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Journal of Paleolimnology

, Volume 62, Issue 4, pp 425–441 | Cite as

DNA metabarcoding reveals modern and past eukaryotic communities in a high-mountain peat bog system

  • Sandra Garcés-PastorEmail author
  • Owen S. Wangensteen
  • Aaron Pérez-Haase
  • Albert Pèlachs
  • Ramon Pérez-Obiol
  • Núria Cañellas-Boltà
  • Stefano Mariani
  • Teresa Vegas-Vilarrúbia
Original paper

Abstract

Peat bogs located in high mountains are suitable places to study local environmental responses to climate variability. These ecosystems host a large number of eukaryotes with diverse taxonomic and functional diversity. We carried out a metabarcoding study using universal 18S and COI markers to explore the composition of past and present eukaryotic communities of a Pyrenean peat bog ecosystem. We assessed the molecular biodiversity of four different moss micro-habitats along a flood gradient in the lentic Bassa Nera system (Central Pyrenees). Five samples collected from different sediment depths at the same study site were also analysed, to test the suitability of these universal markers for studying paleoecological communities recovered from ancient DNA and to compare the detected DNA sequences to those obtained from the modern community. We also compared the information provided by the sedimentary DNA to the reconstruction from environmental proxies such as pollen and macro-remains from the same record. We successfully amplified ancient DNA with both universal markers from all sediment samples, including the deepest one (~ 10,000 years old). Most of the metabarcoding reads obtained from sediment samples, however, were assigned to living edaphic organisms and only a small fraction of those reads was considered to be derived from paleoecological communities. Inferences from ancient sedimentary DNA were complementary to the reconstruction based on pollen and macro-remains, and the combined records reveal more detailed information. This molecular study yielded promising findings regarding the diversity of modern eukaryotic peat bog communities. Nevertheless, even though information about past communities could be retrieved from sediment samples, preferential amplification of DNA from living communities is a caveat for the use of universal metabarcoding markers in paleoecology.

Keywords

Sedimentary DNA Community DNA Peat bog paleoecology Eukaryotes Pyrenees 

Notes

Acknowledgements

We thank Professor Xavier Turon for providing us with the 18S primers. We are indebted to Editor Mark Brenner and to three anonymous reviewers for their suggestions, which contributed to improvement upon earlier versions of this manuscript.

