Planktonic foraminifera-derived environmental DNA extracted from abyssal sediments preserves patterns of plankton macroecology

Abstract

Abstract. Deep-sea sediments constitute a unique archive of ocean change, fueled by a permanent rain of mineral and organic remains from the surface ocean. Until now, paleoecological analyses of this archive have been mostly based on information from taxa leaving fossils. In theory, environmental DNA (eDNA) in the sediment has the potential to provide information on non-fossilized taxa, allowing more comprehensive interpretations of the fossil record. Yet, the process controlling the transport and deposition of eDNA onto the sediment and the extent to which it preserves the features of past oceanic biota remains unknown. Planktonic foraminifera are the ideal taxa to allow an assessment of the eDNA signal modification during deposition because their fossils are well preserved in the sediment and their morphological taxonomy is documented by DNA barcodes. Specifically, we re-analyze foraminiferal-specific metabarcodes from 31 deep-sea sediment samples, which were shown to contain a small fraction of sequences from planktonic foraminifera. We confirm that the largest portion of the metabarcode originates from benthic bottom-dwelling foraminifera, representing the in situ community, but a small portion (< 10 %) of the metabarcodes can be unambiguously assigned to planktonic taxa. These organisms live exclusively in the surface ocean and the recovered barcodes thus represent an allochthonous component deposited with the rain of organic remains from the surface ocean. We take advantage of the planktonic foraminifera portion of the metabarcodes to establish to what extent the structure of the surface ocean biota is preserved in sedimentary eDNA. We show that planktonic foraminifera DNA is preserved in a range of marine sediment types, the composition of the recovered eDNA metabarcode is replicable and that both the similarity structure and the diversity pattern are preserved. Our results suggest that sedimentary eDNA could preserve the ecological structure of the entire pelagic community, including nonfossilized taxa, thus opening new avenues for paleoceanographic and paleoecological studies.

Unveiling the Ecological Applications of Ancient DNA From Mollusk Shells

“…Although earlier studies demonstrated permafrost as one of the best environments for long-term preservation of animal DNA in keratin-and calcium phosphate-based remains, we show here for the first time that permafrost also preserves calcium carbonate-based remains over significant timescales. Past marine diversity was formerly recovered from <43 kyr sediments that yielded DNA from protists, including haptophytes and foraminifera, which are other organisms producing calcium carbonate exoskeletons surviving or dissolving within sediments (Boere et al, 2009;Coolen et al, 2013;Lejzerowicz et al, 2013;Pawłowska et al, 2014;Morard et al, 2017;More et al, 2018;Armbrecht et al, 2019).…”

DNA Metabarcoding of Deep-Sea Sediment Communities Using COI: Community Assessment, Spatio-Temporal Patterns and Comparison with 18S rDNA

“…Moreover, it is important to note that recovering DNA directly from sediments without any sieving allows the inclusion of many micro-eukaryotes poorly represented in the databases, thus diminishing assignment success. Not sieving also means that more organismal traces and extracellular DNA are retained, which has the risk of incorporating non-benthic organisms whose DNA has sunk to the bottom [28,77] or even non-marine DNA. It has been said that the deep-sea sediments constitute an archive of present and past marine biodiversity [78,79].…”

Changes in the composition of marine and sea-ice diatoms derived from sedimentary ancient DNA of the eastern Fram Strait over the past 30 000 years

“…The marine environment is a complex ecosystem in which the distribution of organisms is controlled significantly by abiotic constraints such as sea-surface temperatures (SSTs), salinity, nutrient distribution, light conditions, and sea-ice cover (Cherkasheva et al, 2014;Ibarbalz et al, 2019;Nöthig et al, 2015;Pierella Karlusich et al, 2020). Over the past 30 000 years the subarctic North Atlantic Ocean has been subject to frequent sea-ice expansions and contractions (Müller et al, 2009;Müller and Stein, 2014;Syring et al, 2020;Werner et al, 2013), which are expected to have affected the composition of the regional species pool. Diatoms (Bacillariophyta) are unicellular, siliceous organisms that are photoautotrophic and thrive in the euphotic zone of the ocean.…”

“…Next to microfossil-based reconstructions, the diatom-produced sea-ice proxy IP 25 (a highly branched isoprenoid alkene with 25 carbon atoms; Belt et al, 2007) combined with phytoplankton biomarkers (e.g. brassicasterol, dinosterol; Volkman, 1986) permit semi-quantitative reconstructions of past sea-ice distribution (Belt, 2018;Belt and Müller, 2013;Müller et al, 2009;Müller and Stein, 2014;Stein et al, 2012Stein et al, , 2017. However, diatoms in northern highlatitudinal regions are less silicified and more prone to silica dissolution (Kohly, 1998;Stabell, 1986) compared to diatoms of the southern polar oceans (Harrison and Cota, 1991).…”