Search

Menu
Search
in Ecology

Response to multigenerational graphene oxide exposure in acheta domesticus strains selected for longevity

87 Views


Abstract

The development of new nanotechnologies and their use in everyday life always carries the risk of environmental hazards and consequences for human health. Among them, graphene oxide (GO) is a promising material. Due to its excellent physicochemical properties, GO is attractive not only for industrial applications but also in medicine. There is still a lack of sufficient reports on the long-term effects of GO on organisms, including studies of a multigenerational nature. We investigated the health status of two strains of Acheta domesticus: the wild type and the long-lived. The strains were exposed to GO for five generations and a sixth recovery generation. We investigated parameters that may indirectly explain the mechanisms involved in transmitting the informational pattern of the stress response to subsequent generations: DNA stability, mitochondrial potential, apoptosis, and autophagy. GO intoxication induced multilevel cellular responses in five subsequent generations. GO cessation in recovery F5 acted as a new stressor. Across five generations, variation in the response to GO was observed. GO is most likely responsible for changes that persist over generations. We believe that epigenetic inheritance is a likely mechanism underlying the multigenerational adaptation observed in GO-exposed insects, and future research should aim to elucidate this phenomenon in more detail.

Data availability

Raw data are provided on the RepOD database (accession: https://doi.org/10.18150/F3YO29).

References

  1. Ma, Y., Zheng, Y. & Zhu, Y. Towards industrialization of graphene oxide. Science China Materials. 63 1861–1869 Preprint at https://doi.org/10.1007/s40843-019-9462-9 (2020).

  2. Nishina, Y. Mass production of graphene oxide beyond the laboratory: bridging the gap between academic research and industry. ACS Nano Preprint at https://doi.org/10.1021/acsnano.4c13297 (2024).

  3. Tiwari, S. K., Mishra, R. K., Ha, S. K. & Huczko, A. Evolution of graphene oxide and graphene: from imagination to industrialization. ChemNanoMat vol. 4 598–620 Preprint at https://doi.org/10.1002/cnma.201800089 (2018).

  4. Rhazouani, A. et al. Synthesis and toxicity of graphene oxide nanoparticles: a literature review of in vitro and in vivo studies. Biomed Res Int (2021). (2021).

  5. Seabra, A. B., Paula, A. J., De Lima, R. & Alves, O. L. Durán, N. Nanotoxicity of graphene and graphene oxide. Chem. Res. Toxicol. 27, 159–168 (2014).

    Google Scholar 

  6. Wang, K. et al. Biocompatibility of graphene oxide. Nanoscale Res. Lett. 6, 1–8 (2011).

    Google Scholar 

  7. Dziewięcka, M., Karpeta-Kaczmarek, J., Augustyniak, M., Majchrzycki, Ł. & Augustyniak-Jabłokow, M. A. Evaluation of in vivo graphene oxide toxicity for acheta domesticus in relation to nanomaterial purity and time passed from the exposure. J. Hazard. Mater. 305, 30–40 (2016).

    Google Scholar 

  8. Dziewięcka, M., Karpeta-Kaczmarek, J., Augustyniak, M. & Rost-Roszkowska, M. Short-term in vivo exposure to graphene oxide can cause damage to the gut and testis. J. Hazard. Mater. 328, 80–89 (2017).

    Google Scholar 

  9. Flasz, B. et al. Age-and lifespan-dependent differences in GO caused DNA damage in acheta domesticus. Int. J. Mol. Sci 290 (2022). (2023).

  10. Siqueira, P. R. et al. Concentration- and time-dependence toxicity of graphene oxide (GO) and reduced graphene oxide (rGO) nanosheets upon zebrafish liver cell line. Aquat. Toxicol. 248, 106199 (2022).

    Google Scholar 

  11. Jin, L. et al. Sublethal toxicity of graphene oxide in caenorhabditis elegans under multi-generational exposure. Ecotoxicol. Environ. Saf. 229, 113064 (2022).

    Google Scholar 

  12. Liu, Y., Fan, W., Xu, Z., Peng, W. & Luo, S. Transgenerational effects of reduced graphene oxide modified by Au, Ag, Pd, Fe3O4, Co3O4 and SnO2 on two generations of daphnia magna. Carbon N Y. 122, 669–679 (2017).

    Google Scholar 

  13. Krishnakumar, S., Malavika, R. N., Nair, S. V., Menon, D. & Paul-Prasanth, B. Nano-graphene oxide particles induce inheritable anomalies through altered gene expressions involved in oocyte maturation. Nanotoxicology 18, 160–180 (2024).

    Google Scholar 

  14. Klibaner-Schiff, E. et al. Environmental exposures influence multigenerational epigenetic transmission. Clinical Epigenetics vol. 16 Preprint at (2024). https://doi.org/10.1186/s13148-024-01762-3

  15. Berger, S. L. The complex Language of chromatin regulation during transcription. Nature 447, 407–412 (2007).

    Google Scholar 

  16. Sen, P., Shah, P. P., Nativio, R. & Berger, S. L. Epigenetic mechanisms of longevity and aging. Cell vol. 166 822–839 Preprint at (2016). https://doi.org/10.1016/j.cell.2016.07.050

  17. Flasz, B. et al. Multigenerational effects of graphene oxide nanoparticles on acheta domesticus DNA stability. Int J. Mol. Sci 24, 23, 1826 (2023). https://doi.org/10.3390/ ijms241612826

  18. Babczyńska, A. et al. Adult young as the fragile ontogenetic stage of the house crickets dietary exposed to GO nanoparticles – digestive enzymes perspective. Chemosphere 367, 143641 (2024). https://doi.org/10.1016/j.chemosphere.2024.143641

  19. Dziewięcka, M. et al. Graphene oxide as a new anthropogenic stress factor – multigenerational study at the molecular, cellular, individual and population level of acheta domesticus. J. Hazard. Mater. 396, 122775 (2020).

    Google Scholar 

  20. Flasz, B., Dziewięcka, M., Kędziorski, A., Tarnawska, M. & Augustyniak, M. Vitellogenin expression, DNA damage, health status of cells and catalase activity in acheta domesticus selected according to their longevity after graphene oxide treatment. Science Total Environment 737, 140274 (2020). https://doi.org/10.1016/j.scitotenv.2020.140274

  21. Dziewięcka, M. et al. The structure–properties–cytotoxicity interplay: A crucial pathway to determining graphene oxide biocompatibility. Int J. Mol. Sci 22, 5401 (2021). https://doi.org/10.3390/ijms22105401

  22. Horch, H. W., Mito, T., Popadi, A., Ohuchi, H. & Noji, S. The cricket as a model organism. Cricket. As Model. Organism. https://doi.org/10.1007/978-4-431-56478-2 (2017).

    Google Scholar 

  23. Flasz, B. et al. Multigenerational selection towards longevity changes the protective role of vitamin C against graphene oxide-induced oxidative stress in house crickets. Environmental Pollution 290, 117996 (2021). https://doi.org/10.1016/j.envpol.2021.117996

  24. Flasz, B. et al. Ascorbic acid and graphene oxide exposure in the model organism acheta domesticus can change the reproduction potential. Molecules 29, 4594 (2024). https://doi.org/10.3390/molecules29194594

  25. Dziewięcka, M. et al. Reduced fecundity and cellular changes in acheta domesticus after multigenerational exposure to graphene oxide nanoparticles in food. Sci. Total Environ. 635, 947–955 (2018).

    Google Scholar 

  26. Domenech, J., Rodríguez-Garraus, A., de Cerain, A. L., Azqueta, A. & Catalán, J. Genotoxicity of Graphene-Based Materials. Nanomaterials vol. 12 Preprint at (2022). https://doi.org/10.3390/nano12111795

  27. Szmidt, M. et al. Toxicity of different forms of graphene in a chicken embryo model. Environ. Sci. Pollut. Res. 23, 19940–19948 (2016).

    Google Scholar 

  28. Flasz, B. et al. Graphene oxide in low concentrations can change mitochondrial potential, autophagy, and apoptosis paths in two strains of invertebrates with different life strategies. Biochem Biophys. Res. Commun 736, 150898 (2024). https://doi.org/10.1016/j.bbrc.2024.150898

  29. Mukhopadhyay, S. et al. Autophagy and apoptosis: where do they meet? Apoptosis 555-566 https://doi.org/10.1007/s10495-014-0967-2 (2014).

  30. Shiloh, Y. & Ziv, Y. The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat. Rev. Mol. Cell. Biol. 14, 197–210 (2013).

    Google Scholar 

  31. Babczyńska, A. et al. Effects on digestive enzyme activities in the house crickets acheta domesticus exposed to graphene oxide in food for several generations. Nanotoxicology https://doi.org/10.1080/17435390.2025.2500430 (2025). 

  32. Fitz-James, M. H. & Cavalli, G. Molecular mechanisms of transgenerational epigenetic inheritance. Nat. Rev. Genet. 23, 325–341 (2022).

    Google Scholar 

  33. Aldal’In, H. K. et al. A review on the epigenetics modifications to nanomaterials in humans and animals: novel epigenetic regulator. Annals Anim. Sci. 23, 615–628 (2023).

    Google Scholar 

  34. Choudhury, S. R. et al. From the cover: zinc oxide Nanoparticles-Induced reactive oxygen species promotes multimodal Cyto- and epigenetic toxicity. Toxicol. Sci. 156, 261–274 (2017).

    Google Scholar 

  35. Pogribna, M. et al. Effect of titanium dioxide nanoparticles on DNA methylation in multiple human cell lines. Nanotoxicology 14, 534–553 (2020).

    Google Scholar 

  36. Patil, N. A., WN, G., Deobagkar, D. D. & and Epigenetic modulation upon exposure of lung fibroblasts to TiO2 and ZnO nanoparticles: alterations in DNA methylation. Int. J. Nanomed. 11, 4509–4519 (2016).

    Google Scholar 

  37. Gong, C. et al. SiO2 nanoparticles induce global genomic hypomethylation in HaCaT cells. Biochem. Biophys. Res. Commun. 397, 397–400 (2010).

    Google Scholar 

  38. Ghazimoradi, M. M. et al. Epigenetic effects of graphene oxide and its derivatives: A mini-review. Mutation Research – Genetic Toxicology and Environmental Mutagenesis vol. 878 Preprint at (2022). https://doi.org/10.1016/j.mrgentox.2022.503483

  39. Li, Y. et al. Creating a pro-survival phenotype through epigenetic modulation. Surgery 152, 455–464 (2012).

    Google Scholar 

  40. Vaquero, A. Sirtuin-dependent epigenetic regulation in the maintenance of genome integrity. The FEBS Journal 282, 1745–1767 (2015).

  41. Hoffmann, A. A. & Hercus, M. J. Environmental stress as an evolutionary force. Bioscience 50, 217–226 (2000).

    Google Scholar 

  42. Chen, M., Qin, X. & Zeng, G. Biodegradation of carbon Nanotubes, Graphene, and their derivatives. Trends Biotechnol. 35, 836–846 (2017).

    Google Scholar 

  43. Qu, Y. et al. A novel environmental fate of graphene oxide: biodegradation by a bacterium labrys sp. WJW to support growth. Water Res. 143, 260–269 (2018).

    Google Scholar 

  44. Jemielity, S., Chapuisat, M., Parker, J. D. & Keller, L. Long live the queen: studying aging in social insects. Age (Omaha). 27, 241–248 (2005).

