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Life cycle exposure to titanium dioxide nanoparticles (TiO2-NPs) induces filial toxicity and population decline in the nematode Caenorhabditis elegans

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Abstract

Titanium dioxide nanoparticle (TiO2-NP) exposure has raised significant concern due to their potential toxicity and adverse ecological impacts. Despite their ubiquitous presence in various environmental compartments, the long-term consequences of TiO2-NPs remain poorly understood. In this study, we combined data of in vivo toxicity and modeling to investigate the potential negative impacts of TiO2-NP exposure. We employed the nematode Caenorhabditis elegans, an environmental organism, to conduct a full life cycle TiO2-NP toxicity assays. Moreover, to assess the potential impact of TiO2-NP toxicity on population dynamics, we applied a stage-constructed matrix population model (MPM). Results showed that TiO2-NPs caused significant reductions in reproduction, survival, and growth of parental C. elegans (P0) at the examined concentrations. Moreover, these toxic effects were even more pronounced in the subsequent generation (F1) when exposed to TiO2-NPs. Furthermore, parental TiO2-NP exposure resulted in significant toxicity in non-exposed C. elegans progeny (TiO2-NPs free), adversely affecting their reproduction, survival, and growth. MPM analysis revealed decreased transition probabilities of surviving (Pi), growth (Gi), and fertility (Fi) in scenarios with TiO2-NP exposure. Additionally, the population growth rate (λmax) was found to be less than 1 in both P0 and F1, indicating a declining population trend after successive generations. Sensitivity analysis pinpointed L1 larvae as the most vulnerable stage, significantly contributing to the observed population decline in both P0 and F1 generations under TiO2-NP exposure. Our findings provide insight into the potential risk of an environmental organism like nematode by life cycle exposure to TiO2-NPs.

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Data availability

All data supporting the findings of this study are available within the paper and its Supplementary Information, and are available from the corresponding author upon reasonable request.

References

  • Abbas Q, Yousaf B, Ali MU, Munir MAM, El-Naggar A, Rinklebe J, Naushad M (2020) Transformation pathways and fate of engineered nanoparticles (ENPs) in distinct interactive environmental compartments: a review. Environ Int 138:105646

    Article  CAS  Google Scholar 

  • Álvarez OA, Jager T, Kooijman S, Kammenga J (2005) Responses to stress of Caenorhabditis elegans populations with different reproductive strategies. Funct Ecol 19:656–664

    Article  Google Scholar 

  • Bäuerlein PS, Emke E, Tromp P, Hofman JAMH, Carboni A, Schooneman F, de Voogt P, van Wezel AP (2017) Is there evidence for man-made nanoparticles in the Dutch environment? Sci Total Environ 576:273–283

    Article  Google Scholar 

  • Caswell H (1997) Matrix methods for population analysis. Structured-population models in marine, terrestrial, and freshwater systems, 19–58

  • Caswell H (2001) Matrix population models: construction, analysis, and interpretation, 1. Sinauer Associates, Sunderland, MA, USA

    Google Scholar 

  • Ellis L-JA, Kissane S, Hoffman E, Valsami-Jones E, Brown JB, Colbourne JK, Lynch I (2021) Multigenerational exposure to nano-TiO2 induces ageing as a stress response mitigated by environmental interactions. Adv Nanobiomed Res 1:2000083

    Article  CAS  Google Scholar 

  • Galhano V, Zeumer R, Monteiro MS, Knopf B, Meisterjahn B, Soares AMVM, Loureiro S, Schlechtriem C, Lopes I (2022) Effects of wastewater-spiked nanoparticles of silver and titanium dioxide on survival, growth, reproduction and biochemical markers of Daphnia magna. Sci Total Environ 839:156079

    Article  CAS  Google Scholar 

  • Hu C, Hou J, Zhu Y, Lin D (2020) Multigenerational exposure to TiO2 nanoparticles in soil stimulates stress resistance and longevity of survived C. elegans via activating insulin/IGF-like signaling. Environ Pollut 263:114376

    Article  CAS  Google Scholar 

  • Huang C-W, Yen P-L, Kuo Y-H, Chang C-H, Liao VH-C (2022) Nanoplastic exposure in soil compromises the energy budget of the soil nematode C. elegans and decreases reproductive fitness. Environ Pollut 312:120071

    Article  CAS  Google Scholar 

  • Li WH, Ju YR, Liao CM, Liao VH (2014) Assessment of selenium toxicity on the life cycle of Caenorhabditis elegans. Ecotoxicology 23:1245–1253

