Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Microplastic fragmentation by rotifers in aquatic ecosystems contributes to global nanoplastic pollution

Nature Nanotechnology volume 19, pages 406–414 (2024)Cite this article

Subjects

Abstract

The role of aquatic organisms in the biological fragmentation of microplastics and their contribution to global nanoplastic pollution are poorly understood. Here we present a biological fragmentation pathway that generates nanoplastics during the ingestion of microplastics by rotifers, a commonly found and globally distributed surface water zooplankton relevant for nutrient recycling. Both marine and freshwater rotifers could rapidly grind polystyrene, polyethylene and photo-aged microplastics, thus releasing smaller particulates during ingestion. Nanoindentation studies of the trophi of the rotifer chitinous mastax revealed a Young’s modulus of 1.46 GPa, which was higher than the 0.79 GPa for polystyrene microparticles, suggesting a fragmentation mechanism through grinding the edges of microplastics. Marine and freshwater rotifers generated over 3.48 × 105 and 3.66 × 105 submicrometre particles per rotifer in a day, respectively, from photo-aged microplastics. Our data suggest the ubiquitous occurrence of microplastic fragmentation by different rotifer species in natural aquatic environments of both primary and secondary microplastics of various polymer compositions and provide previously unidentified insights into the fate of microplastics and the source of nanoplastics in global surface waters.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Ingestion of PS microplastics of different sizes by marine and freshwater rotifers as imaged and counted by optical microscopy.
Fig. 2: Fragmentation of PS microplastics by marine and freshwater rotifers as imaged by LSCM.
Fig. 3: Direct evidence for PS microplastic fragmentation in rotifers as examined by LCM-Raman, HSI and RISE.
Fig. 4: SEM images of the ingested PS microplastics and the trophi of marine rotifers after grinding, and their mechanical properties.
Fig. 5: Qualitative and quantitative analyses of PS fragments ground by rotifers after exposure to photo-aged PS microplastics.
Fig. 6: The fragmentation of different types of microplastic by rotifers and the global distribution of microplastics and rotifers.

Similar content being viewed by others

Data availability

The raw data that support the findings of this study are available at the publicly accessible online repository Figshare with the identifier https://doi.org/10.6084/m9.figshare.24125016. Source data are provided with this paper.

References

  1. Stubbins, A., Law, K. L., Muñoz, S. E., Bianchi, T. S. & Zhu, L. Plastics in the earth system. Science 373, 51–55 (2021).

    Article  ADS  CAS  PubMed  Google Scholar 

  2. Ross, P. S. et al. Pervasive distribution of polyester fibres in the Arctic Ocean is driven by Atlantic inputs. Nat. Commun. 12, 106 (2021).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  3. Aves, A. R. et al. First evidence of microplastics in Antarctic snow. Cryosphere 16, 2127–2145 (2022).

    Article  ADS  Google Scholar 

  4. Woodward, J., Li, J., Rothwell, J. & Hurley, R. Acute riverine microplastic contamination due to avoidable releases of untreated wastewater. Nat. Sustain. 4, 793–802 (2021).

    Article  Google Scholar 

  5. Peng, X. et al. Microplastics contaminate the deepest part of the world’s ocean. Geochem. Perspect. Lett. 9, 1–5 (2018).

    Google Scholar 

  6. Santos, R. G., Machovsky-Capuska, G. E. & Andrades, R. Plastic ingestion as an evolutionary trap: toward a holistic understanding. Science 373, 56–60 (2021).

    Article  ADS  CAS  PubMed  Google Scholar 

  7. MacLeod, M., Arp, H. P. H., Tekman, M. B. & Jahnke, A. The global threat from plastic pollution. Science 373, 61–65 (2021).

    Article  ADS  CAS  PubMed  Google Scholar 

  8. Gigault, J. et al. Nanoplastics are neither microplastics nor engineered nanoparticles. Nat. Nanotechnol. 16, 501–507 (2021).

    Article  ADS  CAS  PubMed  Google Scholar 

  9. Vethaak, A. D. & Legler, J. Microplastics and human health. Science 371, 672–674 (2021).

    Article  ADS  CAS  PubMed  Google Scholar 

  10. Wagner, S. & Reemtsma, T. Things we know and don’t know about nanoplastic in the environment. Nat. Nanotechnol. 14, 300–301 (2019).

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Gerritse, J., Leslie, H. A., Caroline, A., Devriese, L. I. & Vethaak, A. D. Fragmentation of plastic objects in a laboratory seawater microcosm. Sci. Rep. 10, 10945 (2020).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  12. Dawson, A. L. et al. Turning microplastics into nanoplastics through digestive fragmentation by Antarctic krill. Nat. Commun. 9, 1001 (2018).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  13. Wang, C., Zhao, J. & Xing, B. Environmental source, fate, and toxicity of microplastics. J. Hazard. Mater. 407, 124357 (2021).

