SpringerLink
Log in

Spatial and temporal dynamics of a freshwater eukaryotic plankton community revealed via 18S rRNA gene metabarcoding

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

DNA metabarcoding is a sophisticated molecular tool that can enhance biological surveys of freshwater plankton communities by providing broader taxonomic coverage and, for certain groups, higher taxonomic resolution compared to morphological methods. We conducted 18S rRNA gene metabarcoding analyses on 214 water samples collected over a four-month period from multiple sites within a freshwater reservoir. We detected 1,314 unique operational taxonomic units that included various metazoans, protists, chlorophytes, and fungi. Alpha diversity differed among sites, suggesting local habitat variation linked to differing species responses. Strong temporal variation was detected at both daily and monthly scales. Diversity and relative abundance patterns for several protist groups (including dinoflagellates, ciliates, and cryptophytes) differed from arthropods (e.g., cladocerans and copepods), a traditional focus of plankton surveys. This suggests that the protists respond to different environmental dimensions and may therefore provide additional information regarding ecosystem status. Comparison of the sequence-based population survey data to conventional-based data revealed similar trends for taxa that were ranked among the most abundant in both approaches, although some groups were missing in each data set. These results highlight the potential benefit of supplementing conventional biological survey approaches with metabarcoding to obtain a more comprehensive understanding of freshwater plankton community structure and dynamics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anderson, M. J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32–46.

    Google Scholar 

  • Bachy, C., J. R. Dolan, P. López-García, P. Deschamps & David Moreira, 2013. Accuracy of protist diversity assessments: morphology compared with cloning and direct pyrosequencing of 18S rRNA genes and ITS regions using the conspicuous tintinnid ciliates as a case study. The ISME Journal 7: 244–255.

    Article  PubMed  CAS  Google Scholar 

  • Bista, I., G. R. Carvalho, K. Walsh, M. Seymour, M. Hajibabae, D. Lallias, M. Christmas & S. Creer, 2017. Annual time-series analysis of aqueous eDNA reveals ecologically relevant dynamics of lake ecosystem biodiversity. Nature Communications 8: 14087.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Blaise, C. & J. F. Férard, 2005. Small-Scale Freshwater Toxicity Investigations, Vol. 1. Springer, Berlin: 1–68.

    Book  Google Scholar 

  • Blinn, D. W. & D. B. Herbst, 2003. Use of diatoms and soft algae as indicators of environmental determinants in the Lahontan Basin, USA. Annual Report for California State Water Resources Board Contract Agreement 704558.01.CT766.

  • Bradley, I. M., A. J. Pinto & J. S. Guest, 2016. Design and evaluation of Illumina MiSeq-compatible, 18S rRNA gene-specific primers for improved characterization of mixed phototrophic communities. Applied & Environmental Microbiology 82: 5878–5891.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Buskey, E. J., 1997. Behavioral components of feeding selectivity of the heterotrophic dinoflagellate Protoperidinium pellucidum. Marine Ecology Progress Series 153: 77–89.

    Article  Google Scholar 

  • Camacho, C., G. Coulouris, V. Avagyan, N. Ma, J. Papadopoulos, K. Bealer, & T. L. Madden, 2009. BLAST+: architecture and applications. BMC Bioinformatics 10: 421.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carpenter, S. R., N. F. Caraco, D. L. Correll, R. W. Howarth, A. N. Sharpley & V. H. Smith, 1998. Nonpoint pollution of surface waters with phosphorous and nitrogen. Ecological Applications 8: 559–568.

    Article  Google Scholar 

  • Chan, A., L.-P. Chiang, H. C. Hapuarachchi, C.-H. Tan, S.-C. Pang, R. Lee, K.-S. Lee, L.-C. Ng & S.-G. Lam-Phua, 2014. DNA barcoding: complementing morphological identification of mosquito species in Singapore. Parasites & Vectors 7: 569.

    Article  CAS  Google Scholar 

  • Chang, F., J. J. Pagano, B. S. Crimmins, M. S. Milligan, X. **a, P. K. Hopke, & T. M. Holsen, 2012. Temporal trends of polychlorinated biphenyls and organochlorine pesticides in Great Lakes fish, 1999–2009. Science of The Total Environment 439: 284–290.