Supplementary material

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References

  1. Alsos IG, Lammers Y, Yoccoz NG, Jørgensen T, Sjögren P, Gielly L, Edwards ME (2018) Plant DNA metabarcoding of lake sediments: how does it represent the contemporary vegetation. PLoS ONE 13(4):e0195403Google Scholar
  2. Andersen R, Chapman S, Artz R (2013) Microbial communities in natural and disturbed peatlands: a review. Soil Biol Biochem 57:979–994.  https://doi.org/10.1016/j.soilbio.2012.10.003 CrossRefGoogle Scholar
  3. Anderson-Carpenter L (2011) Ancient DNA from lake sediments: bridging the gap between paleoecology and genetics. BMC Evol Biol 11:30Google Scholar
  4. Anslan S, Tedersoo L (2015) Performance of cytochrome c oxidase subunit I (COI), ribosomal DNA large subunit (LSU) and Internal Transcribed Spacer 2 (ITS2) in DNA barcoding of Collembola. Eur J Soil Biol 69:1–7Google Scholar
  5. Asemaninejad A, Thorn R, Lindo Z (2017) Vertical distribution of fungi in hollows and hummocks of boreal peatlands. Fungal Ecol 27:59–68Google Scholar
  6. Bellemain E, Davey ML, Kauserud H, Epp LS, Boessenkool S, Coissac E, Gemi J, Edwards M, Willersley E, Gussarova G, Taberlet P, Haile J, Brochmann C (2013) Fungal palaeodiversity revealed using high-throughput metabarcoding of ancient DNA from arctic permafrost. Environ Microbiol 15:1176–1189Google Scholar
  7. Boyer F, Mercier C, Bonin A, Le Bras Y, Taberlet P, Coissac E (2016) obitools: a unix-inspired software package for DNA metabarcoding. Mol Ecol 16(1):176–182Google Scholar
  8. Cambra J (2015) Micro-scale distribution of algae in a Pyrenean peat-bog, Spain. Hidrobiológica 25:213–222Google Scholar
  9. Cañellas-Boltà N, Rull V, Vigo J, Mercadé A (2009) Modern pollen-vegetation relationships along an altitudinal transect in the central Pyrenees (southwestern Europe). Holocene 19:1185–1200Google Scholar
  10. Capo E, Debroas D, Arnaud F, Domaizon I (2015) Is planktonic diversity well recorded in sedimentary DNA? Toward the reconstruction of past protistan diversity. Microb Ecol 70:865–875Google Scholar
  11. Capo E, Debroas D, Arnaud F, Guillemot T, Bichet V, Millet L, Lejzerowicz F (2016) Long-term dynamics in microbial eukaryotes communities: a palaeolimnological view based on sedimentary DNA. Mol Ecol 25:5925–5943Google Scholar
  12. Capo E, Debroas D, Arnaud F, Perga ME, Chardon C, Domaizon I (2017) Tracking a century of changes in microbial eukaryotic diversity in lakes driven by nutrient enrichment and climate warming. Environ Microbiol 19:2873–2892Google Scholar
  13. Carrillo E, Brugués M, Carreras J, Cros RM, Ferré A, Ninot JM, Pérez-Haase A, Ruiz E (2008) Singularitat de la vegetació de les reserves integrals de Trescuro i d’Aiguamòg. In: Jornades sobre recerca al Parc Nacional d’Aigüestortes i Estany de Sant Maurici. 25–27 October. Vall de Boí, Barruera, pp 177–192Google Scholar
  14. Charman D (2002) Peatlands and environmental change. Wiley, ChichesterGoogle Scholar
  15. Coolen MJ, Shtereva G (2009) Vertical distribution of metabolically active eukaryotes in the water column and sediments of the Black Sea. FEMS Microbiol Ecol 70:525–539Google Scholar
  16. Domaizon I, Winegardner A, Capo E, Gauthier J, Gregory-Eaves I (2017) DNA-based methods in paleolimnology: new opportunities for investigating long-term dynamics of lacustrine biodiversity. J Paleolimnol 58:1–21Google Scholar
  17. Ellison AM (2006) Nutrient limitation and stoichiometry of carnivorous plants. Plant Biol 8:740–747Google Scholar
  18. Epp LS, Boessenkool S, Bellemain EP, Haile J, Esposito A, Riaz T, Erseus C, Gusarov VI, Edwards ME, Johnsen A, Stenøien HK (2012) New environmental metabarcodes for analysing soil DNA: potential for studying past and present ecosystems. Mol Ecol 21:1821–1833Google Scholar
  19. Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176Google Scholar
  20. Garcés-Pastor S, Cañellas-Boltà N, Clavaguera A, Calero MA, Vegas-Vilarrúbia T (2016) Vegetation shifts, human impact and peat bog development in Bassa Nera pond (Central Pyrenees) during the past millennium. Holocene 27:553–565Google Scholar
  21. Garcés-Pastor S, Cañellas-Boltà N, Pèlachs A, Soriano JM, Pérez-Obiol R, Pérez-Haase A, Calero MA, Andreu O, Escolà N, Vegas-Vilarrúbia T (2017) Environmental history and vegetation dynamics in response to climate variations and human pressure during the Holocene in Bassa Nera, Central Pyrenees. Palaeogeogr Palaeocl 479:48–60Google Scholar