    Google Scholar 

  45. Weale, R. A. Biorepair mechanisms and longevity. Journals Gerontology: Ser. A. 59, B449–B454 (2004).

    Google Scholar 

  46. Promislow, D. E. L. DNA repair and the evolution of longevity: A critical analysis. J. Theor. Biol. 170, 291–300 (1994).

    Google Scholar 

  47. Hyun, M. et al. Longevity and resistance to stress correlate with DNA repair capacity in caenorhabditis elegans. Nucleic Acids Res. 36, 1380–1389 (2008).

    Google Scholar 

Download references

Funding

This research was funded by the National Science Centre (NCN) in Poland, based on Agreement No. UMO-2020/37/B/NZ7/00570. The publication was co-financed by the funds granted under the Research Excellence Initiative of the University of Silesia in Katowice.

Author information

Authors and Affiliations

  1. Institute of Biology, Biotechnology and Environmental Protection, University of Silesia in Katowice, Katowice, Poland

    Barbara Flasz, Agnieszka Babczyńska, Monika Tarnawska, Andrzej Kędziorski, Ewa Świerczek, Katarzyna Rozpędek & Maria Augustyniak

  2. Department of Medicine, Division of Renal Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, 02115, USA

    Amrendra K. Ajay

  3. Polish Academy of Sciences, Institute of Ichthyobiology and Aquaculture in Gołysz, Chybie, 43–520, Poland

    Łukasz Napora-Rutkowski

Authors

  1. Barbara Flasz
    View author publications

    Search author on:PubMed Google Scholar

  2. Agnieszka Babczyńska
    View author publications

    Search author on:PubMed Google Scholar

  3. Monika Tarnawska
    View author publications

    Search author on:PubMed Google Scholar

  4. Amrendra K. Ajay
    View author publications

    Search author on:PubMed Google Scholar

  5. Andrzej Kędziorski
    View author publications

    Search author on:PubMed Google Scholar

  6. Łukasz Napora-Rutkowski
    View author publications

    Search author on:PubMed Google Scholar

  7. Ewa Świerczek
    View author publications

    Search author on:PubMed Google Scholar

  8. Katarzyna Rozpędek
    View author publications

    Search author on:PubMed Google Scholar

  9. Maria Augustyniak
    View author publications

    Search author on:PubMed Google Scholar

Contributions

Conceptualization, M.A.; methodology, A.B.; software, Ł.N-R.; validation, B.F., M.A.; formal analysis, B.F.; investigation, A.B., M.T.; resources, A.K., E.Ś., and K.R.; data curation, B.F.; writing—original draft preparation, B.F.; writing—review and editing, M.A., B.F., and A.K.A.; visualization, B.F.; supervision, M.A.; project administration, M.A.; funding acquisition, M.A. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to
Barbara Flasz.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary Material 1

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and permissions

About this article

Cite this article

Flasz, B., Babczyńska, A., Tarnawska, M. et al. Response to multigenerational graphene oxide exposure in acheta domesticus strains selected for longevity.
Sci Rep (2026). https://doi.org/10.1038/s41598-026-37623-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41598-026-37623-7

Keywords

  • Graphene oxide
  • DNA damage
  • Mitochondrial potential
  • Apoptosis
  • Multigenerational effects
  • Epigenetics

Source: Ecology - nature.com

Trace metal pollution and ecological effects on five crops around a typical manganese mining area in Chongqing, China

Analysis of river water quality in Rourkela Odisha using multiple indices to inform sustainable water management

This portal is not a newspaper as it is updated without periodicity. It cannot be considered an editorial product pursuant to law n. 62 of 7.03.2001. The author of the portal is not responsible for the content of comments to posts, the content of the linked sites. Some texts or images included in this portal are taken from the internet and, therefore, considered to be in the public domain; if their publication is violated, the copyright will be promptly communicated via e-mail. They will be immediately removed.

Back to Top
Close