    Article  PubMed  CAS  Google Scholar 

  • Chen, K., J. Allen & J. Lu, 2017. Community structures of phytoplankton with emphasis on toxic cyanobacteria in an Ohio inland lake during bloom season. Journal of Water Resources and Protection 9: 1299–1318.

    Article  Google Scholar 

  • Creer, S., V. G. Fonseca, D. L. Porazinska, R. M. Giblin-Davis, W. Sung, D. M. Power, M. Packer, G. R. Carvalho, M. L. Blaxter, P. J. Lambshead & W. K. Thomas, 2010. Ultrasequencing of the meiofaunal biosphere: practice, pitfalls and promises. Molecular Ecology 19: 4–20.

    Article  PubMed  Google Scholar 

  • Debroas, D., I. Domaizon, J. F. Humbert, L. Jardillier, C. Lepère, A. Oudart & N. Taib, 2017. Overview of freshwater microbial eukaryotes diversity: a first analysis of publicly available metabarcoding data. FEMS Microbiology Ecology. https://doi.org/10.1093/femsec/fix023.

    Article  PubMed  Google Scholar 

  • Diaz, R. J., 2001. Overview of hypoxia around the world. Journal of Environmental Quality 30: 275–281.

    Article  PubMed  CAS  Google Scholar 

  • Edsall, T. A., M. T. Bur, O. T. Gorman & J. S. Schaeffer, 2005. Burrowing mayflies as indicators of ecosystem health: status of populations in western Lake Erie, Saginaw Bay and Green Bay. Aquatic Ecosystem Health & Management 8: 107–116.

    Article  Google Scholar 

  • Edgar, R. C., 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461.

    Article  PubMed  CAS  Google Scholar 

  • Edlund, M. B., J. M. Ramstack, D. R. Engstrom, J. E. Elias, & B. M. Lafrancois, 2011. Biomonitoring using diatoms and paleolimnology in the western Great Lakes national parks. Natural Resource Technical Report NPS/GLKN/NRTR—2011/447. National Park Service, Fort Collins, Colorado.

  • Emilson, C. E., D. G. Thompson, L. A. Venier, T. M. Porter, T. Swystun, D. Chartrand, S. Capell, & M. Hajibabaei. 2017. DNA metabarcoding and morphological macroinvertebrate metrics reveal the same changes in boreal watersheds across an environmental gradient. Scientific Reports 7, Article number: 12777.

  • Fenchel, T., 2008. The microbial loop—25 years later. Journal of Experimental Marine Biology and Ecology 366: 99–103.

    Article  Google Scholar 

  • Finlay, B. J., 1981. Oxygen availability and seasonal migrations of ciliated protozoa in a freshwater lake. Microbiology 123: 173–178.

    Article  Google Scholar 

  • Gihring, T. M., S. J. Green & C. W. Schadt, 2012. Massively parallel rRNA gene sequencing exacerbates the potential for biased community diversity comparisons due to variable library sizes. Environmental Microbiology 14: 285–290.

    Article  PubMed  CAS  Google Scholar 

  • Hadziavdic, K., K. Lekang, A. Lanzen, I. Jonassen, E. M. Thompson & C. Troedsson, 2014. Characterization of the 18S rRNA gene for designing universal eukaryote specific primers. PLoS ONE 9: e87624.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hänfling, B., H. L. Lawson, D. S. Read, C. Hahn, J. Li, P. Nichols, R. C. Blackman, A. Oliver & I. J. Winfield, 2016. Environmental DNA metabarcoding of lake fish communities reflects long-term data from established survey methods. Molecular Ecology 25: 3101–3119.

    Article  PubMed  CAS  Google Scholar 

  • Harrell, F. E., Jr., C. Dupont, & others. 2017. Hmisc: Harrell Miscellaneous. R package version 4.0-3. https://CRAN.R-project.org/package=Hmisc.

  • Havel, J. E. & J. B. Shurin, 2004. Mechanisms, effects, and scales of dispersal in freshwater zooplankton. Limnology and Oceanography 49: 1229–1238.

    Article  Google Scholar 

  • Hayes, N. M., B. R. Deemer, J. R. Corman, N. R. Razavi, & K. E. Strock, 2017. Key differences between lakes and reservoirs modify climate signals: A case for a new conceptual model. Limnology and Oceanography Letters 2: 47–62.

