Abstract
Rotifers are essential invertebrates in freshwater ecosystems. Rotifer community structure reflects the environmental changes. To assess the diversity of rotifers in the Pearl River Delta, we investigated the rotifer community structure in different water bodies types using morphology and DNA metabarcoding. A total of 101 species in 30 genera were recorded. 82 rotifer species were identified by morphology and 31 by OTUs based on DNA metabarcoding. Only 40% (2 orders), 42.9% (9 families), 29.7% (11 genera), and 4% (4 species) were shared by the two identification methods. Primers and imperfect rotifer databases might be responsible for the low annotation of rotifer OTU species. The community structure of rotifer morphospecies and OTUs in the Pearl River Delta changed with seasonal and spatial distribution. Heatmaps showed that different rotifer species responded differently to environmental factors. Our results show that DNA metabarcoding provides complementary rather than identical estimates compared to traditional approaches for rotifers. However, if widely validated and improved, this approach could be a useful alternative for practical applications of rotifers as bioindicators. In the future, environmental DNA metabarcoding is promising for the large-scale study and assessment of rotifer diversity.
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Data availability
The data in this study are available from the corresponding author upon reasonable request.
References
Birky, C. W., Jr., 2007. Workshop on barcoded DNA: application to rotifer phylogeny, evolution, and systematics. Hydrobiologia 593: 175–183. https://doi.org/10.1007/s10750-007-9052-y.
Bucklin, A., P. K. Lindeque, N. Rodriguez-Ezpeleta, A. Albaina & M. Lehtiniemi, 2016. Metabarcoding of marine zooplankton: prospects, progress and pitfalls. Journal of Plankton Research 38: 393–400. https://doi.org/10.1093/plankt/fbw023.
Cheung, M. K., C. H. Au, K. H. Chu, H. S. Kwan & C. K. Wong, 2010. Composition and genetic diversity of picoeukaryotes in subtropical coastal waters as revealed by 454 pyrosequencing. The ISME Journal 4: 1053–1059. https://doi.org/10.1038/ismej.2010.26.
Clarke, L. J., J. M. Beard, K. M. Swadling & B. E. Deagle, 2017. Effect of marker choice and thermal cycling protocol on zooplankton DNA metabarcoding studies. Ecology and Evolution 7: 873–883. https://doi.org/10.1002/ece3.2667.
Deiner, K., H. M. Bik, E. Mächler, M. Seymour, A. Lacoursière-Roussel, F. Altermatt, S. Creer, I. Bista, D. M. Lodge, N. de Vere, M. E. Pfrender & L. Bernatchez, 2017. Environmental DNA metabarcoding: transforming how we survey animal and plant communities. Molecular Ecology 26: 5872–5895. https://doi.org/10.1111/mec.14350.
Fontaneto, D., 2014. Molecular phylogenies as a tool to understand diversity in rotifers. International Review of Hydrobiology 99: 178–187. https://doi.org/10.1002/iroh.201301719.
Fontaneto, D., M. Kaya, E. A. Herniou & T. G. Barraclough, 2009. Extreme levels of hidden diversity in microscopic animals (Rotifera) revealed by DNA taxonomy. Molecular Phylogenetics and Evolution 53: 182–189. https://doi.org/10.1016/j.ympev.2009.04.011.
Fontaneto, D., E. M. Eckert, N. Aninic, E. Lara & E. A. Mitchell, 2019. We are ready for faunistic surveys of bdelloid rotifers through DNA barcoding: the example of Sphagnum bogs of the Swiss Jura Mountains. Limnetica 38: 213–225. https://doi.org/10.23818/limn.38.02.
García-Morales, A. E. & M. Elías-Gutiérrez, 2013. DNA barcoding of freshwater Rotifera in Mexico: evidence of cryptic speciation in common rotifers. Molecular Ecology Resources 13: 1097–1107. https://doi.org/10.1111/1755-0998.12080.
Gilbert, J. J., 2017. Non-genetic polymorphisms in rotifers: environmental and endogenous controls, development, and features for predictable or unpredictable environments. Biological Reviews 92: 964–992. https://doi.org/10.1111/brv.12264.
Iakovenko, N. S., J. Smykla, P. Convey, E. Kašparová, I. A. Kozeretska, V. Trokhymets, I. Dykyy, M. Plewka, M. Devetter, Z. Duriš & K. Janko, 2015. Antarctic bdelloid rotifers: diversity, endemism and evolution. Hydrobiologia 761: 5–43. https://doi.org/10.1007/s10750-015-2463-2.