    Article  CAS  Google Scholar 

  • Li Z, Wang X, Ma B, Wang S, Zheng D, She Z, Guo L, Zhao Y, Xu Q, Jin C, Li S, Gao M (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 H, Zeng L, Wang C, Shi C, Li Y, Peng Y, Chen H, Zhang J, Cheng B, Chen C, Xiang M, Huang Y (2022) Review of the toxicity and potential molecular mechanisms of parental or successive exposure to environmental pollutants in the model organism Caenorhabditis elegans. Environ Pollut 311:119927

    Article  CAS  Google Scholar 

  • Li K, Xu D, Liao H, Xue Y, Sun M, Su H, Xiu X, Zhao T (2022) A review on the generation, discharge, distribution, environmental behavior, and toxicity (especially to microbial aggregates) of nano-TiO2 in sewage and surface-water and related research prospects. Sci Total Environ 824:153866

    Article  CAS  Google Scholar 

  • Liu S, Zeng P, Li X, Thuyet DQ, Fan W (2019) Effect of chronic toxicity of the crystalline forms of TiO2 nanoparticles on the physiological parameters of Daphnia magna with a focus on index correlation analysis. Ecotoxicol Environ Saf 181:292–300

    Article  CAS  Google Scholar 

  • Lundström Belleza E, Brinkmann M, Preuss TG, Breitholtz M (2014) Population-level effects in Amphiascus tenuiremis: contrasting matrix- and individual-based population models. Aquat Toxicol 157:207–214

    Article  Google Scholar 

  • Luo X, Xu S, Yang Y, Zhang Y, Wang S, Chen S, XuWu A (2017) A novel method for assessing the toxicity of silver nanoparticles in Caenorhabditis elegans. Chemosphere 168:648–657

    Article  CAS  Google Scholar 

  • Luo Z, Li Z, Xie Z, Sokolova IM, Song L, Peijnenburg W, Hu M, Wang Y (2020) Rethinking nano-TiO2 safety: overview of toxic effects in humans and aquatic animals. Small 16:e2002019

    Article  Google Scholar 

  • Nederstigt TAP, Peijnenburg WJGM, Blom R, Vijver MG (2022) Correlation analysis of single- and multigenerational endpoints in Daphnia magna toxicity tests: a case-study using TiO2 nanoparticles. Ecotoxicol Environ Saf 241:113792

    Article  CAS  Google Scholar 

  • Savić-Zdravković D, Jovanović B, Đurđević A, Stojković-Piperac M, Savić A, Vidmar J, Milošević D (2018) An environmentally relevant concentration of titanium dioxide (TiO2) nanoparticles induces morphological changes in the mouthparts of Chironomus tentans. Chemosphere 211:489–499

    Article  Google Scholar 

  • Sengul AB, Asmatulu E (2020) Toxicity of metal and metal oxide nanoparticles: a review. Environ Chem Lett 18:1659–1683

    Article  CAS  Google Scholar 

  • Shang Y, Wu F, Wei S, Guo W, Chen J, Huang W, Hu M, Wang Y (2020) Specific dynamic action of mussels exposed to TiO2 nanoparticles and seawater acidification. Chemosphere 241:125104

    Article  CAS  Google Scholar 

  • Shimizu M, Tainaka H, Oba T, Mizuo K, Umezawa M, Takeda K (2009) Parental exposure to nanoparticulate titanium dioxide during the prenatal period alters gene expression related to brain development in the mouse. Part Fibre Toxicol 6

  • Slomberg DL, Auffan M, Guéniche N, Angeletti B, Campos A, Borschneck D, Aguerre-Chariol O, Rose J (2020) Anthropogenic release and distribution of titanium dioxide particles in a river downstream of a nanomaterial manufacturer industrial site. Front Environ Sci 8

  • Sun TY, Gottschalk F, Hungerbuhler K, Nowack B (2014) Comprehensive probabilistic modelling of environmental emissions of engineered nanomaterials. Environ Pollut 185:69–76

    Article  CAS  Google Scholar 

  • Sun TY, Bornhoft NA, Hungerbuhler K, Nowack B (2016) Dynamic probabilistic modeling of environmental emissions of engineered nanomaterials. Environ Sci Technol 50:4701–4711

    Article  CAS  Google Scholar 

  • Takeda K, Suzuki KI, Ishihara A, Kubo-Irie M, Fujimoto R, Tabata M, Oshio S, Nihei Y, Ihara T, Sugamata M (2009) Nanoparticles transferred from pregnant mice to their offspring can damage the genital and cranial nerve systems. J Health Sci 55:95–102