    Article  Google Scholar 

  • Holdren, C., W. Jones, & J. Taggart, 2001. Managing lakes and reservoirs. North American Lake Management Society and Terrene Institute, in cooperation with Office of Water, Assessment and Watershed Protection Division, Madison, WI.

  • Hopkins, G. W. & R. P. Freckleton, 2002. Declines in the numbers of amateur and professional taxonomists: implications for conservation. Animal Conservation Forum 5: 245–249.

    Article  Google Scholar 

  • Indiana Department of Environmental Management. 2016. Indiana’s 2016 consolidated assessment and listing methodology (CALM). http://www.in.gov/idem/nps/files/ir_2016_report_apndx_l_attch_1.pdf. Accessed 19 July 2017.

  • Jeong, H. J., Y. D. Yoo, S. T. Kim & N. S. Kang, 2004. Feeding by the heterotrophic dinoflagellate Protoperidinium bipes on the diatom Skeletonema costatum. Inter-Research Aquatic Microbial Ecology 36: 171–179.

    Article  Google Scholar 

  • Jørgensen, S. E., F.-L. Xu & R. Costanza, 2016. Handbook of ecological indicators for assessment of ecosystem health, 2nd ed. CRC Press Taylor & Francis Group, New York.

    Google Scholar 

  • Kammerlander, B., H.-W. Breiner, S. Filker, R. Sommaruga, B. Sonntag & T. Stoeck, 2015. High diversity of protistan plankton communities in remote high mountain lakes in the European Alps and the Himalayan mountains. FEMS Microbiology Ecology 91(4): fiv010.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kans, J., 2017. Entrez Direct: E-utilities on the UNIX Command Line. https://www.ncbi.nlm.nih.gov/books/NBK179288/?report=reader#!po=0.574713. Accessed 12 July 2017.

  • Kapoor, V., M. Elk, X. Li, C. A. Impellitteri & J. W. Santo Domingo, 2016. Effects of Cr(III) and Cr(VI) on nitrification inhibition as determined by SOUR, function-specific gene expression and 16S rRNA sequence analysis of wastewater nitrifying enrichments. Chemosphere 147: 361–367.

    Article  PubMed  CAS  Google Scholar 

  • Karr, J. R., 1981. Assessment of biotic integrity using fish communities. Fisheries 6: 21–27.

    Article  Google Scholar 

  • Keck, F., V. Vasselon, K. Tapolczai, F. Rimet, & A. Bouchez, 2017. Freshwater biomonitoring in the Information Age. Frontiers in Ecology and the Environment 15: 266–274.

    Article  Google Scholar 

  • Kelly, R. P., J. A. Port, K. M. Yamahara & L. B. Crowder, 2014. Using environmental DNA to census marine fishes in a large mesocosm. PLoS ONE 9: e86175.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kentucky Department for Environmental Protection, Division of Water, 2016. Standard operating procedures. http://water.ky.gov/Pages/SurfaceWaterSOP.aspx.

  • Ko, H.-L., Y.-T. Wang, T.-S. Chiu, M.-A. Lee, M.-Y. Leu, K.-Z. Chang, W.-Y. Chen & K.-T. Shao, 2013. Evaluating the accuracy of morphological identification of larval fishes by applying DNA barcoding. PLoS ONE 8: e53451.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kumar, S., G. Stecher & K. Tamura, 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874.

    Article  PubMed  CAS  Google Scholar 

  • Leray, M. & N. Knowlton, 2016. Censusing marine eukaryotic diversity in the twenty-first century. Philosophical Transactions of the Royal Society B: Biological Sciences 371: 20150331.

    Article  Google Scholar 

  • Lepère, C., I. Doimazon, M. Hugoni, A. Vellet & D. Debroas, 2016. Diversity and dynamics of active small microbial eukaryotes in the anoxic zone of a freshwater meromictic lake (Pavin, France). Frontiers in Microbiology 7: 130.

    Article  PubMed  PubMed Central  Google Scholar 

  • Leung, B., D. M. Lodge, D. Finnoff, J. F. Shogren, M. A. Lewis & G. Lamberti, 2002. An ounce of prevention or a pound of cure: bioeconomic risk analysis of invasive species. Proceedings of the Royal Society B—Biological Sciences 269: 2407–2413.

