Microplastics and phagotrophic soil protists: evidence of ingestion
see video as supplementary material
Keywords:plastic pollution, soil ecotoxicology, global change, soil biota
Microplastics (MPs) can now be found in all the Earth’s biomes, thereby representing a global change phenomenon with largely unknown consequences for biodiversity and ecosystem functioning. Soil protists are eukaryotic, primarily single celled organisms that play important roles in the soil food web. Microplastics have been shown to affect protist populations in freshwater and marine environments. However, the interactions between soil protists and MPs remain largely unknown. Here we examined whether phagotrophic soil protists can ingest MPs and, if so, whether they experience declines in abundance. We exposed protists to soil treatments with different concentrations of MPs using commercial polymer fluorescent microspheres and used fluorescence microscopy to find evidence of MP ingestion. In addition, we quantified the total number of active phagotrophic protists over time. We show that most soil protists (> 75 % individuals) can readily ingest and keep MPs within their food vacuoles, even at relatively small MP concentrations (0.1 % w/w). There was a trend for higher prevalence of ingestion and for declines in protist abundance at the highest concentration of MPs (1 % w/w). However, more data are necessary to further ascertain cause-effect relationships. This is the first report indicating that soil protists can play an important role in the transport and uptake of MPs in the soil food web.
Adl, M. S. & V. V. S. R. Gupta (2006): Protists in soil ecology and forest nutrient cycling. – Canadian Journal of Forest Research. Journal Canadien de La Recherche Forestière 36 (7): 1805–1817 [https://doi.org/10.1139/x06-056].
Adl, S. M., A. G. B. Simpson, M. A. Farmer, R. A. Andersen, O. R. Anderson, J. R. Barta, S. S. Bowser, G. Brugerolle, R. A. Fensome, S. Fredericq, T. Y. James, S. Karpov, P. Kugrens, J. Krug, Lane, C. E., L. A. Lewis, J. Lodge, D. H. Lynn, D. G. Mann, & M. F. J. R. Taylor (2005): The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. – The Journal of Eukaryotic Microbiology 52(5): 399–451 [https://doi.org/10.1111/j.1550-7408.2005.00053.x].
Alongi, D. M. (2018): Extraction of protists in aquatic sediments via density gradient centrifugation. – In: P. Kemp, F., B. F. Sherr, E. B. Sherr, J. J. Cole (eds): Handbook of Methods in Aquatic Microbial Ecology. – CRC Press , Boca Raton: 109–114 [https://doi.org/10.1201/9780203752746-14].
Andrady, A. L. (2011): Microplastics in the marine environment. – Marine Pollution Bulletin 62(8): 1596–1605 [https://doi.org/10.1016/j.marpolbul.2011.05.030].
Azzarello, M. Y. & E. S. Van Vleet (1987): Marine birds and plastic pollution. – Marine Ecology Progress Series 37: 295–303 [https://doi.org/10.3354/meps037295].
Bringer, A., J. Cachot, G. Prunier, E. Dubillot, C. Clérandeau, & H. Thomas (2020): Experimental ingestion of fluorescent microplastics by pacific oysters, Crassostrea gigas, and their effects on the behaviour and development at early stages. – Chemosphere 254: 126793 [https://doi.org/10.1016/j.chemosphere.2020.126793].
Chamas, A., H. Moon, J. Zheng, Y. Qiu, T. Tabassum, J.H. Jang, M. Abu-Omar, S.L. Scott & S. Suh (2020): Degradation Rates of Plastics in the Environment. – ACS Sustainable Chemistry & Engineering 8(9): 3494–3511 [https://doi.org/10.1021/acssuschemeng.9b06635].
de Souza Machado, A. A., W. Kloas, C. Zarfl, S. Hempel & M.C. Rillig (2018): Microplastics as an emerging threat to terrestrial ecosystems. – Global Change Biology 24(4): 1405–1416 [https://onlinelibrary.wiley.com/doi/abs/10.1111/gcb.14020].
de Souza Machado, A. A., C. W. Lau, J. Till, W. Kloas, A. Lehmann, R. Becker & M. C. Rillig (2018): Impacts of Microplastics on the Soil Biophysical Environment. – Environmental Science & Technology 52(17): 9656–9665 [https://doi.org/10.1021/acs.est.8b02212].
Fenchel, T. (1980): Suspension feeding in ciliated protozoa: feeding rates and their ecological significance. Microbial Ecology, 6(1): 13–25.
Foissner, W. (1992): Estimating the species richness of soil protozoa using the “non-flooded petri dish method.” Protocols in Protozoology, Society of Protozoologists, Lawrence. P. B-10. 1-B-10. 2 [http://www.wfoissner.at/data_prot/Foissner_1992_B-10-1.pdf].
Fuller, S. & A. Gautam (2016): A Procedure for Measuring Microplastics using Pressurized Fluid Extraction. – Environmental Science & Technology 50(11): 5774–5780 [https://doi.org/10.1021/acs.est.6b00816].
