Quantification of palladium-labelled nanoplastics algal uptake by single cell and single particle inductively coupled plasma mass spectrometry

Elizabeth C. Bair; Zhangzhen Guo; Tammi L. Richardson; Jamie R. Lead

doi:10.1071/EN24011

RESEARCH ARTICLE

Previous Contents Vol 21(5)

Quantification of palladium-labelled nanoplastics algal uptake by single cell and single particle inductively coupled plasma mass spectrometry

Elizabeth C. Bair

^A , Zhangzhen Guo ^B , Tammi L. Richardson

^C and Jamie R. Lead ^A ^*

+ Author Affiliations

- Author Affiliations

^A Department of Environmental Health Sciences, Arnold School of Public Health, University of South Carolina, Columbia, SC 29208, USA.

^B Department of Environmental Science, College of Resources and Environment, Shanxi Agricultural University, Taigu, Jinzhong City, Shanxi, 030801, PR China.

^C Department of Biological Sciences and School of the Earth, Ocean and Environment, University of South Carolina, Columbia, SC 29208, USA.

^* Correspondence to: jlead@mailbox.sc.edu

Handling Editor: Graeme Batley

Environmental Chemistry 21, EN24011 https://doi.org/10.1071/EN24011

Submitted: 17 February 2024 Accepted: 2 August 2024 Published: 27 August 2024

Abstract

Environmental context

Plastic pollution is widespread and continues to be a major concern, both for the environment and human health. Identifying nanoplastics is challenging but is important to understand how they behave once in the environment. It is shown that a combination of single particle (SP) and single cell (SC) inductively coupled plasma mass spectrometry (ICP-MS) can be used to quantify nanoplastics on a per cell basis after exposure to algal cells.

Abstract

The effects of plastic pollution on human health and the environment are not well known but there are significant concerns. Although research has increased in recent years, there remain many obstacles to the quantification of nanoplastics. This rapid communication demonstrates that combined single particle (SP)– and single cell (SC)–inductively coupled plasma–mass spectrometry (ICP-MS) provide a novel means to quantify pre-formed core–shell metal–plastic composite nanoparticles when exposed to two freshwater algal cells, Cryptomonas ovata (C. ovata) and Cryptomonas ozolini (C. ozolini). It is shown that individual palladium plastic nanoparticles (Pd NPPs) exposed to algal cells form agglomerates in the cell suspension respectively consisting of 165 and 157 (±3.8) individual Pd NPPs for C. ozolini and C. ovata cells, and that the agglomerates are also cell-associated with 1.75–1.85 agglomerates per cell.

Keywords: algae, algal exposure to nanoplastics, core shell nanoparticles, environmental nanoscience, freshwater algae, nanoparticles, nanoplastics, plastic nanoparticles, single cell, single particle, SC-ICP-MS, SP-ICP-MS.

References

Baalousha M, Lead JR (2012) Rationalizing nanomaterial sizes measured by atomic force microscopy, flow field-flow fractionation, and dynamic light scattering: sample preparation, polydispersity, and particle structure. Environmental Science & Technology 46, 6134-6142.
| Crossref | Google Scholar | PubMed |

Baalousha M, Ju-Nam Y, Cole PA, Gaiser B, Fernandes TF, Hriljac JA, Jepson MA, Stone V, Tyler CR, Lead JR (2012a) Characterization of cerium oxide nanoparticles – part 1: size measurements. Environmental Toxicology and Chemistry 31, 983-993.
| Crossref | Google Scholar |

Baalousha M, Ju-nam Y, Cole PA, Hriljac JA, Jones IP, Tyler CR, Stone V, Fernandes TF, Jepson MA, Lead JR (2012b) Characterization of cerium oxide nanoparticles – part 2: nonsize measurements. Environmental Toxicology and Chemistry 31, 994-1003.
| Crossref | Google Scholar |

Bi X, Lee S, Ranville JF, Sattigeri P, Spanias A, Herckes P, Westerhoff P (2014) Quantitative resolution of nanoparticle sizes using single particle inductively coupled plasma mass spectrometry with the K-means clustering algorithm. Journal of Analytical Atomic Spectrometry 29, 1630-1639.
| Crossref | Google Scholar |

Cao J, Liao Y, Yang W, Jiang X, Li M (2022) Enhanced microalgal toxicity due to polystyrene nanoplastics and cadmium co-exposure: from the perspective of physiological and metabolomic profiles. Journal of Hazardous Materials 427, 127937.
| Crossref | Google Scholar | PubMed |

Carr SA, Liu J, Tesoro AG (2016) Transport and fate of microplastic particles in wastewater treatment plants. Water Resources 91, 174-182.
| Crossref | Google Scholar | PubMed |