    Article  PubMed Central  Google Scholar 

  • Lovell, D., V. Pawlowsky-Glahn, J. J. Egozcue, S. Marguerat & J. Bähler, 2015. Proportionality: a valid alternative to correlation for relative data. PLOS Computational Biology. https://doi.org/10.1371/journal.pcbi.1004075.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lynch, A. J., S. J. Cooke, A. M. Deines, S. D. Bower, D. B. Bunnell, I. G. Cowx, V. M. Nguyen, J. Nohner, K. Phouthavong, B. Riley, M. W. Rogers, W. W. Taylor, W. Woelmer, S.-J. Youn & T. D. Beard Jr., 2016. The social, economic, and environmental importance of inland fish and fisheries. Environmental Reviews 24: 115–121.

    Article  Google Scholar 

  • Martin, M., 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal 17: 10–12.

    Article  Google Scholar 

  • McCune, B., & M. J. Mefford, 2016. PC-ORD: multivariate analysis of ecological data; Version 7.02.

  • McMahon, G. F., & M. C. Farmer, 2004. Reallocation of federal multipurpose reservoirs: principles, policy and practice. Proceedings of the 2003 Georgia Water Resources Conference, held April 23–24, 2003, at the University of Georgia. Kathryn J. Hatcher, editor, Institute of Ecology, The University of Georgia, Athens, Georgia.

  • Merchant, S. S., S. E. Prochnik, O. Vallon, E. H. Harris, S. J. Karpowicz, G. B. Witman, A. Terry, A. Salamov, L. K. Fritz-Laylin, L. Maréchal-Drouard, W. F. Marshall, L.-H. Qu, D. R. Nelson, A. A. Sanderfoot, M. H. Spalding, V. V. Kapitonov, Q. Ren, P. Ferris, E. Lindquist, H. Shapiro, S. M. Lucas, J. Grimwood, J. Schmutz, P. Cardol, H. Cerutti, G. Chanfreau, C.-L. Chen, V. Cognat, M. T. Croft, R.l Dent, S. Dutcher, E. Fernández, H. Fukuzawa, D. González-Ballester, D. González-Halphen, A. Hallmann, M. Hanikenne, M. Hippler, W. Inwood, K. Jabbari, M. Kalanon, R. Kuras, P. A. Lefebvre, S. D. Lemaire, A. V. Lobanov, M. Lohr, A. Manuell, I. Meier, L. Mets, M. Mittag, T. Mittelmeier, J. V. Moroney, J. Moseley, C. Napoli, A. M. Nedelcu, K. Niyogi, S. V. Novoselov, I. T. Paulsen, G. Pazour, S. Purton, J.-P. Ral, D. M. Riaño-Pachón, W. Riekhof, L. Rymarquis, M. Schroda, D. Stern, J. Umen, R. Willows, N. Wilson, S. Lana Zimmer, J. Allmer, J. Balk, K. Bisova, C.-J. Chen, M. Elias, K. Gendler, C. Hauser, M. Rose Lamb, H. Ledford, J. C. Long, J. Minagawa, M. D. Page, J. Pan, W. Pootakham, S. Roje, A. Rose, E. Stahlberg, A. M. Terauchi, P. Yang, S. Ball, C. Bowler, C. L. Dieckmann, V. N. Gladyshev, P. Green, R. Jorgensen, S. Mayfield, B. Mueller-Roeber, S. Rajamani, R. T. Sayre, P. Brokstein, I. Dubchak, D. Goodstein, L. Hornick, Y. W. Huang, J. Jhaveri, Y. Luo, D. Martínez, W. Chi, A. Ngau, B.Otillar, A. Poliakov, A. Porter, L. Szajkowski, G. Werner, K. Zhou, I. V. Grigoriev, D. S. Rokhsar, & A. R. Grossman, 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245–250.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Naigaga, I., H. Kaiser, W. J. Muller, L. Ojok, D. Mbabazi, G. Magezi, & E. Muhumuza, 2011. Fish as bioindicators in aquatic environmental pollution assessment: a case study in Lake Victoria wetlands, Uganda. Physics and Chemistry of the Earth 36: 918–928.

    Article  Google Scholar 

  • Oksanen, J., F. G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. McGlinn, P. R. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, E. Szoecs, & H. Wagner, 2017. vegan: Community Ecology Package. R package version 2.4-3. https://CRAN.R-project.org/package=vegan.

  • Pace, N. R., D. A. Stahl, D. J. Lane, & G. J. Olsen, 1986. The analysis of natural microbial populations by ribosomal RNA sequences. In Advances in Microbial Ecology (pp. 1–55). Springer, USA.

  • Patz, J. A., P. Daszak, G. M. Tabor, A. A. Aguirre, M. Pearl, J. Epstein, N. D. Wolfe, A. M. Kilpatrick, J. Foufopoulos, D. Molyneux, D. J. Bradley & Members of the Working Group on Land Use Change Disease Emergence, 2004. Unhealthy landscapes: policy recommendations on land use change and infectious disease emergence. Environmental Health Perspectives 112: 1092–1098.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pawlowski, J., F. Lejzerowicz, L. Apotheloz-Perret-Gentil, J. Visco & P. Esling, 2016. Protist metabarcoding and environmental biomonitoring: time for change. European Journal of Protistology 55: 12–25.

    Article  PubMed  CAS  Google Scholar 

  • Piredda, R., M. P. Tomasino, A. M. D’Erchia, C. Manzari, G. Pesole, M. Montresor, W. H. C. F. Kooistra, D. Sarno & A. Zingone, 2017. Diversity and temporal patterns of planktonic protist assemblages at a Mediterranean Long Term Ecological Research site. FEMS Microbiology Ecology. https://doi.org/10.1093/femsec/fiw200.

    Article  PubMed  Google Scholar 

  • Pochon, X., S. A. Wood, N. B. Keeley, F. Lejzerowicz, P. Esling, J. Drew & J. Pawlowski, 2015. Accurate assessment of the impact of salmon farming on benthic sediment enrichment using foraminiferal metabarcoding. Marine Pollution Bulletin 100: 370–382.

    Article  PubMed  CAS  Google Scholar 

  • Pruesse, E., J. Peplies, & F. O. Glöckner, 2012. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28: 1823–1829. (Online alignment tool and search engine accessed via https://www.arb-silva.de/aligner/). Accessed 3 June 2017.

  • Rimet, F., V. Vasselon, B. A. Keszte & A. Bouchez, 2018. Do we similarly assess diversity with microscopy and high-throughput sequencing? Case of microalgae in lakes. Organisms Diversity & Evolution 8: 1–12.

    Google Scholar 

  • Quast, C., E. Pruesse, P. Yilmaz, J. Gerken, T. Schweer, P. Yarza, J. Peplies & F. O. Glöckner, 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41: D590–D596.

    Article  PubMed  CAS  Google Scholar 

  • R Core Team, 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.

  • Rees, H. C., B. C. Maddison, D. J. Middleditch, J. R. M. Patmore & K. C. Gough, 2014. The detection of aquatic animal species using environmental DNA—a review of eDNA as a survey tool in ecology. Journal of Applied Ecology 51: 1450–1459.

    Article  CAS  Google Scholar 

  • Roller, B. R. K., S. F. Stoddard & T. M. Schmidt, 2016. Exploiting rRNA operon copy number to investigate bacterial reproductive strategies. Nature microbiology 1(11): 16160.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schmidt, T. M., E. F. DeLong & N. R. Pace, 1991. Analysis of a marine picoplankton community by 16S rRNA gene cloning and sequencing. Journal of Bacteriology 173: 4371–4378.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schulz, R., 2004. Field studies on exposure, effects, and risk mitigation of aquatic nonpoint-source insecticide pollution. Journal of Environmental Quality 33: 419–448.

    Article  PubMed  CAS  Google Scholar 

  • Sherr, E. B. & B. F. Sherr, 2002. Significance of predation by protists in aquatic microbial food webs. Antonie van Leeuwenhoek 81: 293–308.

    Article  PubMed  CAS  Google Scholar 

  • Sherr, E. B. & B. F. Sherr, 2007. Heterotrophic dinoflagellates: a significant component of microzooplankton biomass and major grazers of diatoms in the sea. Marine Ecology Progress Series 352: 187–197.

