Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Silver nanoparticles (AgNPs) internalization and passage through the Lactuca sativa (Asteraceae) outer cell wall

Sergimar Kennedy de Paiva Pinheiro https://orcid.org/0000-0002-6232-9069 A , Thaiz Batista Azevedo Rangel Miguel B , Marlos de Medeiros Chaves A , Francisco Claudio de Freitas Barros C , Camila Pessoa Farias C , Thiago Alves de Moura D , Odair Pastor Ferreira C , Alexandre Rocha Paschoal D , Antonio Gomes Souza Filho E and Emilio de Castro Miguel A *
+ Author Affiliations
- Author Affiliations

A Biomaterials Laboratory (BIOMAT), Department of Metallurgical Engineering and Materials (DEMM) and Analytical Center, Federal University of Ceará (UFC), Campus do Pici Fortaleza, CEP 60455-900, Fortaleza, CE, Brazil.

B Biotechnology Laboratory, Food Engineering Department, Federal University of Ceará (UFC), Campus do Pici Fortaleza, Fortaleza, CE, Brazil.

C Advanced Functional Materials Laboratory (LaMFA), Department of Physics, Federal University of Ceará, Fortaleza, CE, Brazil.

D Tip Enhanced Raman Spectroscopy Laboratory, Department of Physics, Federal University of Ceará (UFC), Fortaleza, CE, Brazil.

E Physics Department, School of Science, Federal University of Ceará (UFC), Campus do Pici Fortaleza, Fortaleza 60455-900, CE, Brazil.

* Correspondence to: emiliomiguel@ufc.br

Handling Editor: Honghong Wu

Functional Plant Biology 48(11) 1113-1123 https://doi.org/10.1071/FP21161
Submitted: 22 October 2020  Accepted: 11 July 2021   Published: 29 September 2021

© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Silver nanoparticle (AgNPs) toxicity is related to nanoparticle interaction with the cell wall of microorganisms and plants. This interaction alters cell wall conformation with increased reactive oxygen species (ROS) in the cell. With the increase of ROS in the cell, the dissolution of zero silver (Ag0) to ionic silver (Ag+) occurs, which is a strong oxidant agent to the cellular wall. AgNP interaction was evaluated by transmission electron microscopy (TEM) on Lactuca sativa roots, and the mechanism of passage through the outer cell wall (OCW) was also proposed. The results suggest that Ag+ binds to the hydroxyls (OH) present in the cellulose structure, thus causing the breakdown of the hydrogen bonds. Changes in cell wall structure facilitate the passage of AgNPs, reaching the plasma membrane. According to the literature, silver nanoparticles with an average diameter of 15 nm are transported across the membrane into the cells by caveolines. This work describes the interaction between AgNPs and the cell wall and proposes a transport model through the outer cell wall.

Keywords: AgNPs, cell wall, electron microscopy, nanotoxicology, outer cell wall, plant NPs interaction, Raman spectroscopy, silver nanoparticles.


References

Abedin M, King N (2010) Diverse evolutionary paths to cell adhesion. Trends in Cell Biology 20, 734–742.
Diverse evolutionary paths to cell adhesion.Crossref | GoogleScholarGoogle Scholar | 20817460PubMed |

Adams CP, Walker KA, Obare SO, Docherty KM (2014) Size-dependent antimicrobial effects of novel palladium nanoparticles. PLoS One 9, e85981
Size-dependent antimicrobial effects of novel palladium nanoparticles.Crossref | GoogleScholarGoogle Scholar | 24465824PubMed |

Akinc A, Battaglia G (2013) Exploiting endocytosis for nanomedicines. Cold Spring Harbor Perspectives in Biology 5, a016980
Exploiting endocytosis for nanomedicines.Crossref | GoogleScholarGoogle Scholar | 24186069PubMed |

