:182–189

    CAS  Google Scholar 

  • Gornati R, Longo A, Rossi F, Maisano M, Sabatino G, Mauceri A, Bernardini G, Fasulo S (2016) Effects of titanium dioxide nanoparticle exposure in Mytilus galloprovincialis gills and digestive gland. Nanotoxicology 10(6):807–817

    Article  CAS  Google Scholar 

  • Gottschalk F, Sonderer T, Scholz RW, Nowack B (2009) Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environ Sci Technol 43:9216–9222

    Article  CAS  Google Scholar 

  • Haque MN, Eom HJ, Nam SE, Shin YK, Rhee JS (2019) Chlorothalonil induces oxidative stress and reduces enzymatic activities of Na+/K+-ATPase and acetylcholinesterase in gill tissues of marine bivalves. PLoS ONE 14(4):e0214236

    Article  CAS  Google Scholar 

  • Huang X, Liu Z, Xie Z, Dupont S, Huang W, Wu F, Kong H, Liu L, Sui Y, Lin D, Lu W, Hu M, Wang Y (2018) Oxidative stress induced by titanium dioxide nanoparticles increases under seawater acidification in the thick shell mussel Mytilus coruscus. Mar Environ Res 137:49–59

    Article  CAS  Google Scholar 

  • Hull MS, Chaurand P, Rose J, Auffan M, Bottero JY, Jones JC, Schultz IR, Vikesland PJ (2011) Filter-feeding bivalves store and biodeposit colloidally stable gold nanoparticles. Environ Sci Technol 45(15):6592–6599

    Article  CAS  Google Scholar 

  • Jackson MC, Woodford DJ, Weyl OL (2016) Linking key environmental stressors with the delivery of provisioning ecosystem services in the freshwaters of southern Africa. Geo: Geogr Environ 3(2):e00026

    Google Scholar 

  • Jiang W, Fang J, Gao Y, Du M, Fang J, Wang X, Li F, Lin F, Jiang Z (2019) Biomarkers responses in Manila clam, Ruditapes philippinarum after single and combined exposure to mercury and benzo[a]pyrene. Comp Biochem Physiol C 220:1–8

    CAS  Google Scholar 

  • Jones DP, Eklow L, Thor H, Orrenius S (1981) Metabolism of Hydrogen-Peroxide in Isolated Hepatocytes - Relative Contributions of Catalase and Glutathione-Peroxidase in Decomposition of Endogenously Generated H2O2. Arch Biochem Biophys 210:505–516

    Article  CAS  Google Scholar 

  • Leite C, Coppola F, Monteiro R, Russo T, Polese G, Lourenço MA, Pereira E (2020) Biochemical and histopathological impacts of rutile and anatase (TiO2 forms) in Mytilus galloprovincialis. Sci Total Environ 719:134886

    Article  CAS  Google Scholar 

  • Li ZW, Wang XJ, Ma BR, Wang S, Zheng D, She ZL, Guo L, Zhao YG, Xu QY, Jin CJ, Li SS, Gao MC (2017) Long-term impacts of titanium dioxide nanoparticles (TiO2 NPs) on performance and microbial community of activated sludge. Bioresour Technol 238:361–368

    Article  CAS  Google Scholar 

  • Li J, Lusher AL, Rotchell JM, Deudero S, Turra A, Bråte ILN, Shi H (2019) Using mussel as a global bioindicator of coastal microplastic pollution. Environ Pollut 244:522–533

    Article  CAS  Google Scholar 

  • Li Z, Hu M, Song H, Lin D, Wang Y (2021) Toxic effects of nano-TiO2 in bivalves—A synthesis of meta-analysis and bibliometric analysis. J Environ Sci 104:188–203

    Article  Google Scholar 

  • Luo Z, Wang Z, Li Q, Pan Q, Yan C, Liu F (2011) Spatial distribution, electron microscopy analysis of titanium and its correlation to heavy metals: occurrence and sources of titanium nanomaterials in surface sediments from Xiam en Bay, China. J Environ Monit 13:1046–1052

    Article  CAS  Google Scholar 

  • Luo Z, Li Z, Xie Z, Sokolova IM, Song L, Peijnenburg WJGM, Hu M, Wang Y (2020) Rethinking nano-TiO2 safety: overview of toxic effects in humans and aquatic animals. Smll. 16(36):2002019

    CAS  Google Scholar 

  • Manduzio H, Monsinjon T, Galap C, Leboulenger F, Rocher B (2004) Seasonal variations in antioxidant defences in blue mussels Mytilus edulis collected from a polluted area: major contributions in gills of an inducible isoform of Cu/Zn-superoxide dismutase and of glutathione S-transferase. Aquat Toxicol 70:83–93