    Article  Google Scholar 

  • Siciliano, A., R. Gesuele & M. Guida, 2015. How Daphnia (Cladocera) assays may be used as bioindicators of health effects. Journal of Biodiversity & Endangered Species S1: 005.

    Google Scholar 

  • Simon, M., P. López-García, P. Deschamps, D. Moreira, G. Restoux, P. Bertolino & L. Jardillie, 2015. Marked seasonality and high spatial variability of protist communities in shallow freshwater systems. The ISME Journal 9: 1941–1953.

    Article  PubMed  PubMed Central  Google Scholar 

  • Smayda, T. J., 2008. Complexity in the eutrophication-harmful algal bloom relationship, with comment on the importance of grazing. Harmful Algae 8: 140–151.

    Article  CAS  Google Scholar 

  • Sogin, M. L., H. G. Morrison, J. A. Huber, D. M. Welch, S. M. Huse, P. R. Neal, J. M. Arrieta & G. J. Herndl, 2006. Microbial diversity in the deep sea and the underexplored ‘‘rare biosphere’’. Proceeding of the National Academy of Sciences USA 103: 12115–12120.

    Article  CAS  Google Scholar 

  • Stoddard, S. F., B. J. Smith, R. Hein, B. R. K. Roller, & T. M. Schmidt, 2014. rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Research 43: D593–D598. https://doi.org/10.1093/nar/gku1201

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tautz, D., P. Arctander, A. Minelli, R. H. Thomas & A. P. Vogler, 2003. A plea for DNA taxonomy. Trends in Ecology & Evolution 18: 70–74.

    Article  Google Scholar 

  • Techtmann, S. M., M. Zhuang, P. Campo, E. Holder, M. Elk, T. C. Hazen, R. Conmy & J. W. Santo Domingo, 2017. Corexit 9500 enhances oil biodegradation and changes active bacterial community structure of oil-enriched microcosms. Applied and Environmental Microbiology 83: e03462-16.

    Article  PubMed  PubMed Central  Google Scholar 

  • Trebitz, A. S., J. C. Hoffman, J. A. Darling, E. M. Pilgrim, J. R. Kelly, E. A. Brown, W. L. Chadderton, S. P. Egan, E. K. Grey, S. A. Hashsham, K. E. Klymus, A. R. Mahon, J. L. Ram, M. T. Schultz, C. A. Stepien & J. C. Schardt, 2017. Early detection monitoring for aquatic non-indigenous species: optimizing surveillance, incorporating advanced technologies, and identifying research needs. Journal of Environmental Management 202: 299–310.

    Article  PubMed  CAS  Google Scholar 

  • USEPA, 2016. National Lakes Assessment 2012: A Collaborative Survey of Lakes in the United States. EPA 841-R-16-113. U.S. Environmental Protection Agency, Washington, DC. https://nationallakesassessment.epa.gov/.

  • USEPA, 2017. Indicators used in the national aquatic resource surveys. https://www.epa.gov/national-aquatic-resource-surveys/indicators-used-national-aquatic-resource-surveys. Accessed 25 June 2017.

  • Valentini, A., P. Taberlet, C. Miaud, R. Civade, J. Herder, P. F. Thomsen, E. Bellemain, A. Besnard, E. Coissac, F. Boyer, C. Gaboriaud, P. Jean, N. Poulet, N. Roset, G. H. Copp, P. Geniez, D. Pont, C. Argillier, J. M. Baudoin, T. Peroux, A. J. Crivelli, A. Olivier, M. Acqueberge, M. Le Brun, P. R. Møller, E. Willerslev & T. Dejean, 2016. Next-generation monitoring of aquatic biodiversity using environmental DNA metabarcoding. Molecular Ecology 25: 929–942.

    Article  PubMed  CAS  Google Scholar 

  • Vasselon, V., F. Rimet, K. Tapolczai & A. Bouchez, 2017. Assessing ecological status with diatoms DNA metabarcoding: scaling-up on a WFD monitoring network (Mayotte island, France). Ecological Indicators 82: 1–12.

    Article  CAS  Google Scholar 

  • Wagner, C. & R. Adrian, 2011. Consequences of changes in thermal regime for plankton diversity and trait composition in a polymictic lake: a matter of temporal scale. Freshwater Biology 56: 1949–1961.

