The Challenges of Reconstructing Tropical Biodiversity With Sedimentary Ancient DNA: A 2200-Year-Long Metagenomic Record From Bwindi Impenetrable Forest, Uganda

René Dommain, Morgan Andama, Molly M. McDonough, Natalia A. Prado, Tobias Goldhammer, Richard Potts, Jesús E. Maldonado, John Bosco Nkurunungi, Michael G. Campana

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25 Scopus citations

Abstract

Sedimentary ancient DNA has been proposed as a key methodology for reconstructing biodiversity over time. Yet, despite the concentration of Earth’s biodiversity in the tropics, this method has rarely been applied in this region. Moreover, the taphonomy of sedimentary DNA, especially in tropical environments, is poorly understood. This study elucidates challenges and opportunities of sedimentary ancient DNA approaches for reconstructing tropical biodiversity. We present shotgun-sequenced metagenomic profiles and DNA degradation patterns from multiple sediment cores from Mubwindi Swamp, located in Bwindi Impenetrable Forest (Uganda), one of the most diverse forests in Africa. We describe the taxonomic composition of the sediments covering the past 2200 years and compare the sedimentary DNA data with a comprehensive set of environmental and sedimentological parameters to unravel the conditions of DNA degradation. Consistent with the preservation of authentic ancient DNA in tropical swamp sediments, DNA concentration and mean fragment length declined exponentially with age and depth, while terminal deamination increased with age. DNA preservation patterns cannot be explained by any environmental parameter alone, but age seems to be the primary driver of DNA degradation in the swamp. Besides degradation, the presence of living microbial communities in the sediment also affects DNA quantity. Critically, 92.3% of our metagenomic data of a total 81.8 million unique, merged reads cannot be taxonomically identified due to the absence of genomic references in public databases. Of the remaining 7.7%, most of the data (93.0%) derive from Bacteria and Archaea, whereas only 0–5.8% are from Metazoa and 0–6.9% from Viridiplantae, in part due to unbalanced taxa representation in the reference data. The plant DNA record at ordinal level agrees well with local pollen data but resolves less diversity. Our animal DNA record reveals the presence of 41 native taxa (16 orders) including Afrotheria, Carnivora, and Ruminantia at Bwindi during the past 2200 years. Overall, we observe no decline in taxonomic richness with increasing age suggesting that several-thousand-year-old information on past biodiversity can be retrieved from tropical sediments. However, comprehensive genomic surveys of tropical biota need prioritization for sedimentary DNA to be a viable methodology for future tropical biodiversity studies.

Original languageEnglish (US)
Article number218
JournalFrontiers in Ecology and Evolution
Volume8
DOIs
StatePublished - Jul 10 2020

Bibliographical note

Funding Information:
We acknowledge the LacCore facility for their support in equipment renting, core storage and processing. This research and core export were approved by the Uganda National Council of Science and Technology (Ref. No. NS13ES) and by the Uganda Wildlife Authority (Ref. No. UWA/COD96/05). We are grateful for the support from Lornah Nabukwasi, Jessica Quinta, Lydia Olaka, Casim Umba Tolo, Julius B. Lejju, Matt Tocheri, Bodo Bookhagen, Manfred Strecker, Paul Glaser, and Mark Shapley and from J?rg Gelbrecht, Grit Siegert, Constancia Levertz, Elisabeth Schuette, Sarah Krocker, and Thomas Rossoll of IGB Berlin. At Bwindi we received generous help from the Uganda Wildlife Authority, especially from wardens George Businge, Raymond Kato, Joseph Arinaitwe, and Pontius Ezuma as well as from all staff of the Institute of Tropical Forest Conservation, Chrispino Mugarura, the Uganda Police Force and from many porters at Ruhija. This research was conducted using the Smithsonian Institution High Performance Cluster (SI/HPC): https://doi.org/10.25572/SIHPC. Funding. This material was based upon work supported by the Global Genome Initiative under Grant No. (GGI-Exploratory Science-2016) awarded to RD. This work was financially also supported by Geo.X, the Research Network for Geosciences in Berlin anPotsdam. RD acknowledges a KoUP seed fund from the University of Potsdam for establishing collaboration with Mbarara University of Science and Technology. The Smithsonian Institution (Human Origins Program, National Museum of Natural History and the Smithsonian National Zoological Park and Conservation Biology Institute) supported this research. Elevation data in Figure 1 are based on the TanDEM-X Science DEM granted to RD by the German Space Agency (DLR 2017). We acknowledge the support of the open-access publication fund of the University of Potsdam.

Publisher Copyright:
© Copyright © 2020 Dommain, Andama, McDonough, Prado, Goldhammer and Nkurunungi. At least a portion of this work is authored by Michael G. Campana, Richard Potts and Jesús E. Maldonado on behalf of the U.S. Government and, as regards Drs. Campana, Potts and Maldonado and the U.S. Government are not subject to copyright protection in the United States. Foreign and other copyrights may apply.

Copyright:
Copyright 2020 Elsevier B.V., All rights reserved.

Keywords

  • DNA preservation
  • metagenomic analysis
  • sediment
  • sedimentary ancient DNA
  • shotgun sequencing
  • tropical biodiversity
  • tropical swamp

Continental Scientific Drilling Facility tags

  • DNA

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