    Article  CAS  PubMed  Google Scholar 

  14. Hewitt, D. P. & George, D. G. The population dynamics of Keratella cochlearis in a hypereutrophic tarn and the possible impact of predation by young roach. Hydrobiologia 147, 221–227 (1987).

    Article  Google Scholar 

  15. Jeong, C. B. et al. Microplastic size-dependent toxicity, oxidative stress induction, and p-JNK and p-p38 activation in the monogonont rotifer (Brachionus koreanus). Environ. Sci. Technol. 50, 8849–8857 (2016).

    Article  ADS  CAS  PubMed  Google Scholar 

  16. Baer, A., Langdon, C., Mills, S., Schulz, C. & Hamre, K. Particle size preference, gut filling and evacuation rates of the rotifer Brachionus “Cayman” using polystyrene latex beads. Aquaculture 282, 75–82 (2008).

    Article  Google Scholar 

  17. Stelzer, C. P., Riss, S. & Stadler, P. Genome size evolution at the speciation level: the cryptic species complex Brachionus plicatilis (Rotifera). BMC Evol. Biol. 11, 90 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Papakostas, S. et al. Integrative taxonomy recognizes evolutionary units despite widespread mitonuclear discordance: evidence from a rotifer cryptic species complex. Syst. Biol. 65, 508–524 (2016).

    Article  PubMed  Google Scholar 

  19. Gilbert, J. J. & Walsh, E. J. Brachionus calyciflorus is a species complex: mating behavior and genetic differentiation among four geographically isolated strains. Hydrobiologia 546, 257–265 (2005).

    Article  CAS  Google Scholar 

  20. Drago, C. & Weithoff, G. Variable fitness response of two rotifer species exposed to microplastics particles: the role of food quantity and quality. Toxics 9, 305 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Fournier, S. B. et al. Nanopolystyrene translocation and fetal deposition after acute lung exposure during late-stage pregnancy. Part. Fibre Toxicol. 17, 55 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Kleinow, W. & Wratil, H. On the structure and function of the mastax of Brachionus plicatilis (Rotifera), a scanning electron microscope analysis. Zoomorphology 116, 169–177 (1996).

    Article  Google Scholar 

  23. Klusemann, J., Kleinow, W. & Peters, W. The hard parts (trophi) of the rotifer mastax do contain chitin: evidence from studies on Brachionus plicatilis. Histochemistry 94, 277–283 (1990).

    Article  CAS  PubMed  Google Scholar 

  24. Cornillac, A., Wurdak, E. & Clément, P. Biology of Rotifers (Springer, 1983).

  25. Garvey, C. J. et al. Molecular-scale understanding of the embrittlement in polyethylene ocean debris. Environ. Sci. Technol. 54, 11173–11181 (2020).

    Article  ADS  CAS  PubMed  Google Scholar 

  26. Liu, Z. et al. Quantifying the dynamics of polystyrene microplastics UV-aging process. Environ. Sci. Technol. Lett. 9, 50–56 (2022).

    Article  Google Scholar 

  27. Huang, Z. et al. Influence of protein configuration on aggregation kinetics of nanoplastics in aquatic environment. Water Res. 219, 118522 (2022).

    Article  CAS  PubMed  Google Scholar 

  28. Iyer, N. & Rao, T. Responses of the predatory rotifer Asplanchna intermedia to prey species differing in vulnerability: laboratory and field studies. Freshw. Biol. 36, 521–533 (1996).

    Article  Google Scholar 

  29. Yuan, W., Liu, X., Wang, W., Di, M. & Wang, J. Microplastic abundance, distribution and composition in water, sediments, and wild fish from Poyang Lake, China. Ecotoxicol. Environ. Saf. 170, 180–187 (2019).

    Article  CAS  PubMed  Google Scholar 

  30. Wang, J., Wu, J., Yu, Y., Wang, T. & Gong, C. The specific list, quantitative distribution and change of zooplankton in the season of spring and autumn in Poyang Lake. J. Lake Sci. 15, 345–352 (2003).

    Article  CAS  Google Scholar 

  31. Gilbert, J. J. Food niches of planktonic rotifers: diversification and implications. Limnol. Oceanogr. 67, 2218–2251 (2022).

    Article  ADS  Google Scholar 

  32. Han, M. et al. Distribution of microplastics in surface water of the lower Yellow River near estuary. Sci. Total Environ. 707, 135601 (2020).

    Article  ADS  CAS  PubMed  Google Scholar 

  33. Fan, Y. et al. Spatiotemporal dynamics of microplastics in an urban river network area. Water Res. 212, 118116 (2022).

    Article  CAS  PubMed  Google Scholar 

  34. Janakiraman, A., Naveed, M. S. & Altaff, K. Impact of domestic sewage pollution on rotifer abundance in Adyar estuary. Int. J. Environ. Sci. 3, 689–696 (2012).

    CAS  Google Scholar 

  35. Cai, H., Chen, M., Du, F., Matthews, S. & Shi, H. Separation and enrichment of nanoplastics in environmental water samples via ultracentrifugation. Water Res. 203, 117509 (2021).