Jersabek, C. D. & M. F. Leitner, 2013. The Rotifer World Catalog. World Wide Web electronic publication. http://www.rotifera.hausdernatur.at/, accessed 2023–01–29.
Keck, F., R. C. Blackman, R. Bossart, J. Brantschen, M. Couton, S. Hürlemann, D. Kirschner, N. Locher, H. Zhang & F. Altermatt, 2022. Meta-analysis shows both congruence and complementarity of DNA and eDNA metabarcoding to traditional methods for biological community assessment. Molecular Ecology 31: 1820–1835. https://doi.org/10.1111/mec.16364.
Koste, W., 1978. Rotatoria: Die Rädertiere Mitteleuropas. Gebrüder Borntraeger, Berlin.
Liang, D., Q. Wang, N. Wei, C. Tang, X. Sun & Y. F. Yang, 2020. Biological indicators of ecological quality in typical urban river-lake ecosystems: the planktonic rotifer community and its response to environmental factors. Ecological Indicators 112: 106127. https://doi.org/10.1016/j.ecolind.2020.106127.
Mills, S., J. A. Alcántara-Rodríguez, J. Ciros-Pérez, A. Gómez, A. Hagiwara, K. H. Galindo, C. D. Jersabek, R. Malekzadeh-Viayeh, F. Leasi, J. S. Lee, D. B. M. Welch, S. Papakostas, S. Riss, H. Segers, M. Serra, R. Shiel, R. Smolak, T. W. Snell, C. P. Stelzer, C. Q. Tang, R. L. Wallace, D. Fontaneto & E. J. Walsh, 2017. Fifteen species in one: deciphering the Brachionus plicatilis species complex (Rotifera, Monogononta) through DNA taxonomy. Hydrobiologia 796: 39–58. https://doi.org/10.1007/s10750-016-2725-7.
Novotny, A., S. Zamora-Terol & M. Winder, 2021. DNA metabarcoding reveals trophic niche diversity of micro and mesozooplankton species. Proceedings of the Royal Society B 288: 20210908. https://doi.org/10.1098/rspb.2021.0908.
Obertegger, U., D. Fontaneto & G. Flaim, 2012. Using DNA taxonomy to investigate the ecological determinants of plankton diversity: explaining the occurrence of Synchaeta spp. (Rotifera, Monogononta) in mountain lakes. Freshwater Biology 57: 1545–1553. https://doi.org/10.1111/j.1365-2427.2012.02815.x.
Oliver, T. H., M. S. Heard, N. J. Isaac, D. B. Roy, D. Procter, F. Eigenbrod, R. Freckleton, A. Hector, C. D. L. Orme, O. L. Petchey, V. Proença, D. Raffaelli, K. B. Suttle, G. M. Mace, B. Martín-López, B. A. Woodcock & J. M. Bullock, 2015. Biodiversity and resilience of ecosystem functions. Trends in Ecology & Evolution 30: 673–684. https://doi.org/10.1016/j.tree.2015.08.009.
Örstan, A., 2021. An extraordinary new fluvial bdelloid rotifer, Coronistomus impossibilis gen. nov., sp. nov., with adaptations for turbulent flow (Rotifera: Bdelloidea: Coronistomidae fam. nov.). Zootaxa 4966: 1628. https://doi.org/10.11646/ZOOTAXA.4966.1.2.
Segers, H., 2007. Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Zootaxa 1564: 1–104. https://doi.org/10.11646/zootaxa.1564.1.1.
Segers, H., 2008. Global diversity of rotifers (Rotifera) in freshwater. Hydrobiologia 595: 49–59. https://doi.org/10.1007/s10750-007-9003-7.
Song, M. O. & C. H. Lee, 2022. Descriptions of Philodinavus koreanus n. sp. and two new species of Philodina (Rotifera, Bdelloidea) from Korea. Zootaxa 5129: 399–411. https://doi.org/10.11646/zootaxa.5129.3.4.
Song, J. & D. Liang, 2023. Community structure of zooplankton and its response to aquatic environmental changes based on eDNA metabarcoding. Journal of Hydrology 622: 129692.