Amato E, Diaz-Fernandez YA, Taglietti A, Pallavicini P, Pasotti L, Cucca L, Milanese C, Grisoli P, Dacarro C, Fernandez-Hechavarria JM, Necchi V (2011) Synthesis, characterization and antibacterial activity against gram positive and gram negative bacteria of biomimetically coated silver nanoparticles. Langmuir 27, 9165–9173.
Synthesis, characterization and antibacterial activity against gram positive and gram negative bacteria of biomimetically coated silver nanoparticles.Crossref | GoogleScholarGoogle Scholar | 21736306PubMed |

Anjum NA, Rodrigo MAM, Moulick A, Heger Z, Kopel P, Zítka O, Adam V, Lukatkin AS, Duarte AC, Pereira E, Kizek R (2016) Transport phenomena of nanoparticles in plants and animals/humans. Environmental Research 151, 233–243.
Transport phenomena of nanoparticles in plants and animals/humans.Crossref | GoogleScholarGoogle Scholar | 27504871PubMed |

Ansari MA, Khan HM, Khan AA, Cameotra SS, Pal R (2014) Antibiofilm efficacy of silver nanoparticles against biofilm of extended spectrum β-lactamase isolates of Escherichia coli and Klebsiella pneumoniae. Applied Nanoscience 4, 859–868.
Antibiofilm efficacy of silver nanoparticles against biofilm of extended spectrum β-lactamase isolates of Escherichia coli and Klebsiella pneumoniae.Crossref | GoogleScholarGoogle Scholar |

AshaRani PV, Mun GLK, Hande MP, Valiyaveettil S (2009) Cytotoxicity and genotoxicity of silver nanomaterials in human cells. ACS Nano 3, 279–290.
Cytotoxicity and genotoxicity of silver nanomaterials in human cells.Crossref | GoogleScholarGoogle Scholar | 19236062PubMed |

Athie-García MS, Piñón-Castillo HA, Muñoz-Castellanos LN, Ulloa-Ogaz AL, Martínez-Varela PI, Quintero-Ramos A, Duran R, Murillo-Ramirez JG, Orrantia-Borunda E (2018) Cell wall damage and oxidative stress in Candida albicans ATCC10231 and Aspergillus niger caused by palladium nanoparticles. Toxicology In Vitro 48, 111–120.
Cell wall damage and oxidative stress in Candida albicans ATCC10231 and Aspergillus niger caused by palladium nanoparticles.Crossref | GoogleScholarGoogle Scholar | 29331636PubMed |

Auffan M, Bottero J-Y, Chaneac C, Rose J (2010) Inorganic manufactured nanoparticles: how their physicochemical properties influence their biological effects in aqueous environments. Nanomedicine 5, 999–1007.
Inorganic manufactured nanoparticles: how their physicochemical properties influence their biological effects in aqueous environments.Crossref | GoogleScholarGoogle Scholar | 20735233PubMed |

Babele PK, Thakre PK, Kumawat R, Tomar RS (2018) Zinc oxide nanoparticles induce toxicity by affecting cell wall integrity pathway, mitochondrial function and lipid homeostasis in Saccharomyces cerevisiae. Chemosphere 213, 65–75.
Zinc oxide nanoparticles induce toxicity by affecting cell wall integrity pathway, mitochondrial function and lipid homeostasis in Saccharomyces cerevisiae.Crossref | GoogleScholarGoogle Scholar | 30212720PubMed |

Barngrover BM, Aikens CM (2011) Incremental binding energies of gold(I) and silver(I) thiolate clusters. Journal of Physical Chemistry A 115, 11818–11823.
Incremental binding energies of gold(I) and silver(I) thiolate clusters.Crossref | GoogleScholarGoogle Scholar |

Barrena R, Casals E, Colón J, Font X, Sánchez A, Puntes V (2009) Evaluation of the ecotoxicity of model nanoparticles. Chemosphere 75, 850–857.
Evaluation of the ecotoxicity of model nanoparticles.Crossref | GoogleScholarGoogle Scholar | 19264345PubMed |

Biswas N, Kapoor S, Mahal HS, Mukherjee T (2007) Adsorption of CGA on colloidal silver particles: DFT and SERS study. Chemical Physics Letters 444, 338–345.
Adsorption of CGA on colloidal silver particles: DFT and SERS study.Crossref | GoogleScholarGoogle Scholar |