  22. Geller J, Meyer C, Parker M, Hawk H (2013) Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Mol Ecol 13:851–861Google Scholar
  23. Godwin H (1981) The archives of the peat bogs. Cambridge University Press, CambridgeGoogle Scholar
  24. Guardiola M, Uriz MJ, Taberlet P, Coissac E, Wangensteen OS, Turon X (2015) Deep-sea, deep-sequencing: metabarcoding extracellular DNA from sediments of marine canyons. PLoS ONE 10:e0139633Google Scholar
  25. Guardiola M, Wangensteen O, Taberlet P, Coissac E (2016) Spatio-temporal monitoring of deep-sea communities using metabarcoding of sediment DNA and RNA. PeerJ 4:e2807Google Scholar
  26. Harder CB, Rønn R, Brejnrod A, Bass D, Al-Soud WA, Ekelund F (2016) Local diversity of heathland Cercozoa explored by in-depth sequencing. ISME J 10:2488Google Scholar
  27. Jersabek C, Brancelj A, Stoch F, Schabetsberger R (2001) Distribution and ecology of copepods in mountainous regions of the Eastern Alps. Hydrobiologia 453:309–324Google Scholar
  28. Jørgensen T, Haile J, Möller P, Andreev A (2012) A comparative study of ancient sedimentary DNA, pollen and macrofossils from permafrost sediments of northern Siberia reveals long-term vegetational stability. Mol Ecol 21:1989–2003Google Scholar
  29. Lejzerowicz F, Esling P, Majewski W, Szczucinski W, Decelle J, Obadia C, Martines Arbizu P, Pawlowski J (2013a) Ancient DNA complements microfossil record in deepsea subsurface sediments. Biol Lett 9:20130283.  https://doi.org/10.1098/rsbl.2013.0283 CrossRefGoogle Scholar
  30. Lejzerowicz F, Voltsky I, Pawlowski J (2013b) Identifying active foraminifera in the Sea of Japan using metatranscriptomic approach. Deep Sea Res Part II 86:214–220Google Scholar
  31. Mann M (2002) The value of multiple proxies. Science 297:1481–1482Google Scholar
  32. Mauquoy D, Hughes P, van Geel B (2010) A protocol for plant macrofossil analysis of peat deposits. Mires Peat 7:1–5Google Scholar
  33. Moore PD, Webb JA, Collinson ME (1991) Pollen analysis. Blackwell, OxfordGoogle Scholar
  34. Múrria C, Väisänen LOS, Somma S, Wangensteen OS, Arnedo MA, Prat N (2019) Towards an Iberian DNA barcode reference library of freshwater macroinvertebrates and fishes. Limnetica (in press)Google Scholar
  35. Ninyerola M, Pons X, Roure JM (2003) Atles Climàtic Digital de Catalunya. Universitat Autònoma de Barcelona, BarcelonaGoogle Scholar
  36. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2018) vegan: community ecology package. R package version 2.5-3Google Scholar
  37. Pääbo S, Poinar H, Serre D, Jaenicke-Després V, Hebler J, Rohland N, Hofreiter M (2004) Genetic analyses from ancient DNA. Annu Rev Genet 38:645–679Google Scholar
  38. Pansu J, Giguet-Covex C, Ficetola G, Gielly L, Boyer F, Zinger L, Choler P (2015) Reconstructing long-term human impacts on plant communities: an ecological approach based on lake sediment DNA. Mol Ecol 24:1485–1498Google Scholar
  39. Parducci L, Väliranta M, Salonen JS, Ronkainen T, Matetovici I, Fontana SL, Eskola T, Sarala P, Suyama Y (2015) Proxy comparison in ancient peat sediments: pollen, macrofossil and plant DNA. Philos Trans R Soc B 370:20130382Google Scholar
  40. Parducci L, Bennett K, Ficetola G, Alsos I, Suyama Y, Wood JR, Pedersen MW (2017) Ancient plant DNA in lake sediments. New Phytol 214:924–942Google Scholar
  41. Pawlowski J, Holzmann M (2014) A plea for DNA barcoding of foraminifera. J Foramin Res 44:62–67Google Scholar
  42. Pawlowski J, Esling P, Lejzerowicz F, Cedhagen T, Wilding TA (2014) Environmental monitoring through protist next-generation sequencing metabarcoding: assessing the impact of fish farming on benthic foraminifera communities. Mol Ecol 14:1129–1140Google Scholar
  43. Pedersen M, Ginolhac A, Orlando L, Olsen J, Andersen K, Holm J, Kjær KH (2013) A comparative study of ancient environmental DNA to pollen and macrofossils from lake sediments reveals taxonomic overlap and additional plant taxa. Quat Sci Rev 75:161–168Google Scholar
  44. Pèlachs A, Pérez-Obiol R, Soriano JM, Pérez-Haase A (2016) Dinàmica de la vegetació, contaminació ambiental i incendis durant els últims 10.000 anys a la Bassa Nera (Val d’Aran). X Jornades sobre Recerca al Parc Nacional d’Aigüestortes i Estany de Sant Maurici. Vall de Boí, Barruera, pp 75–87Google Scholar
