Skip to main content
SpringerLink
Log in

Is Planktonic Diversity Well Recorded in Sedimentary DNA? Toward the Reconstruction of Past Protistan Diversity

  • Microbiology of Aquatic Systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  1. Caron DA, Worden AZ, Countway PD, Demir E, Heidelberg KB (2009) Protists are microbes too: a perspective. ISME J 3(1):4–12. doi:10.1038/ismej.2008.101

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  3. Lepère C, Domaizon I, Debroas D (2008) Unexpected importance of potential parasites in the composition of the freshwater small-eukaryote community. Appl Environ Microbiol 74:2940–2949. doi:10.1128/AEM.01156-07

    Article  PubMed Central  PubMed  Google 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM (2009) A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS ONE 4:e6372. doi:10.1371/journal.pone.0006372

    Article  PubMed Central  PubMed  Google Scholar 

  6. Lepère C, Domaizon I, Taïb N, Mangot JF, Bronner G, Boucher D, Debroas D (2013) Geographic distance and ecosystem size determine the distribution of smallest protists in lacustrine ecosystems. FEMS Microbiol Ecol 85:85–94. doi:10.1111/1574-6941.12100

    Article  PubMed  Google Scholar 

  7. Mangot JF, Domaizon I, Taib N, Marouni N, Duffaud E, Bronner G, Debroas D (2013) Short-term dynamics of diversity patterns: evidence of continual reassembly within lacustrine small eukaryotes. Environ Microbiol 15:1745–1758. doi:10.1111/1462-2920.12065

    Article  CAS  PubMed  Google 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, Dordrecht

    Google Scholar 

  11. Millet L, Arnaud F, Heiri O, Magny M, Verneaux V, Desmet M (2009) Late-Holocene summer temperature reconstruction from chironomid assemblages of Lake Anterne, northern French Alps. The Holocene 19:317–328. doi:10.1177/0959683608100576

    Article  Google 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

    Article  Google 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

    Article  CAS  Google 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

    Article  CAS  PubMed  Google Scholar 

  15. Corinaldesi C, Barucca M, Luna GM, Dell’Anno A (2011) Preservation, origin and genetic imprint of extracellular DNA in permanently anoxic deep-sea sediments. Mol Ecol 20:642–654. doi:10.1111/j.1365-294X.2010.04958.x

    Article  CAS  PubMed  Google Scholar 

  16. Stoof-Leichsenring KR, Epp LS, Trauth MH, Tiedemann R (2012) Hidden diversity in diatoms of Kenyan Lake Naivasha: a genetic approach detects temporal variation. Mol Ecol 21:1918–1930. doi:10.1111/j.1365-294X.2011.05412.x

    Article  CAS  PubMed  Google Scholar 

  17. Fernandez-Carazo R, Verleyen E, Hodgson DA, Roberts SJ, Waleron K, Vyverman W, Wilmotte A (2013) Late Holocene changes in cyanobacterial community structure in maritime Antarctic lakes. J Paleolimnol 50:15–31. doi:10.1007/s10933-013-9700-3

    Article  Google 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

    Article  CAS  Google Scholar 

  19. Coolen MJL, Talbot HM, Abbas BA, Ward C, Schouten S, Volkman JK, Damsté JSS (2008) Sources for sedimentary bacteriohopanepolyols as revealed by 16S rDNA stratigraphy. Environ Microbiol 10:1783–1803. doi:10.1111/j.1462-2920.2008.01601.x

    Article  CAS  PubMed  Google Scholar 

  20. Domaizon I, Savichtcheva O, Debroas D, Arnaud F, Villar C, Pignol C, Perga ME et al (2013) DNA from lake sediments reveals the long-term dynamics and diversity of Synechococcus assemblages. Biogeosciences 10:3817–3838. doi:10.5194/bg-10-3817-2013

    Article  Google Scholar 

  21. Pawlowski J, Audic S, Adl S, Bass D, Belbahri L, Berney C, de Vargas C et al (2012) CBOL protist working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLoS Biol 10:e1001419. doi:10.1371/journal.pbio.1001419

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Coolen MJL, Orsi WD, Balkema C, Quince C, Harris K, Sylva SP, Giosan L et al (2013) Evolution of the plankton paleome in the Black Sea from the Deglacial to Anthropocene. Proc Natl Acad Sci U S A 110:8609–8614. doi:10.1073/pnas.1219283110

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Boere AC, Sinninghe Damsté JS, Rijpstra WIC et al (2011) Source-specific variability in post-depositional DNA preservation with potential implications for DNA based paleoecological records. Org Geochem 42:1216–1225. doi:10.1016/j.orggeochem.2011.08.005

    Article  CAS  Google Scholar 

  24. Dell’Anno A, Bompadre S, Danovaro R (2002) Quantification, base composition, and fate of extracellular DNA in marine sediments. Limnol Oceanogr 47:899–905. doi:10.4319/lo.2002.47.3.0899

    Article  Google Scholar 

  25. Corinaldesi C, Beolchini F, Dell’Anno A (2008) Damage and degradation rates of extracellular DNA in marine sediments: implications for the preservation of gene sequences. Mol Ecol 17:3939–3951. doi:10.1111/j.1365-294X.2008.03880

    Article  CAS  PubMed  Google Scholar 

  26. Boere AC, Rijpstra WIC, De Lange GJ, Sinninghe-Damsté JS, Coolen MJL (2011) Preservation potential of ancient plankton DNA in Pleistocene marine sediments. Geobiology 9:377–393. doi:10.1111/j.1472-4669.2011.00290.x

    Article  CAS  PubMed  Google Scholar 

  27. Sogin ML, Morrison HG, Huber JA, Mark-Welch D, Huse SM, Neal PR, Herndl GJ et al (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci U S A 103(32):12115–12120. doi:10.1073/pnas.0605127103

    Article  PubMed Central  CAS  PubMed  Google 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

  29. Taïb N, Mangot JF, Domaizon I, Bronner G, Debroas D (2013) Phylogenetic affiliation of SSU rRNA genes generated by massively parallel sequencing: new insights into the freshwater protist diversity. PLoS ONE 8(3):e58950. doi:10.1371/journal.pone.0058950

    Article  PubMed Central  PubMed  Google Scholar 

  30. Dunthorn M, Otto J, Berger SA, Stamatakis A, Mahé F, Romac S, Stoeck T et al (2014) Placing environmental next-generation sequencing amplicons from microbial eukaryotes into a phylogenetic context. Mol Biol Evol 31:993–1009. doi:10.1093/molbev/msu055

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed Central  CAS  PubMed  Google 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

    CAS  Google Scholar 

  33. Giguet-Covex C, Arnaud F, Poulenard J et al (2009) Sedimentological and geochemical records of past trophic state and hypolimnetic anoxia in large, hard-water Lake Bourget, French Alps. J Paleolimnol 43:171–190. doi:10.1007/s10933-009-9324-9

    Article  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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Giongo A, Crabb DB, Davis-Richardson AG, Chauliac D, Mobberley JM, Gano KA, Triplett EW et al (2010) PANGEA: pipeline for analysis of next generation amplicons. ISME J 4:852–861. doi:10.1038/ismej.2010.16

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi:10.1093/bioinformatics/btr381

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461

    Article  CAS  PubMed  Google Scholar 

  38. Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. doi:10.1371/journal.pone.0009490

    Article  PubMed Central  PubMed  Google Scholar 

  39. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196. doi:10.1093/nar/gkm864

    Article  PubMed Central  CAS  PubMed  Google 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  41. Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506. doi:10.1128/AEM.71.3.1501-1506.2005

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2

    Article  CAS  PubMed  Google Scholar 

  43. Wilhelm L, Besemer K, Fasching C et al (2014) Rare but active taxa contribute to community dynamics of benthic biofilms in glacier-fed streams. Environ Microbiol 16:2514–2524. doi:10.1111/1462-2920.12392

    Article  CAS  PubMed  Google 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Coolen MJL, Shtereva G (2009) Vertical distribution of metabolically active eukaryotes in the water column and sediments of the Black Sea. FEMS Microbiol Ecol 70:525–539. doi:10.1111/j.1574-6941.2009.00756.x

    Article  CAS  PubMed  Google Scholar 

  46. Stoeck T, Kasper J, Bunge J, Leslin C, Ilyin V, Epstein S (2007) Protistan diversity in the Arctic: a case of paleoclimate shaping modern biodiversity? PLoS ONE 2:e728. doi:10.1371/journal.pone.0000728