Boran H, Boyle D, Altinok I, Patsiou D, Henry TB (2016) Aqueous Hg(2+) associates with TiO2 nanoparticles according to particle size, changes particle agglomeration, and becomes less bioavailable to zebrafish. Aquatic Toxicology 174, 242–246.
Aqueous Hg(2+) associates with TiO2 nanoparticles according to particle size, changes particle agglomeration, and becomes less bioavailable to zebrafish.Crossref | GoogleScholarGoogle Scholar | 26970871PubMed |

Brasil, Ministério da Agricultura Pecuária e Abastecimento (2009) ‘Regras para análise de sementes. (Ed. Assessoria de Comunicação Social). (Biblioteca Nacional de Agricultura – BINAGRI Brasil: Brasilia, Brazil). 10.2307/2261447

Chelikani P, Fita I, Loewen PC (2004) Diversity of structures and properties among catalases. Cellular and Molecular Life Sciences 61, 192–208.
Diversity of structures and properties among catalases.Crossref | GoogleScholarGoogle Scholar | 14745498PubMed |

Chichiriccò G, Poma A (2015) Penetration and toxicity of nanomaterials in higher plants. Nanomaterials 5, 851–873.
Penetration and toxicity of nanomaterials in higher plants.Crossref | GoogleScholarGoogle Scholar | 28347040PubMed |

Christian P, Von der Kammer F, Baalousha M, Hofmann T (2008) Nanoparticles: structure, properties, preparation and behaviour in environmental media. Ecotoxicology 17, 326–343.
Nanoparticles: structure, properties, preparation and behaviour in environmental media.Crossref | GoogleScholarGoogle Scholar | 18459043PubMed |

Concha-Guerrero SI, Brito EMS, Piñón-Castillo HA, Tarango-Rivero SH, Caretta CA, Luna-Velasco A, Duran R, Orrantia-Borunda E (2014) Effect of CuO nanoparticles over isolated bacterial strains from agricultural soil. Journal of Nanomaterials 2014, 148743
Effect of CuO nanoparticles over isolated bacterial strains from agricultural soil.Crossref | GoogleScholarGoogle Scholar |

Costa Verdera H, Gitz-Francois JJ, Schiffelers RM, Vader P (2017) Cellular uptake of extracellular vesicles is mediated by clathrin-independent endocytosis and macropinocytosis. Journal of Controlled Release 266, 100–108.
Cellular uptake of extracellular vesicles is mediated by clathrin-independent endocytosis and macropinocytosis.Crossref | GoogleScholarGoogle Scholar | 28919558PubMed |

Daffé M (2015) The cell envelope of tubercle bacilli. Tuberculosis 95, S155–S158.
The cell envelope of tubercle bacilli.Crossref | GoogleScholarGoogle Scholar | 25819158PubMed |

de Paiva Pinheiro SK, de Medeiros Chaves M, Rangel Miguel TBA, de Freitas Barros FC, Farias CP, Ferreira OP, de Castro Miguel E (2020) Toxic effects of silver nanoparticles on the germination and root development of lettuce (Lactuca sativa). Australian Journal of Botany 68, 127–136.
Toxic effects of silver nanoparticles on the germination and root development of lettuce (Lactuca sativa).Crossref | GoogleScholarGoogle Scholar |

Dibrov P, Dzioba J, Gosink KK, Hase CC (2002) Chemiosmotic mechanism of antimicrobial activity of Ag+ in Vibrio cholerae. Antimicrobial Agents and Chemotherapy 46, 2668–2670.
Chemiosmotic mechanism of antimicrobial activity of Ag+ in Vibrio cholerae.Crossref | GoogleScholarGoogle Scholar | 12121953PubMed |

Eckhardt S, Brunetto PS, Gagnon J, Priebe M, Giese B, Fromm KM (2013) Nanobio silver: its interactions with peptides and bacteria, and its uses in medicine. Chemical Reviews 113, 4708–4754.
Nanobio silver: its interactions with peptides and bacteria, and its uses in medicine.Crossref | GoogleScholarGoogle Scholar | 23488929PubMed |

Feynman RP (1960) There’s plenty of room at the bottom. Engineering and Science 23, 22–36.