Geisen, S., E. A. D. Mitchell, S. Adl, M. Bonkowski, M. Dunthorn, F. Ekelund, L. D. Fernández, A. Jousset, V. Krashevska, D. Singer, F. W. Spiegel, J. Walochnik & E. Lara (2018): Soil protists: a fertile frontier in soil biology research. – FEMS Microbiology Reviews 42(3): 293–323 [https://doi.org/10.1093/femsre/fuy006].
Geisen, S., E. Lara, E. A. D. Mitchell, E. Völcker & V. Krashevska (2020): Soil protist life matters!. – Soil Organisms 92(3):189–196 [https://doi.org/10.25674/so92iss3pp189].
Hekman, W. E., P. J. Van den Boogert & K. B. Zwart (1992): The physiology and ecology of a novel, obligate mycophagous flagellate. – FEMS Microbiology Letters 86(3): 255–265.
Helcoski, R., L. T. Yonkos, A. Sanchez & A. H. Baldwin (2020): Wetland soil microplastics are negatively related to vegetation cover and stem density. – Environmental Pollution 256: 113391 [https://doi.org/10.1016/j.envpol.2019.113391].
Hidalgo-Ruz, V., L. Gutow, R. C. Thompson & M. Thiel (2012): Microplastics in the marine environment: a review of the methods used for identification and quantification. – Environmental Science & Technology 46(6): 3060–3075 [https://doi.org/10.1021/es2031505].
Huang, Y., Y. Zhao, J. Wang, M. Zhang, W. Jia & X. Qin (2019): LDPE microplastic films alter microbial community composition and enzymatic activities in soil. – Environmental Pollution 254(Pt A): 112983 [https://doi.org/10.1016/j.envpol.2019.112983].
Jacques, O & R. S. Prosser (2021): A probabilistic risk assessment of microplastics in soil ecosystems. – The Science of the Total Environment 757: 143987 [https://doi.org/10.1016/j.scitotenv.2020.143987].
Johansen, J. L., R. Rønn & F. Ekelund (2018): Toxicity of cadmium and zinc to small soil protists. – Environmental Pollution 242(Pt B): 1510–1517 [https://doi.org/10.1016/j.envpol.2018.08.034].
Kim, S. W & Y.-J. An (2020): Edible size of polyethylene microplastics and their effects on springtail behavior. – Environmental Pollution 266(Pt 1): 115255 [https://doi.org/10.1016/j.envpol.2020.115255].
Kim, S. W., D. Kim, S.-W. Jeong & Y.-J. An (2020). Size-dependent effects of polystyrene plastic particles on the nematode Caenorhabditis elegans as related to soil physicochemical properties. Environmental Pollution 258: 113740 [https://doi.org/10.1016/j.envpol.2019.113740].
Kim, S. W., W. R. Waldman, T.-Y Kim & M. C. Rillig (2020): Effects of different microplastics on nematodes in the soil environment: Tracking the Extractable Additives Using an Ecotoxicological Approach. – Environmental Science & Technology 54(21): 13868–13878 [https://doi.org/10.1021/acs.est.0c04641].
Lambert, S., C. Sinclair & A. Boxall (2014): Occurrence, degradation, and effect of polymer-based materials in the environment. – Reviews of Environmental Contamination and Toxicology 227: 1–53 [https://doi.org/10.1007/978-3-319-01327-5_1].
Lei, L., S. Wu, S. Lu, M. Liu, Y. Song, Z. Fu, H. Shi, K. M. Raley-Susman & D. He (2018): Microplastic particles cause intestinal damage and other adverse effects in zebrafish Danio rerio and nematode Caenorhabditis elegans. – The Science of the Total Environment 619-620: 1–8 [https://doi.org/10.1016/j.scitotenv.2017.11.103].
Liu, P., X. Zhan, X. Wu, J. Li, H. Wang & S. Gao (2020): Effect of weathering on environmental behavior of microplastics: Properties, sorption and potential risks. – Chemosphere 242: 125193 [https://doi.org/10.1016/j.chemosphere.2019.125193].
Lozano, Y. M., T. Lehnert, L. T. Linck, A. Lehmann & M. C. Rillig (2021): Microplastic shape, polymer type, and concentration affect soil properties and plant biomass. –
Frontiers in Plant Science 12: 616645 [https://doi.org/10.3389/fpls.2021.616645].
McKeen, L. W. (2013): The Effect of UV Light and Weather on Plastics and Elastomers. William Andrew [https://play.google.com/store/books/details?id=IqCo2mZcDx4C].
Mueller, M.-T., H. Fueser, S. Höss & W. Traunspurger (2020): Species-specific effects of long-term microplastic exposure on the population growth of nematodes, with a focus on microplastic ingestion. – Ecological Indicators 118: 106698 [https://doi.org/10.1016/j.ecolind.2020.106698].