Cassano D, Bogni A, La Spina R, Gilliland D, Ponti J (2023) Investigating the cellular uptake of model nanoplastics by single-cell ICP-MS. Nanomaterials 13, 594.
| Crossref | Google Scholar | PubMed |

Chang X, Xue Y, Li J, Zou L, Tang M (2020) Potential health impact of environmental micro‐ and nanoplastics pollution. Journal of Applied Toxicology 40, 4-15.
| Crossref | Google Scholar | PubMed |

Danopoulos E, Twiddy M, West R, Rotchell JM (2022) A rapid review and meta-regression analyses of the toxicological impacts of microplastic exposure in human cells. Journal of Hazardous Materials 427, 127861.
| Crossref | Google Scholar | PubMed |

Domingos RF, Baalousha MA, Ju-Nam Y, Reid MM, Tufenkji N, Lead JR, Leppard GG, Wilkinson KJ (2009) Characterizing manufactured nanoparticles in the environment: multimethod determination of particle sizes. Environmental Science & Technology 43, 7277-7284.
| Crossref | Google Scholar | PubMed |

Ferreira I, Venâncio C, Lopes I, Oliveira M (2019) Nanoplastics and marine organisms: what has been studied? Environmental Toxicology and Pharmacology 67, 1-7.
| Crossref | Google Scholar | PubMed |

Gigault J, Halle AT, Baudrimont M, Pascal P-Y, Gauffre F, Phi T-L, El Hadri H, Grassl B, Reynaud S (2018) Current opinion: what is a nanoplastic? Environmental Pollution 235, 1030-1034.
| Crossref | Google Scholar | PubMed |

Gonçalves JM, Bebianno MJ (2021) Nanoplastics impact on marine biota: a review. Environmental Pollution 273, 116426.
| Crossref | Google Scholar | PubMed |

Hartmann NB, Rist S, Bodin J, Jensen LH, Schmidt SN, Mayer P, Meibom A, Baun A (2017) Microplastics as vectors for environmental contaminants: exploring sorption, desorption, and transfer to biota. Integrated Environmental Assessment and Management 13, 488-493.
| Crossref | Google Scholar | PubMed |

Hendriks L, Kissling VM, Buerki-Thurnherr T, Mitrano DM (2023) Development of single-cell ICP-TOFMS to measure nanoplastics association with human cells. Environmental Science: Nano 10, 3439-3449.
| Crossref | Google Scholar | PubMed |

Huang D, Tao J, Cheng M, Deng R, Chen S, Yin L, Li R (2021) Microplastics and nanoplastics in the environment: macroscopic transport and effects on creatures. Journal of Hazardous Materials 407, 124399.
| Crossref | Google Scholar | PubMed |

Kashiwada S (2006) Distribution of nanoparticles in the see-through medaka (Oryzias latipes). Environmental Health Perspectives 114, 1697-1702.
| Crossref | Google Scholar | PubMed |

Kińska K, Jiménez-Lamana J, kowalska J, Krasnodębska-Ostręga B, Szpunar J (2018) Study of the uptake and bioaccumulation of palladium nanoparticles by Sinapis alba using single particle ICP-MS. Science of the Total Environment 615, 1078-1085.
| Crossref | Google Scholar | PubMed |

Lead JR, Batley GE, Alvarez PJJ, Croteau MN, Handy RD, Mclaughlin MJ, Judy JD, Schirmer K (2018) Nanomaterials in the environment: behavior, fate, bioavailability, and effects – an updated review. Environmental Toxicology and Chemistry 37, 2029-2063.
| Crossref | Google Scholar | PubMed |

Lee S, Bi X, Reed RB, Ranville JF, Herckes P, Westerhoff P (2014) Nanoparticle size detection limits by single particle ICP-MS for 40 elements. Environmental Science & Technology 48, 10291-10300.
| Crossref | Google Scholar | PubMed |

Long M, Moriceau B, Gallinari M, Lambert C, Huvet A, Raffray J, Soudant P (2015) Interactions between microplastics and phytoplankton aggregates: impact on their respective fates. Marine Chemistry 175, 39-46.
| Crossref | Google Scholar |

Mattsson K, Adolfsson K, Ekvall MT, Borgström MT, Linse S, Hansson L-A, Cedervall T, Prinz CN (2016) Translocation of 40 nm diameter nanowires through the intestinal epithelium of Daphnia magna. Nanotoxicology 10, 1160-1167.
| Crossref | Google Scholar | PubMed |

Mattsson K, Johnson EV, Malmendal A, Linse S, Hansson L-A, Cedervall T (2017) Brain damage and behavioural disorders in fish induced by plastic nanoparticles delivered through the food chain. Scientific Reports 7, 11452.
| Crossref | Google Scholar | PubMed |