Geisler-Lee J, Wang Q, Yao Y, Zhang W, Geisler M, Li K, Huang Y, Chen Y, Kolmakov A, Ma X (2013) Phytotoxicity, accumulation and transport of silver nanoparticles by Arabidopsis thaliana. Nanotoxicology 7, 323–337.
Phytotoxicity, accumulation and transport of silver nanoparticles by Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 22263604PubMed |

Gleiter H (2000) Nanostructured materials: basic concepts and microstructure. Acta Materialia 48, 1–29.
Nanostructured materials: basic concepts and microstructure.Crossref | GoogleScholarGoogle Scholar |

Guo D, Zhu L, Huang Z, Zhou H, Ge Y, Ma W, Wu J, Zhang X, Zhou X, Zhang Y, Zhao Y, Gu N (2013) Anti-leukemia activity of PVP-coated silver nanoparticles via generation of reactive oxygen species and release of silver ions. Biomaterials 34, 7884–7894.
Anti-leukemia activity of PVP-coated silver nanoparticles via generation of reactive oxygen species and release of silver ions.Crossref | GoogleScholarGoogle Scholar | 23876760PubMed |

Höfte H, Voxeur A (2017) Plant cell walls. Current Biology 27, R865–R870.
Plant cell walls.Crossref | GoogleScholarGoogle Scholar | 28898654PubMed |

Hon DNS (1994) Cellulose: a random walk along its historical path. Cellulose 1, 1–25.
Cellulose: a random walk along its historical path.Crossref | GoogleScholarGoogle Scholar |

Hoson T, Wakabayashi K (2015) Role of the plant cell wall in gravity resistance. Phytochemistry 112, 84–90.
Role of the plant cell wall in gravity resistance.Crossref | GoogleScholarGoogle Scholar | 25236694PubMed |

Iannone MF, Groppa MD, de Sousa ME, Fernández van Raap MB, Benavides MP (2016) Impact of magnetite iron oxide nanoparticles on wheat (Triticum aestivum L.) development: evaluation of oxidative damage. Environmental and Experimental Botany 131, 77–88.
Impact of magnetite iron oxide nanoparticles on wheat (Triticum aestivum L.) development: evaluation of oxidative damage.Crossref | GoogleScholarGoogle Scholar |

Jiang X, Musyanovych A, Röcker C, Landfester K, Mailänder V, Ulrich Nienhaus G (2011) Specific effects of surface amines polystyrene nanoparticles in their interactions with mesenchymal stem cells. Nanoscale 3, 2028–2035.
Specific effects of surface amines polystyrene nanoparticles in their interactions with mesenchymal stem cells.Crossref | GoogleScholarGoogle Scholar | 21409242PubMed |

Kar B, Patel P, Ao J, Free SJ (2019) Neurospora crassa family GH72 glucanosyltransferases function to crosslink cell wall glycoprotein N-linked galactomannan to cell wall lichenin. Fungal Genetics and Biology 123, 60–69.
Neurospora crassa family GH72 glucanosyltransferases function to crosslink cell wall glycoprotein N-linked galactomannan to cell wall lichenin.Crossref | GoogleScholarGoogle Scholar | 30503329PubMed |

Keegstra K (2010) Plant cell walls. Plant Physiology 154, 483–486.
Plant cell walls.Crossref | GoogleScholarGoogle Scholar | 20921169PubMed |

Kim JH, Lee Y, Kim EJ, Gu S, Sohn EJ, Seo YS, An HJ, Chang YS (2014) Exposure of iron nanoparticles to Arabidopsis thaliana enhances root elongation by triggering cell wall loosening. Environmental Science & Technology 48, 3477–3485.
Exposure of iron nanoparticles to Arabidopsis thaliana enhances root elongation by triggering cell wall loosening.Crossref | GoogleScholarGoogle Scholar |