  45. Pérez-Haase A, Ninot JM (2006) Caracterització florística i ecològica de les molleres de la Nassa Nera (Aiguamòg). VII Jornades sobre Recerca al Parc Nacional d’Aigüestortes i Estany de Sant Maurici, Generalitat de Catalunya, Barcelona, pp 193–213Google Scholar
  46. Pérez-Haase A, Ninot JM (2017) Hydrological heterogeneity rather than water chemistry explain high plant diversity and uniqueness of a Pyrenean mixed mire. Folia Geobot 1:18Google Scholar
  47. Pérez-Haase A, Ortuño E, Ninot JM (2010) Diversitat de comunitats vegetals a les molleres de la Vall d’Aran (Pirineus centrals). Acta Bot Barc 53:61–112Google Scholar
  48. Siegenthaler A, Wangensteen OS, Benvenuto C, Campos J, Mariani S (2019) DNA metabarcoding unveils multiscale trophic variation in a widespread coastal opportunist. Mol Ecol 28:232–249Google Scholar
  49. Singer D, Lara E, Steciow MM, Seppey CV, Paredes N, Pillonel A, Oskazo T, Belbahri L (2016) High-throughput sequencing reveals diverse oomycete communities in oligotrophic peat bog micro-habitat. Fungal Ecol 23:42–47Google Scholar
  50. Singer G, Fahner NA, Barnes J, McCarthy A, Hajibabaei M (2019) Comprehensive biodiversity analysis via ultra-deep patterned flow cell technology: a case study of eDNA metabarcoding seawater. Sci Rep 9:5991Google Scholar
  51. Smol JP, Birks HJB, Last WM (2001) Tracking environmental change using lake sediments. Volume 3: terrestrial, algal and siliceous indicators, developments in paleoenvironmental research. Kluwer Academic Publishers, DordrechtGoogle Scholar
  52. Taberlet P, Coissac E, Pompanon F, Brochmann C, Willerslev E (2012) Towards next-generation biodiversity assessment using DNA metabarcoding. Mol Ecol 21:2045–2050Google Scholar
  53. Tarrats P, Cañedo-Argüelles M, Rieradevall M, Prat N (2017) Chironomid communities as indicators of local and global changes in an oligotrophic high mountain lake (Enol Lake, Northwestern Spain). J Limnol 76:355–365Google Scholar
  54. Thorp J, Covich A (eds) (2009) Ecology and classification of North American freshwater invertebrates. Academic Press, New YorkGoogle Scholar
  55. Torti A, Lever MA, Jørgensen BB (2015) Origin, dynamics, and implications of extracellular DNA pools in marine sediments. Mar Genom 24:185–196Google Scholar
  56. Wangensteen OS, Turon X (2017) Metabarcoding techniques for assessing biodiversity of marine animal forests. In: Rossi S, Bramanti L, Gori A, Orejas C (eds) Marine animal forests, the ecology of benthic biodiversity hotspots. Springer, Cham, pp 445–473Google Scholar
  57. Wangensteen OS, Cebrian E, Palacín C, Turon X (2018a) Under the canopy: community-wide effects of invasive algae in marine protected areas revealed by metabarcoding. Mar Pollut Bull 127:54–66Google Scholar
  58. Wangensteen OS, Palacín C, Guardiola M, Turon X (2018b) DNA metabarcoding of littoral hard-bottom communities: high diversity and database gaps revealed by two molecular markers. PeerJ 6:e4705Google Scholar
  59. Xie C, Lou H (2009) Secondary metabolites in bryophytes: an ecological aspect. Chem Biodivers 6:303–312Google Scholar
  60. Young JM, Weyrich LS, Cooper A (2014) Forensic soil DNA analysis using high-throughput sequencing: a comparison of four molecular markers. Forensic Sci Int Genet 13:176–184Google Scholar
  61. Zhu F, Massana R, Not F (2005) Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene. FEMS Microbiol Ecol 52:79–92Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Sandra Garcés-Pastor
    • 1
    • 2
    Email author
  • Owen S. Wangensteen
    • 3
    • 4
  • Aaron Pérez-Haase
    • 1
    • 5
  • Albert Pèlachs
    • 6
  • Ramon Pérez-Obiol
    • 7
  • Núria Cañellas-Boltà
    • 8
  • Stefano Mariani
    • 3
  • Teresa Vegas-Vilarrúbia
    • 1
  1. 1.Department of Evolutionary Biology, Ecology and Environmental SciencesUniversitat de BarcelonaBarcelonaSpain
  2. 2.Tromsø MuseumUiT The Arctic University of NorwayTromsøNorway
  3. 3.Ecosystems and Environment Research Centre, School of Environment and Life SciencesUniversity of SalfordGreater ManchesterUK
  4. 4.Norwegian College of Fishery ScienceUiT The Arctic University of NorwayTromsøNorway
  5. 5.Center for Advanced Studies of BlanesSpanish Research Council (CEAB-CSIC)BlanesSpain
  6. 6.Department of GeographyUniversitat Autònoma de BarcelonaBellaterraSpain
  7. 7.Botany Unit, Department of Animal Biology, Plant Biology and EcologyUniversitat Autònoma de BarcelonaBellaterraSpain
  8. 8.Institute of Earth Sciences JaumeAlmera (ICTJA-CSIC)BarcelonaSpain

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