    Article  PubMed Central  PubMed  Google Scholar 

  47. Blazewicz SJ, Barnard RL, Daly RA, Firestone MK (2013) Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses. ISME J 7:2061–2068. doi:10.1038/ismej.2013.102

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Edgcomb VP, Beaudoin D, Gast R, Biddle JF, Teske A (2011) Marine subsurface eukaryotes: the fungal majority. Environ Microbiol 13:172–183. doi:10.1111/j.1462-2920.2010.02318.x

    Article  CAS  PubMed  Google Scholar 

  49. Orsi W, Biddle JF, Edgcomb V (2013) Deep sequencing of subseafloor eukaryotic rRNA reveals active Fungi across marine subsurface provinces. PLoS ONE 8:e56335. doi:10.1371/journal.pone.0056335

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  50. Chambouvet A, Berney C, Romac S, Audic S, Maguire F, De Vargas C, Richards TA (2014) Diverse molecular signatures for ribosomally “active” Perkinsea in marine sediments. BMC Microbiol 14:110. doi:10.1186/1471-2180-14-110

    Article  PubMed Central  PubMed  Google Scholar 

  51. Fenchel T, Finlay BJ (1991) Synchronous division of an endosymbiotic methanogenic bacterium in the anaerobic ciliate Plagiopyla Frontata Kahl. J Protozool 38:22–28. doi:10.1111/j.1550-7408.1991.tb04790.x

    Article  Google Scholar 

  52. Miyazono A, Nagai S, Kudo I, Tanizawa K (2012) Viability of Alexandrium tamarense cysts in the sediment of Funka Bay, Hokkaido, Japan: over a hundred year survival times for cysts. Harmful Algae 16:81–88. doi:10.1016/j.hal.2012.02.001

    Article  Google Scholar 

  53. Berthon V, Marchetto A, Rimet F et al (2013) Trophic history of French sub-alpine lakes over the last ~150 years: phosphorus reconstruction and assessment of taphonomic biases. J Limnol 72:e34. doi:10.4081/jlimnol.2013.e34

    Article  Google Scholar 

  54. Randlett M-È, Coolen MJL, Stockhecke M et al (2014) Alkenone distribution in Lake Van sediment over the last 270 ka: influence of temperature and haptophyte species composition. Quat Sci Rev 104:53–62. doi:10.1016/j.quascirev.2014.07.009

    Article  Google Scholar 

  55. Barberán A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6:343–351. doi:10.1038/ismej.2011.119

    Article  PubMed Central  PubMed  Google Scholar 

  56. Chow C-ET, Kim DY, Sachdeva R et al (2014) Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists. ISME J 8:816–829. doi:10.1038/ismej.2013.199

    Article  PubMed Central  CAS  PubMed  Google 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

  58. Letunic I, Bork P (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39:475–478. doi:10.1093/nar/gkr201

    Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. INRA, UMR 42 CARRTEL, 74203, Thonon-les-bains Cedex, France

    Eric Capo & Isabelle Domaizon

  2. Université Savoie Mont Blanc, UMR 42 CARRTEL, 73379, Le Bourget du Lac, France

    Eric Capo

  3. Clermont Université, Université Blaise Pascal, CNRS, UMR 6023 LMGE, 63171, Aubière, France

    Didier Debroas

  4. CNRS, UMR 5204 EDYTEM, Université Savoie Mont Blanc, 73379, Le Bourget du Lac Cedex, France

    Fabien Arnaud

Authors
  1. Eric Capo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Didier Debroas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fabien Arnaud
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Isabelle Domaizon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isabelle Domaizon.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 126 kb)

ESM 2

(DOCX 17 kb)

ESM 3

(DOCX 13 kb)

ESM 4

(DOCX 44 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Capo, E., Debroas, D., Arnaud, F. et al. Is Planktonic Diversity Well Recorded in Sedimentary DNA? Toward the Reconstruction of Past Protistan Diversity. Microb Ecol 70, 865–875 (2015). https://doi.org/10.1007/s00248-015-0627-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-015-0627-2

Keywords

Search

Navigation