Pischedda, A., M. Tosin & F. Degli-Innocenti (2019): Biodegradation of plastics in soil: The effect of temperature. – Polymer Degradation and Stability 170: 109017 [https://doi.org/10.1016/j.polymdegradstab.2019.109017].
Prokić, M. D., B. R. Gavrilović, T. B. Radovanović, J. P. Gavrić, T. G. Petrović, S. G. Despotović & C. Faggio (2021): Studying microplastics: Lessons from evaluated literature on animal model organisms and experimental approaches. – Journal of Hazardous Materials 414: 125476 [https://doi.org/10.1016/j.jhazmat.2021.125476].
Ren, X., J. Tang, L. Wang & Q. Liu (2021): Microplastics in soil-plant system: effects of nano/microplastics on plant photosynthesis, rhizosphere microbes and soil properties in soil with different residues. – Plant and Soil [https://doi.org/10.1007/s11104-021-04869-1].
Rillig, M. C. (2012): Microplastic in terrestrial ecosystems and the soil? – Environmental Science & Technology 46(12): 6453–6454 [https://doi.org/10.1021/es302011r].
Rillig, M. C. & M. Bonkowski (2018): Microplastic and soil protists: A call for research. – Environmental Pollution 241: 1128–1131) [https://doi.org/10.1016/j.envpol.2018.04.147].
Rillig, M. C., E. Leifheit & J. Lehmann (2021): Microplastic effects on carbon cycling processes in soils. – PLoS Biology 19(3): e3001130 [https://doi.org/10.1371/journal.pbio.3001130].
Ritchie, H. & M. Roser (2018): Plastic pollution. Our world in data. “Plastic Pollution”. – Published online at OurWorldInData.org.
– Retrieved from: ‘https://ourworldindata.org/plastic-pollution’ [Online Resource].
Setälä, O., V. Fleming-Lehtinen & M. Lehtiniemi (2014): Ingestion and transfer of microplastics in the planktonic food web. – Environmental Pollution 185: 77–83) [https://doi.org/10.1016/j.envpol.2013.10.013].
Shang, X., J. Lu, C. Feng, Y. Ying, Y. He, S. Fang, Y. Lin, R. Dahlgren & J. Ju (2020): Microplastic (1 and 5 μm) exposure disturbs lifespan and intestine function in the nematode Caenorhabditis elegans. – The Science of the Total Environment 705: 135837 [https://doi.org/10.1016/j.scitotenv.2019.135837].
Shan, J., J. Zhao, L. Liu, Y. Zhang, X. Wang & F. Wu (2018): A novel way to rapidly monitor microplastics in soil by hyperspectral imaging technology and chemometrics. – Environmental Pollution 238: 121–129 [https://doi.org/10.1016/j.envpol.2018.03.026].
Strungaru, S.-A., R. Jijie, M. Nicoara, G. Plavan & C. Faggio (2019): Micro- (nano) plastics in freshwater ecosystems: Abundance, toxicological impact and quantification methodology. – TrAC Trends in Analytical Chemistry 110: 116–128 [https://doi.org/10.1016/j.trac.2018.10.025].
Verni, F. & P. Gualtieri (1997): Feeding behaviour in ciliated protists. – Micron 28 (6): 487–504) [https://doi.org/10.1016/s0968-4328(97)00028-0].
Waldman, W. R. & M. C. Rillig (2020): Microplastic research should embrace the complexity of secondary particles. – Environmental Science & Technology 54(13): 7751–7753 [https://doi.org/10.1021/acs.est.0c02194].
Wang, J., X. Liu, Y. Li, T. Powell, X. Wang, G. Wang & P. Zhang (2019): Microplastics as contaminants in the soil environment: A mini-review. – The Science of the Total Environment 691: 848–857 [https://doi.org/10.1016/j.scitotenv.2019.07.209].
Wood, S. A. & M. A. Bradford (2018): Chapter 4 - Leveraging a New Understanding of how Belowground Food Webs Stabilize Soil Organic Matter to Promote Ecological Intensification of Agriculture. – Academic Press, Soil Carbon Storage: 117–136 [https://doi.org/10.1016/B978-0-12-812766-7.00004-4].
Yuan, J., Ma, J., Sun, Y., Zhou, T., Zhao, Y., & Yu, F. (2020): Microbial degradation and other environmental aspects of microplastics/plastics. – The Science of the Total Environment 715: 136968 [https://doi.org/10.1016/j.scitotenv.2020.136968].
Zantis, L. J., E. L. Carroll, S. E. Nelms & T. Bosker (2021): Marine mammals and microplastics: A systematic review and call for standardisation. – Environmental Pollution 269: 116142 [https://doi.org/10.1016/j.envpol.2020.116142].
Zhang, M., Y. Zhao, X. Qin, W. Jia, L. Chai, M. Huang & Y. Huan (2019): Microplastics from mulching film is a distinct habitat for bacteria in farmland soil. – The Science of the Total Environment 688: 470–478 [https://doi.org/10.1016/j.scitotenv.2019.06.108].