Merrifield RC, Stephan C, Lead JR (2018) Quantification of Au nanoparticle biouptake and distribution to freshwater algae using single cell-ICP-MS. Environmental Science & Technology 52, 2271-2277.
| Crossref | Google Scholar | PubMed |

Mitrano DM, Beltzung A, Frehland S, Schmiedgruber M, Cingolani A, Schmidt F (2019) Synthesis of metal-doped nanoplastics and their utility to investigate fate and behaviour in complex environmental systems. Nature Nanotechnology 14, 362-368.
| Crossref | Google Scholar | PubMed |

Murray A, Örmeci B (2020) Removal effectiveness of nanoplastics (<400 nm) with separation processes used for water and wastewater treatment. Water 12, 635.
| Crossref | Google Scholar |

Pace HE, Rogers NJ, Jarolimek C, Coleman VA, Higgins CP, Ranville JF (2011) Determining transport efficiency for the purpose of counting and sizing nanoparticles via single particle inductively coupled plasma mass spectrometry. Analytical Chemistry 83, 9361-9369.
| Crossref | Google Scholar | PubMed |

Reed RB, Higgins CP, Westerhoff P, Tadjiki S, Ranville JF (2012) Overcoming challenges in analysis of polydisperse metal-containing nanoparticles by single particle inductively coupled plasma mass spectrometry. Journal of Analytical Atomic Spectrometry 27, 1093-1100.
| Crossref | Google Scholar |

Schmidt R, Nachtnebel M, Dienstleder M, Mertschnigg S, Schroettner H, Zankel A, Poteser M, Hutter H-P, Eppel W, Fitzek H (2021) Correlative SEM-Raman microscopy to reveal nanoplastics in complex environments. Micron 144, 103034.
| Crossref | Google Scholar | PubMed |

Tharaud M, Gondikas AP, Benedetti MF, von der Kammer F, Hofmann T, Cornelis G (2017) TiO₂ nanomaterial detection in calcium rich matrices by spICPMS. A matter of resolution and treatment. Journal of Analytical Atomic Spectrometry 32, 1400-1411.
| Crossref | Google Scholar |

Thiagarajan V, Alex SA, Seenivasan R, Chandrasekaran N, Mukherjee A (2021) Interactive effects of micro/nanoplastics and nanomaterials/pharmaceuticals: their ecotoxicological consequences in the aquatic systems. Aquatic Toxicology 232, 105747.
| Crossref | Google Scholar | PubMed |

Utermöhl H (1931) Neue Wege in der quantitativen Erfassung des Plankton. (Mit besonderer Berücksichtigung des Ultraplanktons.). SIL Proceedings, 1922-2010 5, 567-596 [In German].
| Crossref | Google Scholar |

von Moos N, Burkhardt-Holm P, Köhler A (2012) Uptake and effects of microplastics on cells and tissue of the blue mussel Mytilus edulis L. after an experimental exposure. Environmental Science & Technology 46, 11327-11335.
| Crossref | Google Scholar | PubMed |

Wang Q, Wang J, Chen H, Zhang Y (2022) Toxicity effects of microplastics and nanoplastics with cadmium on the alga Microcystis aeruginosa. Environmental Science and Pollution Research 30, 17360-17373.
| Crossref | Google Scholar | PubMed |

Wang Q, Liu WT, Zeb A, Lian YH, Shi RY, Li JT, Zheng ZQ (2023) Toxicity effects of polystyrene nanoplastics and arsenite on Microcystis aeruginosa. Science of the Total Environment 874, 162496.
| Crossref | Google Scholar |

Worm B, Lotze HK, Jubinville I, Wilcox C, Jambeck J (2017) Plastic as a persistent marine pollutant. Annual Review of Environment and Resources 42, 1-26.
| Crossref | Google Scholar |

Wu Y, Guo P, Zhang X, Zhang Y, Xie S, Deng J (2019) Effect of microplastics exposure on the photosynthesis system of freshwater algae. Journal of Hazardous Materials 374, 219-227.
| Crossref | Google Scholar | PubMed |

Yee MS-L, Hii L-W, Looi CK, Lim W-M, Wong S-F, Kok Y-Y, Tan B-K, Wong C-Y, Leong C-O (2021) Impact of microplastics and nanoplastics on human health. Nanomaterials 11, 496.
| Crossref | Google Scholar | PubMed |

Zhao Y, Tao S, Liu S, Hu T, Zheng K, Shen M, Meng G (2023) Research advances on impacts micro/nanoplastics and their carried pollutants on algae in aquatic ecosystems: a review. Aquatic Toxicology 264, 106725.
| Crossref | Google Scholar | PubMed |

Zhou XX, Liu R, Hao LT, Liu JF (2021) Identification of polystyrene nanoplastics using surface enhanced Raman spectroscopy. Talanta 221, 121552.
| Crossref | Google Scholar | PubMed |