Lara HH, Ixtepan-Turrent L, Garza-Treviño EN, Rodriguez-Padilla C (2010) PVP-coated silver nanoparticles block the transmission of cell-free and cell-associated HIV-1 in human cervical culture. Journal of Nanobiotechnology 8, 15
PVP-coated silver nanoparticles block the transmission of cell-free and cell-associated HIV-1 in human cervical culture.Crossref | GoogleScholarGoogle Scholar | 20626911PubMed |

Le Ouay B, Stellacci F (2015) Antibacterial activity of silver nanoparticles: a surface science insight. Nano Today 10, 339–354.
Antibacterial activity of silver nanoparticles: a surface science insight.Crossref | GoogleScholarGoogle Scholar |

Lee WM, An YJ, Yoon H, Kweon HS (2008) Toxicity and bioavailability of copper nanoparticles to the terrestrial plants mung bean (Phaseolus radiatus) and wheat (Triticum aestivum): plant agar test for water-insoluble nanoparticles. Environmental Toxicology and Chemistry 27, 1915–1921.
Toxicity and bioavailability of copper nanoparticles to the terrestrial plants mung bean (Phaseolus radiatus) and wheat (Triticum aestivum): plant agar test for water-insoluble nanoparticles.Crossref | GoogleScholarGoogle Scholar | 19086317PubMed |

Leung YH, Chan CMN, Ng AMC, Chan HT, Chiang MWL, Djurišić AB, Ng YH, Jim WY, Guo MY, Leung FCC, Chan WK, Au DTW (2012) Antibacterial activity of ZnO nanoparticles with a modified surface under ambient illumination. Nanotechnology 23, 475703
Antibacterial activity of ZnO nanoparticles with a modified surface under ambient illumination.Crossref | GoogleScholarGoogle Scholar | 23103840PubMed |

Liu J, Hurt RH (2010) Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environmental Science & Technology 44, 2169–2175.
Ion release kinetics and particle persistence in aqueous nano-silver colloids.Crossref | GoogleScholarGoogle Scholar |

Liu Y, Mark Worden R (2015) Size dependent disruption of tethered lipid bilayers by functionalized polystyrene nanoparticles. Biochimica et Biophysica Acta – Biomembranes 1848, 67–75.
Size dependent disruption of tethered lipid bilayers by functionalized polystyrene nanoparticles.Crossref | GoogleScholarGoogle Scholar |

Loza K, Diendorf J, Sengstock C, Ruiz-Gonzalez L, Gonzalez-Calbet JM, Vallet-Regi M, Köller M, Epple M (2014) The dissolution and biological effects of silver nanoparticles in biological media. Journal of Materials Chemistry B 2, 1634–1643.
The dissolution and biological effects of silver nanoparticles in biological media.Crossref | GoogleScholarGoogle Scholar | 32261391PubMed |

Marambio-Jones C, Hoek EMV (2010) A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment. Journal of Nanoparticle Research 12, 1531–1551.
A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment.Crossref | GoogleScholarGoogle Scholar |

McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nature Reviews Molecular Cell Biology 12, 517–533.
Molecular mechanism and physiological functions of clathrin-mediated endocytosis.Crossref | GoogleScholarGoogle Scholar | 21779028PubMed |

Meyer DE, Curran MA, Gonzalez MA (2009) An examination of existing data for the industrial manufacture and use of nanocomponents and their role in the life cycle impact of nanoproducts. Environmental Science & Technology 43, 1256–1263.
An examination of existing data for the industrial manufacture and use of nanocomponents and their role in the life cycle impact of nanoproducts.Crossref | GoogleScholarGoogle Scholar |

Mirzajani F, Ghassempour A, Aliahmadi A, Esmaeili MA (2011) Antibacterial effect of silver nanoparticles on Staphylococcus aureus. Research in Microbiology 162, 542–549.
Antibacterial effect of silver nanoparticles on Staphylococcus aureus.Crossref | GoogleScholarGoogle Scholar | 21530652PubMed |

Murugan A, Shanmugasundaram K (2014) Biosynthesis and characterization of silver nanoparticles using the aqueous extract of Vitex negundo Linn. World Journal of Pharmacy and Pharmaceutical Sciences 3, 1385–1393.

Nowack B, Krug HF, Height M (2011) 120 years of nanosilver history: implications for policy makers. Environmental Science & Technology 45, 1177–1183.
120 years of nanosilver history: implications for policy makers.Crossref | GoogleScholarGoogle Scholar |

Piccapietra F, Allue CG, Sigg L, Behra R (2012) Intracellular silver accumulation in Chlamydomonas reinhardtii upon exposure to carbonate coated silver nanoparticles and silver nitrate. Environmental Science & Technology 46, 7390–7397.
Intracellular silver accumulation in Chlamydomonas reinhardtii upon exposure to carbonate coated silver nanoparticles and silver nitrate.Crossref | GoogleScholarGoogle Scholar |

Poptoshev E, Carambassis A, Österberg M, Claesson PM, Rutland MW (2000) Comparison of model surfaces for cellulose interactions: elevated pH. In ‘Surface and colloid science. Progress in colloid and polymer science. Vol. 116’. (Eds V Razumas, B Lindman, T Nylander) pp. 79–83. (Springer: Berlin, Germany)

Radniecki TS, Stankus DP, Neigh A, Nason JA, Semprini L (2011) Influence of liberated silver from silver nanoparticles on nitrification inhibition of Nitrosomonas europaea. Chemosphere 85, 43–49.
Influence of liberated silver from silver nanoparticles on nitrification inhibition of Nitrosomonas europaea.Crossref | GoogleScholarGoogle Scholar | 21757219PubMed |

Rastogi A, Zivcak M, Sytar O, Kalaji HM, He X, Mbarki S, Brestic M (2017) Impact of metal and metal oxide nanoparticles on plant: a critical review. Frontiers in Chemistry 5, 78
Impact of metal and metal oxide nanoparticles on plant: a critical review.Crossref | GoogleScholarGoogle Scholar | 29075626PubMed |

Sahay G, Alakhova DY, Kabanov AV (2010) Endocytosis of nanomedicines. Journal of Controlled Release 145, 182–195.
Endocytosis of nanomedicines.Crossref | GoogleScholarGoogle Scholar | 20226220PubMed |

Schopfer P (2001) Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. The Plant Journal 28, 679–688.

Sendra M, Sánchez-Quiles D, Blasco J, Moreno-Garrido I, Lubián LM, Pérez-García S, Tovar-Sánchez A (2017) Effects of TiO2 nanoparticles and sunscreens on coastal marine microalgae: ultraviolet radiation is key variable for toxicity assessment. Environment International 98, 62–68.
Effects of TiO2 nanoparticles and sunscreens on coastal marine microalgae: ultraviolet radiation is key variable for toxicity assessment.Crossref | GoogleScholarGoogle Scholar | 27712934PubMed |

Thuesombat P, Hannongbua S, Akasit S, Chadchawan S (2014) Effect of silver nanoparticles on rice (Oryza sativa L. cv. KDML 105) seed germination and seedling growth. Ecotoxicology and Environmental Safety 104, 302–309.
Effect of silver nanoparticles on rice (Oryza sativa L. cv. KDML 105) seed germination and seedling growth.Crossref | GoogleScholarGoogle Scholar | 24726943PubMed |

Tombuloglu H, Slimani Y, Tombuloglu G, Almessiere M, Baykal A (2019) Uptake and translocation of magnetite (Fe3O4) nanoparticles and its impact on photosynthetic genes in barley (Hordeum vulgare L.). Chemosphere 226, 110–122.
Uptake and translocation of magnetite (Fe3O4) nanoparticles and its impact on photosynthetic genes in barley (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar | 30925403PubMed |

Vance ME, Kuiken T, Vejerano EP, McGinnis SP, Hochella MF, Rejeski D, Hull MS (2015) Nanotechnology in the real world: redeveloping the nanomaterial consumer products inventory. Beilstein Journal of Nanotechnology 6, 1769–1780.
Nanotechnology in the real world: redeveloping the nanomaterial consumer products inventory.Crossref | GoogleScholarGoogle Scholar | 26425429PubMed |

Voigt J, Stolarczyk A, Zych M, Malec P, Burczyk J (2014) The cell-wall glycoproteins of the green alga Scenedesmus obliquus. The predominant cell-wall polypeptide of Scenedesmus obliquus is related to the cell-wall glycoprotein gp3 of Chlamydomonas reinhardtii. Plant Science 215–216, 39–47.
The cell-wall glycoproteins of the green alga Scenedesmus obliquus. The predominant cell-wall polypeptide of Scenedesmus obliquus is related to the cell-wall glycoprotein gp3 of Chlamydomonas reinhardtii.Crossref | GoogleScholarGoogle Scholar | 24388513PubMed |

Wanasekara ND, Michud A, Zhu C, Rahatekar S, Sixta H, Eichhorn SJ (2016) Deformation mechanisms in ionic liquid spun cellulose fibers. Polymer 99, 222–230.
Deformation mechanisms in ionic liquid spun cellulose fibers.Crossref | GoogleScholarGoogle Scholar |

Wang P, Zhang B, Zhang H, He Y, Ong CN, Yang J (2019) Metabolites change of Scenedesmus obliquus exerted by AgNPs. Journal of Environmental Sciences 76, 310–318.
Metabolites change of Scenedesmus obliquus exerted by AgNPs.Crossref | GoogleScholarGoogle Scholar |

Wiley JH, Atalla RH (1987) Band assignments in the Raman spectra of celluloses. Carbohydrate Research 160, 113–129.
Band assignments in the Raman spectra of celluloses.Crossref | GoogleScholarGoogle Scholar |

Yameen B, Choi WI, Vilos C, Swami A, Shi J, Farokhzad OC (2014) Insight into nanoparticle cellular uptake and intracellular targeting. Journal of Controlled Release 190, 485–499.
Insight into nanoparticle cellular uptake and intracellular targeting.Crossref | GoogleScholarGoogle Scholar | 24984011PubMed |

Yang X, Pan H, Wang P, Zhao FJ (2017) Particle-specific toxicity and bioavailability of cerium oxide (CeO2) nanoparticles to Arabidopsis thaliana. Journal of Hazardous Materials 322, 292–300.
Particle-specific toxicity and bioavailability of cerium oxide (CeO2) nanoparticles to Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 27021431PubMed |

Yuan Z, Li J, Cui L, Xu B, Zhang H, Yu CP (2013) Interaction of silver nanoparticles with pure nitrifying bacteria. Chemosphere 90, 1404–1411.
Interaction of silver nanoparticles with pure nitrifying bacteria.Crossref | GoogleScholarGoogle Scholar | 22985593PubMed |

Zhang C, Hu Z, Deng B (2016b) Silver nanoparticles in aquatic environments: physiochemical behavior and antimicrobial mechanisms. Water Research 88, 403–427.
Silver nanoparticles in aquatic environments: physiochemical behavior and antimicrobial mechanisms.Crossref | GoogleScholarGoogle Scholar | 26519626PubMed |

Zhang L, He Y, Goswami N, Xie J, Zhang B, Tao X (2016a) Uptake and effect of highly fluorescent silver nanoclusters on Scenedesmus obliquus. Chemosphere 153, 322–331.
Uptake and effect of highly fluorescent silver nanoclusters on Scenedesmus obliquus.Crossref | GoogleScholarGoogle Scholar | 27023120PubMed |

Zhang Z, Kong F, Vardhanabhuti B, Mustapha A, Lin M (2012) Detection of engineered silver nanoparticle contamination in pears. Journal of Agricultural and Food Chemistry 60, 10762–10767.
Detection of engineered silver nanoparticle contamination in pears.Crossref | GoogleScholarGoogle Scholar | 23082953PubMed |