    Article  CAS  PubMed  Google Scholar 

  36. Nigamatzyanova, L. & Fakhrullin, R. Dark-field hyperspectral microscopy for label-free microplastics and nanoplastics detection and identification in vivo: a Caenorhabditis elegans study. Environ. Pollut. 271, 116337 (2021).

    Article  CAS  PubMed  Google Scholar 

  37. Stojicic, S., Zivkovic, S., Qian, W., Zhang, H. & Haapasalo, M. Tissue dissolution by sodium hypochlorite: effect of concentration, temperature, agitation, and surfactant. J. Endod. 36, 1558–1562 (2010).

    Article  PubMed  Google Scholar 

  38. Chopinet, L., Formosa, C., Rols, M. P., Duval, R. E. & Dague, E. Imaging living cells surface and quantifying its properties at high resolution using AFM in QI™ mode. Micron 48, 26–33 (2013).

    Article  CAS  PubMed  Google Scholar 

  39. de Vega, R. G. et al. Characterisation of microplastics and unicellular algae in seawater by targeting carbon via single particle and single cell ICP-MS. Anal. Chim. Acta 1174, 338737 (2021).

    Article  Google Scholar 

  40. Podar, M. et al. Global prevalence and distribution of genes and microorganisms involved in mercury methylation. Sci. Adv. 1, e1500675 (2015).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (42192572, U2106213), Taishan Scholars Program of Shandong Province (tsqn201909051), Key Research and Development Program of Shandong Province (2020CXGC010703), Laoshan Laboratory (LSKJ202203901) and Fundamental Research Funds for the Central Universities (202172001, 202141003). We thank Z. Rao at the Chinese Academy of Sciences and J. Li at Zeiss for their assistance on HSI and RISE, respectively.

Author information

Authors and Affiliations

  1. Institute of Coastal Environmental Pollution Control, Key Laboratory of Marine Environment and Ecology (Ministry of Education), Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China, Qingdao, China

    Jian Zhao, Ruyi Lan, Wenli Su, Runze Xue, Zhuomiao Liu, Xia Liu, Yanhui Dai & Tongtao Yue

  2. Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China

    Jian Zhao

  3. Institute of Environmental Processes and Pollution Control, and School of Environmental and Civil Engineering, Jiangnan University, Wuxi, China

    Zhenyu Wang

  4. School of Materials Science and Engineering, Tianjin University, Tianjin, China

    Dongpo Song

  5. Stockbridge School of Agriculture, University of Massachusetts, Amherst, MA, USA

    Zhuomiao Liu & Baoshan Xing

Authors
  1. Jian Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ruyi Lan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhenyu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wenli Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dongpo Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Runze Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhuomiao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xia Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yanhui Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Tongtao Yue
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Baoshan Xing
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.Z. and B.X. conceptualized the idea and designed all the experiments, and J.Z. supervised the project. R.L., W.S., R.X. and J.Z. carried out the experiments. R.L., J.Z. and B.X wrote the manuscript. Z.W., D.S., X.L., T.Y., Z.L. and Y.D. supported the quantitative analysis of nanoplastics, and discussed and revised the manuscript. All authors reviewed and approved the manuscript.

Corresponding author

Correspondence to Baoshan Xing.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Nanotechnology thanks Chang-Bum Jeong, Guntram Weithoff, and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

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

Extended data

Extended Data Fig. 1 The quantitative results on the generation of nanoplastics from different microplastics by rotifers.

(A): The numbers of nanoplastics generated from PS fibers; (B): The numbers of nanoplastics generated from PS microplastics obtained from the food container. Data are presented as mean ± s.d. (n = 3 for all groups in Panel A and “PS debris in rotifers” group in Panel B; n = 4 for “original PS debris” group and “PS debris in medium” group in Panel B). Statistical analyses were performed using a one-sided ANOVA followed by LSD post hoc test.

Source data

Supplementary information

Supplementary Information

Supplementary Figs. 1–38, Videos 1–3 and Tables 1–3.

Supplementary Video 1

Uptake and grinding of PS microplastics by the rotifer.

Supplementary Video 2

Grinding of 10 μm PS microplastics by the rotifer 60 times before internalization.

Supplementary Video 3

Excretion of photo-aged PS microplastics and the fragments by the rotifer.

Supplementary Data 1

Source Data for Supplementary Figures.

Source data

Source Data Fig. 1

Statistical source data.

Source Data Fig. 3

Statistical source data.

Source Data Fig. 5

Statistical source data.

Source Data Extended Data Fig. 1

Statistical source data.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, J., Lan, R., Wang, Z. et al. Microplastic fragmentation by rotifers in aquatic ecosystems contributes to global nanoplastic pollution. Nat. Nanotechnol. 19, 406–414 (2024). https://doi.org/10.1038/s41565-023-01534-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41565-023-01534-9

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing