Is Planktonic Diversity Well Recorded in Sedimentary DNA? Toward the Reconstruction of Past Protistan Diversity
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Studies based on the coupling of a paleolimnological approach and molecular tools (e.g., sequencing of sedimentary DNA) present a promising opportunity to obtain long-term data on past lacustrine biodiversity. However, certain validations are still required, such as the evaluation of DNA preservation in sediments for various planktonic taxa that do not leave any morphological diagnostic features. In this study, we focused on the diversity of planktonic unicellular eukaryotes and verified the presence of their DNA in sediment archives. We compared the molecular inventories (high-throughput sequencing of 18S ribosomal DNA) obtained from monitoring the water column with those obtained for DNA archived in the first 30 cm of sediment. Seventy-one percent of taxonomic units found in the water samples were detected in sediment samples, including pigmented taxa, such as Chlorophyta, Dinophyceae, and Chrysophyceae, phagotrophic taxa, such as Ciliophora, parasitic taxa, such as Apicomplexa and Chytridiomycota, and saprotrophs, such as Cryptomycota. Parallel analysis of 18S ribosomal RNA (rRNA) transcripts revealed the presence of living eukaryotic taxa only in the top 2 cm of sediment; although some limits exist in using RNA/DNA ratio as indicator of microbial activity, these results suggested that the sedimentary DNA mostly represented DNA from past and inactive communities. Only the diversity of a few groups, such as Cryptophyta and Haptophyta, seemed to be poorly preserved in sediments. Our overall results showed that the application of sequencing techniques to sedimentary DNA could be used to reconstruct past diversity for numerous planktonic eukaryotic groups.
KeywordsPaleolimnology Sedimentary DNA Protists Plankton 454 sequencing
For financial support, we thank the EC2CO INSU program (France), who supported the program “REPLAY” and INRA EFPA, who supported the program “CADILAC.” We also benefited from the database on deep peri-alpine lakes observations (SOERE OLA; © SOERE OLA-IS, INRA Thonon-les-Bains, CISALB, Eco-Informatique ORE de l’INRA) and support from ALLENVI for DNA monitoring in lakes. For their technical help in the field, we thank the EDYTEM (CNRS) staff who participated in the sediment coring on Lake Bourget, and P Perney and G Paolini, who performed the water sampling on Lake Bourget. C. Chardon, L. Jacas and B. Leberre brought their technical support for molecular analyses. We thank the Région Rhône-Alpes for their financial support of the PhD thesis of E Capo. English language corrections were performed using the “English Language Editing” Elsevier service and American Manuscript Editors. We are grateful for the useful comments and suggestions from two anonymous reviewers.
Conflict of Interest
The authors declare no conflicts of interest.
- 2.Richards TA, Vepritskiy AA, Gouliamova DE, Nierzwicki-Bauer SA (2005) The molecular diversity of freshwater picoeukaryotes from an oligotrophic lake reveals diverse, distinctive and globally dispersed lineages. Environ Microbiol 7:1413–1425. doi: 10.1111/j.1462-2920.2005.00828.x CrossRefPubMedGoogle Scholar
- 4.Mangot JF, Lepère C, Bouvier C, Debroas D, Domaizon I (2009) Community structure and dynamics of small eukaryotes targeted by new oligonucleotide probes: new insight into the lacustrine microbial food web. Appl Environ Microbiol 75:6373–6381. doi: 10.1128/AEM.00607-09 PubMedCentralCrossRefPubMedGoogle Scholar