    Article  CAS  Google Scholar 

  • Turan NB, Erkan HS, Engin GO, Bilgili MS (2019) Nanoparticles in the aquatic environment: usage, properties, transformation and toxicity—a review. Process Saf Environ Prot 130:238–249

    Article  CAS  Google Scholar 

  • Vidmar J, Zuliani T, Milačič R, Ščančar J (2022) Following the occurrence and origin of titanium dioxide nanoparticles in the Sava river by single particle ICP-MS. Water 14:959

    Article  CAS  Google Scholar 

  • Wang H, Wick RL, Xing B (2009) Toxicity of nanoparticulate and bulk ZnO, Al2O3 and TiO2 to the nematode Caenorhabditis elegans. Environ Pollut 157:1171–1177

    Article  CAS  Google Scholar 

  • Wu C-Y, Tu K-J, Lo Y-S, Pang YL, Wu C-H (2016) Alkaline hydrogen peroxide treatment for TiO2 nanoparticles with superior water-dispersibility and visible-light photocatalytic activity. Mater Chem Phys 181:82–89

    Article  CAS  Google Scholar 

  • Wu Y, Chen L, Chen F, Zou H, Wang Z (2020) A key moment for TiO2: prenatal exposure to TiO2 nanoparticles may inhibit the development of offspring. Ecotoxicol Environ Saf 202:110911

    Article  CAS  Google Scholar 

  • Xing X, Rui Q, Wang D (2009) Lethality toxicities induced by metal exposure during development in nematode Caenorhabditis elegans. Bull Environ Contam Toxicol 83:530–536

    Article  CAS  Google Scholar 

  • Yang Y, Xu S, Xu G, Liu R, Xu A, Chen S, Wu L (2019) Effects of ionic strength on physicochemical properties and toxicity of silver nanoparticles. Sci Total Environ 647:1088–1096

    Article  CAS  Google Scholar 

  • Yao Y, Zhang T, Tang M (2022) A critical review of advances in reproductive toxicity of common nanomaterials to Caenorhabditis elegans and influencing factors. Environ Pollut 306:119270

    Article  CAS  Google Scholar 

  • Yen K, Steinsaltz D, Mobbs CV (2008) Validated analysis of mortality rates demonstrates distinct genetic mechanisms that influence lifespan. Exp Gerontol 43:1044–1051

    Article  Google Scholar 

  • Zhao Y, Chen J, Wang R, Pu X, Wang D (2022) A review of transgenerational and multigenerational toxicology in the in vivo model animal Caenorhabditis elegans. J Appl Toxicol. https://doi.org/10.1002/jat.4360

    Article  Google Scholar 

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Funding

This work was financially supported in part by grants from the National Science and Technology Council of Taiwan (MOST 111–2313-B-002 -052 -MY3 and MOST 111–2320-B-002 -030 -MY3) and from NTU Core Consortiums (Ecotoxicity of long-term exposure to emerging pharmaceutical contaminant in C. elegans, NTU-CC-111L894702) to Professor Vivian H.-C. Liao.

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Author notes

  1. Hsin Yen and Chi-Wei Huang contributed equally to this work.

Authors and Affiliations

  1. Department of Bioenvironmental Systems Engineering, National Taiwan University, No. 1, Sec. 4, Roosevelt Rd., Taipei, 106, Taiwan

    Hsin Yen & Vivian Hsiu-Chuan Liao

  2. Department of Marine Environmental Engineering, National Kaohsiung University of Science and Technology, Kaohsiung, 811, Taiwan

    Chi-Wei Huang

  3. Department of Biomedical Engineering and Environmental Sciences, National Tsing Hua University, 101, Section 2, Kuang-Fu Road, Hsinchu, 300, Taiwan

    Chien-Hou Wu

Authors
  1. Hsin Yen
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  2. Chi-Wei Huang
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  4. Vivian Hsiu-Chuan Liao
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Contributions

Hsin Yen: methodology, investigation, visualization, and writing—original draft. Chi-Wei Huang: methodology, visualization, and writing—original draft. Chien-Hou Wu: providing TiO2-NPs. Vivian H.-C. Liao: conceptualization, resources, writing—review and editing, supervision, and funding acquisition.

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Correspondence to Vivian Hsiu-Chuan Liao.

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Yen, H., Huang, CW., Wu, CH. et al. Life cycle exposure to titanium dioxide nanoparticles (TiO2-NPs) induces filial toxicity and population decline in the nematode Caenorhabditis elegans. Environ Sci Pollut Res (2024). https://doi.org/10.1007/s11356-024-33159-3

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