    Article  Google Scholar 

  • Walker, P. J. & J. R. Winton, 2010. Emerging viral diseases of fish and shrimp. Veterinary Research 41: 51–75.

    Article  PubMed  PubMed Central  Google Scholar 

  • White, M. M. & I. A. McLaren, 2000. Copepod development rates in relation to genome size and 18S rDNA copy number. Genome 43: 750–755.

    Article  PubMed  CAS  Google Scholar 

  • Wilde, S. B., J. R. Johansen, H. D. Wilde, P. Jiang, B. A. Bartelme & R. S. Haynie, 2014. Aetokthonos hydrillicola gen. et sp. nov.: Epiphytic cyanobacteria on invasive aquatic plants implicated in Avian Vacuolar Myelinopathy. Phytotaxa 181: 243–260.

    Article  Google Scholar 

  • Woese, C. R. & G. E. Fox, 1977. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proceedings of the National Academy of Sciences of the United States of America 74: 5088–5090.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wurzbacher, C., A. Fuchs & K. Attermeyer, 2017. Shifts among Eukaryota, Bacteria, and Archaea define the vertical organization of a lake sediment. Microbiome 5: 41.

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu, F.-L., S. Tao, R. W. Dawson, P.-G. Li & J. Cao, 2001. Lake ecosystem health assessment: indicators and methods. Water Research 35: 3157–3167.

    Article  PubMed  CAS  Google Scholar 

  • Yang, J., X. Zhang, Y. **e, C. Song, Y. Zhang, H. Yu, & G. Allen Burton, 2017. Zooplankton community profiling in a eutrophic freshwater ecosystem-Lake Tai Basin by DNA metabarcoding. Scientific Reports 7: 1773.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yarza, P., P. Yilmaz, E. Pruesse, F. O. Glöckner, W. Ludwig, K. H. Schleifer, W. B. Whitman, J. Euzéby, R. Amann & R. Rosselló-Móra, 2014. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nature Reviews Microbiology 12: 635–645.

    Article  PubMed  CAS  Google Scholar 

  • Yi, Z., C. Berney, H. Hartikainen, S. Mahamdallie, M. Gardner, J. Boenigk, T. Cavalier-Smith & D. Bass, 2017. High-throughput sequencing of microbial eukaryotes in Lake Baikal reveals ecologically differentiated communities and novel evolutionary radiations. FEMS Microbiology Ecology. https://doi.org/10.1093/femsec/fix073.

    Article  PubMed  Google Scholar 

  • Yilmaz, P., L. W. Parfrey, P. Yarza, J. Gerken, E. Pruesse, C. Quast, T. Schweer, J. Peplies, W. Ludwig & F. O. Glöckner, 2014. The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Research 42: D643–D648.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge Joel Allen, Mia Varner, Dana Macke, Kit Daniels, and Armah de la Cruz for their role in collecting, transporting and processing the lake water samples used in this study and Chris Nietch and Jade Young for their roles in providing the USACE zooplankton data. The U.S. Environmental Protection Agency, through its Office of Research and Development, partially funded and participated in the research described herein. Any opinions expressed in this paper are those of the authors and do not necessarily reflect the views of the agency; therefore, no official endorsement should be inferred. Any mention of trade names or commercial products does not constitute endorsement or recommendation for use.

Author information

Authors and Affiliations

  1. US Environmental Protection Agency, Cincinnati, OH, 45268, USA

    A. Banerji, M. Bagley, M. Elk, E. Pilgrim, J. Martinson & J. Santo Domingo

Authors
  1. A. Banerji
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Bagley
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Elk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. Pilgrim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Martinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. Santo Domingo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Santo Domingo.

Additional information

Handling editor: Diego Fontaneto

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (TIFF 306 kb) Fig. S1. Rarefaction curve.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Banerji, A., Bagley, M., Elk, M. et al. Spatial and temporal dynamics of a freshwater eukaryotic plankton community revealed via 18S rRNA gene metabarcoding. Hydrobiologia 818, 71–86 (2018). https://doi.org/10.1007/s10750-018-3593-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3593-0

Keywords

Search

Navigation