State Environmental Protection Administration of China, 2002. Methods for Monitoring and Analysis of Water and Wastewater, 4th ed. Chinese Environment Science Press, Beijing:
Tang, C. Q., F. Leasi, U. Obertegger, A. Kieneke, T. G. Barraclough & D. Fontaneto, 2012. The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proceedings of the National Academy of Sciences 109: 16208–16212. https://doi.org/10.1073/pnas.1209160109.
Thornhill, I. A., J. Biggs, M. J. Hill, R. Briers, D. Gledhill, P. J. Wood, J. H. R. Gee, M. Ledger & C. Hassall, 2018. The functional response and resilience in small waterbodies along land-use and environmental gradients. Global Change Biology 24: 3079–3092. https://doi.org/10.1111/gcb.14149.
Wang, J. J., 1961. Freshwater Rotifer Fauna in China. Science Press, Beijing.
Wang, Q., Y. F. Yang & J. Chen, 2009. Impact of environment on the spatiotemporal distribution of rotifers in the tidal Guangzhou segment of the Pearl River Estuary China. International Review of Hydrobiology 94: 688–705. https://doi.org/10.1002/iroh.200811122.
Weigand, H., A. J. Beermann, F. Čiampor, F. O. Costa, Z. Csabai, S. Duarte, M. F. Geiger, M. Grabowski, F. Rimet, B. Rulik, M. Strand, N. Szucsich, A. M. Weigand, E. Willassen, S. A. Wyler, A. Bouchez, A. Borja, Z. Čiamporová-Zaťovičová, S. Ferreira, K. B. Dijkstra, U. Eisendle, J. Freyhof, P. Gadawski, W. Graf, A. Haegerbaeumer, B. B. van der Hoorn, B. Japoshvili, L. Keresztes, E. Keskin, F. Leese, J. N. Macher, T. Mamos, G. Paz, V. Pešić, D. M. Pfannkuchen, M. A. Pfannkuchen, B. W. Price, B. Rinkevich, M. A. L. Teixeira, G. Várbíró & T. Ekrem, 2019. DNA barcode reference libraries for the monitoring of aquatic biota in Europe: gap-analysis and recommendations for future work. Science of the Total Environment 678: 499–524. https://doi.org/10.1016/j.scitotenv.2019.04.247.
Xiong, W., X. Huang, Y. Chen, R. Fu, X. Du, X. Chen & A. Zhan, 2020. Zooplankton biodiversity monitoring in polluted freshwater ecosystems: a technical review. Environmental Science and Ecotechnology 1: 100008. https://doi.org/10.1016/j.ese.2019.100008.
Yang, J. & X. Zhang, 2020. eDNA metabarcoding in zooplankton improves the ecological status assessment of aquatic ecosystems. Environment international 134: 105230. https://doi.org/10.1016/j.envint.2019.105230.
Zhang, G. K., F. J. Chain, C. L. Abbott & M. E. Cristescu, 2018. Metabarcoding using multiplexed markers increases species detection in complex zooplankton communities. Evolutionary Applications 11: 1901–1914. https://doi.org/10.1111/eva.12694.
Zhang, M., B. Ji, S. Wang, J. Gu & Y. Liu, 2022. Granule size informs the characteristics and performance of microalgal-bacterial granular sludge for wastewater treatment. Bioresource Technology 346: 126. https://doi.org/10.1016/j.biortech.2021.126649.
Acknowledgements
This work was supported by Guangdong Basic and Applied Basic Research Foundation (2021A1515010814, 2022A1515011387), and Innovation Group Project of Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai) (311022011). Many thanks to Pingyu Sun and Jianlin Guo for sampling assistance. We thank two anonymous reviewers for offering constructive comments that improved this manuscript. Our special thanks are given to Prof. Larry Liddle (Long Island University, USA) and David Montagnes (The University of Liverpool, UK) for their help to revise this manuscript.
Funding
Funding was provided by Basic and Applied Basic Research Foundation of Guangdong Province (Grant nos. 2021A1515010814, 2022A1515011387) and Innovation Group Project of Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai) (Grant no. 311022011).
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Wang, Q., Wang, W., Liu, L. et al. Temporal and spatial dynamics of rotifer communities in the Pearl River Delta (China) with emphasis on DNA metabarcoding versus morphology to assess rotifer diversity. Hydrobiologia 851, 2999–3012 (2024). https://doi.org/10.1007/s10750-023-05357-6
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DOI: https://doi.org/10.1007/s10750-023-05357-6