- 8.Logares R, Audic S, Bass D, Bittner L, Boutte C, Christen R, et al., Massana R (2014) Patterns of Rare and Abundant Marine Microbial Eukaryotes. Curr Biol 1–9. doi: 10.1016/j.cub.2014.02.050
- 9.Debroas D, Hugoni M, Domaizon I (2015) Evidence for an active rare biosphere within freshwater protists community. Mol Ecol 24:1236–1247. doi: 10.1111/mec.13116
- 10.Battarbee RW, Carvalho L, Jones VJ, Flower RJ, Cameron NG, Bennion H, Juggins S (2001) Diatoms. In: Smol JP, Last WM, Birks HJB (eds) Tracking environmental change using lake sediments volume 3: terrestrial, algal, and siliceous indicators. Kluwer Academic Publishers, DordrechtGoogle Scholar
- 12.Alric B, Perga ME (2011) Effects of production, sedimentation and taphonomic processes on the composition and size structure of sedimenting cladoceran remains in a large deep subalpine lake: paleo-ecological implications. Hydrobiologia 676:101–116. doi: 10.1007/s10750-011-0868-0 CrossRefGoogle Scholar
- 13.Coolen MJ, Muyzer G, Rijpstra WIC, Schouten S, Volkman JK, Sinninghe-Damsté JS (2004) Combined DNA and lipid analyses of sediments reveal changes in Holocene haptophyte and diatom populations in an Antarctic lake. Earth Planet Sci Lett 223:225–239. doi: 10.1016/j.epsl.2004.04.014 CrossRefGoogle Scholar
- 14.Boere AC, Abbas B, Rijpstra WIC, Versteegh GJM, Volkman JK, Sinninghe-Damsté JS, Coolen MJL (2009) Late-Holocene succession of dinoflagellates in an Antarctic fjord using a multi-proxy approach: paleoenvironmental genomics, lipid biomarkers and palynomorphs. Geobiology 7:265–281. doi: 10.1111/j.1472-4669.2009.00202.x CrossRefPubMedGoogle Scholar
- 18.Savichtcheva O, Debroas D, Perga ME, Arnaud F, Villar C, Lyautey E, Kirkham A, Chardon C, Alric B, Domaizon I (2015) Effects of nutrients and warming on Planktothrix dynamics and diversity: a palaeolimnological view based on sedimentary DNA and RNA. Freshw Biol 60(1):31–49. doi: 10.1111/fwb.12465 CrossRefGoogle Scholar
- 28.Shade A, Caporaso JG, Handelsman J, Knight R, Fierer N (2013) A meta-analysis of changes in bacterial and archaeal communities with time. ISME J 71493–1506. doi: 10.1038/ismej.2013.54
- 31.Vergin KL, Beszteri B, Monier A, Thrash JC, Temperton B, Treusch AH, Giovannoni SJ et al (2013) High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series Study site by phylogenetic placement of pyrosequences. ISME J 7:1322–1332. doi: 10.1038/ismej.2013.32 PubMedCentralCrossRefPubMedGoogle Scholar
- 32.Jenny JP, Arnaud F, Dorioz JM, Giguet-Covex C, Frossard V, Sabatier P, Perga ME et al (2013) A spatiotemporal investigation of varved sediments highlights the dynamics of hypolimnetic hypoxia in a large hard-water lake over the last 150 years. Limnol Oceanogr 58:1395–1408. doi: 10.4319/lo.2013.58.4.1395 Google Scholar
- 34.Hugoni M, Taib N, Debroas D, Domaizon I, Jouan-Dufournel I, Bronner G, Galand PE et al (2013) Structure of the rare archaeal biosphere and seasonal dynamics of active ecotypes in surface coastal waters. Proc Natl Acad Sci U S A 110:6004–6009. doi: 10.1073/pnas.1216863110 PubMedCentralCrossRefPubMedGoogle Scholar
- 40.Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. doi: 10.1093/nar/22.22.4673 PubMedCentralCrossRefPubMedGoogle Scholar
- 44.Nolte V, Pandey RV, Jost S, Medinger R, Ottenwälder B, Boenigk J, Schlötterer C (2010) Contrasting seasonal niche separation between rare and abundant taxa conceals the extent of protist diversity. Mol Ecol 19:2908–2915. doi: 10.1111/j.1365-294X.2010.04669.x PubMedCentralCrossRefPubMedGoogle Scholar
- 57.Billard E, Domaizon I, Tissot N, Arnaud F, Lyautey E (2015) Multi-scale phylogenetic heterogeneity of archaea, bacteria, methanogens and methanotrophs in lake sediments. Hydrobiologia 751:159–173. doi: 10.1007/s10750-015-2184-6