    Article  CAS  Google Scholar 

  • Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474

    Article  CAS  Google Scholar 

  • Meador J, Sommers F, Ylitalo G, Sloan C (2006) Altered growth and related physiological responses in juvenile Chinook salmon (Oncorhynchus tshawytscha) from dietary exposure to polycyclic aromatic hydrocarbons (PAHs). Can J Fish Aquat Sci 63:2364–2376

    Article  CAS  Google Scholar 

  • Mezni A, Dammak T, Fkiri A, Mlayah A, Abid Y, Smiri LS (2014a) Photochemistry at the Surface of Gold Nanoprisms from Surface-Enhanced Raman Scattering Blinking. J Phys Chem C 118:17956–17967

    Article  CAS  Google Scholar 

  • Mezni A, Mlayah A, Serin V, Smiri LS (2014b) Synthesis of hybrid AueZnO nanoparticles using a one pot polyol process. Mater Chem Phys 30:1–8

    Google Scholar 

  • Mezni A, Saber NB, Ibrahim MM, El-Kemary M, Aldalbahi A, Feng P, Altalhi T (2017) Facile synthesis of highly thermally stable TiO2 photocatalysts. New J Chem 41(12):5021–5027

    Article  CAS  Google Scholar 

  • Mezni A, Saber NB, Ibrahim MM, Hamdaoui N, Alrooqi A, Mlayah A (2019) Photocatalytic activity of hybrid gold-titania nanocomposites. Mater Chem Phys 221:118–124

    Article  CAS  Google Scholar 

  • Mlouka R, Cachot J, Boukadida K, Clérandeau C, Gourves PY, Banni M (2019) Compared responses to copper and increased temperatures of hybrid and pure offspring of two mussel species. Sci Total Environ 685:795–805

    Article  CAS  Google Scholar 

  • Moore MN (2006) Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environ Int 32(8):967–976

    Article  CAS  Google Scholar 

  • Naasz S, Altenburger R, Kühnel D (2018) Environmental mixtures of nanomaterials and chemicals: The Trojan-horse phenomenon and its relevance for ecotoxicity. Sci Total Environ 635:1170–1181

    Article  CAS  Google Scholar 

  • Pérez-Cadahia B, Laffona B, Pasaro E, Méndez J (2004) Evaluation of PAH bioaccumulation and DNA damage in mussels (Mytilus galloprovincialis) exposed to spilled Prestige crude oil. Comp Biochem Physiol C 138:453–460

    Google Scholar 

  • Regoli F, Giuliani ME (2014) Oxidative pathways of chemical toxicity and oxidative stress biomarkers in marine organisms. Mar Environ Res 93:106–117

    Article  CAS  Google Scholar 

  • Richardson BJ, Mak E, De Luca-Abbott SB, Martin M, McClellan K, Lam PK (2008) Antioxidant responses to polycyclic aromatic hydrocarbons and organochlorine pesticides in green-lipped mussels (Perna viridis): do mussels “integrate” biomarker responses? Mar Pollut Bull 57(6-12):503–514

    Article  CAS  Google Scholar 

  • Sajjad AKL, Sajjad S, Iqbal A (2018) ZnO/WO3 nanostructure as an efficient visible light catalyst. Ceram Int 44(8):9364–9371

    Article  CAS  Google Scholar 

  • Sellami B, Khazri A, Mezni A, Louati H, Dellali M, Aissa P, Mahmoudi E, Beyrem H, Sheehan D (2015) Effect of permethrin, anthracene and mixture exposure on shell components, enzymatic activities and proteins status in the Mediterranean clam Venerupis decussata. Aquat Toxicol 158:22–32

    Article  CAS  Google Scholar 

  • Sellami B, Khazri A, Dellali M, Mahmoudi E, Sheehan D, Beyrem H (2017a) The effects of anthracene on biochemical responses of Mediterranean mussels Mytilus galloprovincialis. Chem Ecol 33(4):309–324

    Article  CAS  Google Scholar 

  • Sellami B, Mezni A, Khazri A, Bouzidi I, Saidani W, Sheehan D, Beyrem H (2017b) Toxicity assessment of ZnO-decorated Au nanoparticles in the Mediterranean clam Ruditapes decussatus. Aquat Toxicol 188:10–19

    Article  CAS  Google Scholar 

  • Stara A, Pagano M, Capillo G, Fabrello J, Sandova M, Vazzana I, Faggio C (2020) Assessing the effects of neonicotinoid insecticide on the bivalve mollusc Mytilus galloprovincialis. Sci Total Environ 700:134914

