Microbial Ecology

, Volume 70, Issue 4, pp 865–875 | Cite as

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

  • Eric Capo
  • Didier Debroas
  • Fabien Arnaud
  • Isabelle Domaizon
Microbiology of Aquatic Systems

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.

Keywords

Paleolimnology Sedimentary DNA Protists Plankton 454 sequencing 

Supplementary material

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References

  1. 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 CrossRefPubMedGoogle Scholar
  2. 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
  3. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  4. 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
  5. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  6. 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 CrossRefPubMedGoogle Scholar
  7. 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 CrossRefPubMedGoogle Scholar
  8. 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. 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. 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
  11. 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 CrossRefGoogle Scholar
  12. 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. 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. 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
  15. 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 CrossRefPubMedGoogle Scholar
  16. 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 CrossRefPubMedGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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
  19. 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 CrossRefPubMedGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  22. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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 CrossRefPubMedGoogle Scholar
  26. 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 CrossRefPubMedGoogle Scholar
  27. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  28. 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. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  30. 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 CrossRefPubMedGoogle Scholar
  31. 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. 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
  33. 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 CrossRefGoogle Scholar
  34. 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
  35. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  36. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  37. 37.
    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461 CrossRefPubMedGoogle Scholar
  38. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  39. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  40. 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
  41. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  42. 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 CrossRefPubMedGoogle Scholar
  43. 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 CrossRefPubMedGoogle Scholar
  44. 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
  45. 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 CrossRefPubMedGoogle Scholar
  46. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  47. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  48. 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 CrossRefPubMedGoogle Scholar
  49. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  50. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 CrossRefGoogle Scholar
  53. 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 CrossRefGoogle Scholar
  54. 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 CrossRefGoogle Scholar
  55. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  56. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  57. 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. 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 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Eric Capo
    • 1
    • 2
  • Didier Debroas
    • 3
  • Fabien Arnaud
    • 4
  • Isabelle Domaizon
    • 1
  1. 1.INRA, UMR 42 CARRTELThonon-les-bains CedexFrance
  2. 2.Université Savoie Mont Blanc, UMR 42 CARRTELLe Bourget du LacFrance
  3. 3.Clermont Université, Université Blaise Pascal, CNRS, UMR 6023 LMGEAubièreFrance
  4. 4.CNRS, UMR 5204 EDYTEMUniversité Savoie Mont BlancLe Bourget du Lac CedexFrance

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