    Article  CAS  Google Scholar 

  • Tian S, Zhang Y, Song C, Zhu X, Xing B (2014) Titanium dioxide nanoparticles as carrier facilitate bioaccumulation of phenanthrene in marine bivalve, ark shell (Scapharca subcrenata). Environ Pollut 192:59–64

    Article  CAS  Google Scholar 

  • Toybou D, Celle C, Aude-Garcia C, Rabilloud T, Simonato JP (2019) A toxicology-informed, safer by design approach for the fabrication of transparent electrodes based on silver nanowires. Environ Sci Nano 6:684–694

    Article  CAS  Google Scholar 

  • Yan J, Wang L, Fu PP, Yu H (2004) Photomutagenicity of 16 polycyclic aromatic hydrocarbons from the US EPA priority pollutant list. Mutat Res Genet Toxicol Environ Mutagen 557:99–108

    Article  CAS  Google Scholar 

  • Zhou JL, Maskoui K (2003) Distribution of polycyclic aromatic hydrocarbons in water and surface sediments from Daya Bay, China. Environ Pollut 121:269–281

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors extend their appreciation to the Researchers Supporting Project (number RSP-2021/17) at King Saud University, Riyadh, Saudi Arabia..

Funding

This work was supported by grants from The Ministry of Higher Education of Carthage (Tunisia), Laboratory of Environment Biomonitoring, Faculty of Sciences of Bizerte 7021 Jarzouna (Tunisia), and Institut de Science des Matériaux de Mulhouse (IS2M). The authors extend their appreciation to the Researchers Supporting Project (number RSP-2021/17) at King Saud University, Riyadh, Saudi Arabia.

Author information

Authors and Affiliations

  1. University of Carthage, Faculty of Sciences of Bizerte, Laboratory of Environment Biomonitoring, Coastal Ecology and Ecotoxicology Unit, 7021, Zarzouna, Tunisia

    Imen Bouzidi, Fehmi Boufahja & Hamouda Beyrem

  2. Université de Strasbourg, Université de Haute Alsace, Institut de Science des Matériaux, IS2M-CNRS-UMR 7361, 15 Rue Jean Starcky, 68057, Mulhouse, France

    Imen Bouzidi, Loic Vidal, Cyril Vaulot, Ludovic Josien & Karine Mougin

  3. Laboratory of Hetero-Organic Compounds and Nanostructured Materials (LR18ES11), Faculty of Sciences of Bizerte, University of Carthage, 7021, Zarzouna, Tunis, Tunisia

    Anis Fkiri & Amine Mezni

  4. Institut National des Sciences et Technologies de la Mer, Tabarka, Tunisia

    Badreddine Sellami

  5. Zoology Department, College of Science, King Saud University, Box 2455, Riyadh, 11451, Saudi Arabia

    Abdel Halim Harrath

Authors
  1. Imen Bouzidi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anis Fkiri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Badreddine Sellami
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Abdel Halim Harrath
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fehmi Boufahja
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Amine Mezni
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Loic Vidal
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Cyril Vaulot
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ludovic Josien
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hamouda Beyrem
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Karine Mougin
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Bouzidi Imen: formal analysis, validation, writing (original draft), writing (review and editing). Fkiri Anis: investigation, writing (review and editing). Sellami Badreddine: conceptualization, formal analysis, investigation, writing (review and editing). Abdel Halim Harrath: funding acquisition, writing (review and editing). Fehmi Boufahja: writing (review and editing). Mezni Amine: methodology, investigation, writing. Loic Vidal: methodology, formal analysis, validation. Cyril Vaulot: methodology, investigation. Ludovic Josien: validation, formal analysis. H. Beyrem: data curation, supervision, investigation. Mougin Karine: funding acquisition, methodology, supervision, validation, writing (review and editing).

Corresponding author

Correspondence to Imen Bouzidi.

Ethics declarations

Ethical approval

Not applicable

Consent to participate

Informed consent was obtained from all individual participants included in the study.

Consent to Publish

Not applicable

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible Editor: Cinta Porte

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bouzidi, I., Fkiri, A., Sellami, B. et al. Does the photocatalytic activity of nanoparticles protect the marine mussel Mytilus galloprovincialis from polycyclic aromatic hydrocarbon toxicity?. Environ Sci Pollut Res 28, 44301–44314 (2021). https://doi.org/10.1007/s11356-021-13908-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-13908-4

Keywords

Search

Navigation