Remote deep-ocean sediment (DOS) ecosystems are among the least explored biomes on Earth. Genomic assessments of their biodiversity have failed to separate indigenous benthic organisms from sinking plankton. Here, we compare global-scale eukaryotic DNA metabarcoding datasets (18 S -V9) from abyssal and lower bathyal surficial sediments and euphotic and aphotic ocean pelagic layers to distinguish plankton from benthic diversity in sediment material. Based on 1685 samples collected throughout the world ocean, we show that DOS diversity is at least threefold that in pelagic realms, with nearly two-thirds represented by abundant yet unknown eukaryotes. These benthic communities are spatially structured by ocean basins and particulate organic carbon (POC) flux from the upper ocean. Plankton DNA reaching the DOS originates from abundant species, with maximal deposition at high latitudes. Its seafloor DNA signature predicts variations in POC export from the surface and reveals previously overlooked taxa that may drive the biological carbon pump.

Sedimentary ancient DNA (sedaDNA) offers a novel retrospective approach to reconstructing the history of marine ecosystems over geological timescales. Until now, the biological proxies used to reconstruct paleoceanographic and paleoecological conditions were limited to organisms whose remains are preserved in the fossil record. The development of ancient DNA analysis techniques substantially expands the range of studied taxa, providing a holistic overview of past biodiversity. Future development of marine sedaDNA research is expected to dramatically improve our understanding of how the marine biota responded to changing environmental conditions. However, as an emerging approach, marine sedaDNA holds many challenges, and its ability to recover reliable past biodiversity information needs to be carefully assessed. This review aims to highlight current advances in marine sedaDNA research and to discuss potential methodological pitfalls and limitations.

The abyssal seafloor is a mosaic of highly diverse habitats that represent the least known marine ecosystems on Earth. Some regions enriched in natural resources, such as polymetallic nodules in the Clarion-Clipperton Zone (CCZ), attract much interest because of their huge commercial potential. Since nodule mining will be destructive, baseline data are necessary to measure its impact on benthic communities. Hence, we conducted an environmental DNA and RNA metabarcoding survey of CCZ biodiversity targeting microbial and meiofaunal eukaryotes that are the least known component of the deep-sea benthos. We analyzed two 18S rRNA gene regions targeting eukaryotes with a focus on Foraminifera (37F) and metazoans (V1V2), sequenced from 310 surface-sediment samples from the CCZ and other abyssal regions. Our results confirm huge unknown deep-sea biodiversity. Over 60% of benthic foraminiferal and almost a third of eukaryotic operational taxonomic units (OTUs) could not be assigned to a known taxon. Benthic Foraminifera are more common in CCZ samples than metazoans and dominated by clades that are only known from environmental surveys. The most striking results are the uniqueness of CCZ areas, both datasets being characterized by a high number of OTUs exclusive to the CCZ, as well as greater beta diversity compared to other abyssal regions. The alpha diversity in the CCZ is high and correlated with water depth and terrain complexity. Topography was important at a local scale, with communities at CCZ stations located in depressions more diverse and heterogeneous than those located on slopes. This could result from eDNA accumulation, justifying the interim use of eRNA for more accurate biomonitoring surveys. Our descriptions not only support previous findings and consolidate our general understanding of deep-sea ecosystems, but also provide a data resource inviting further taxon-specific and large-scale modeling studies. We foresee that metabarcoding will be useful for deep-sea biomonitoring efforts to consider the diversity of small taxa, but it must be validated based on ground truthing data or experimental studies.

The Anthropocene is characterized by dramatic ecosystem changes driven by human activities. The impact of these activities can be assessed by different geochemical and paleontological proxies. However, each of these proxies provides only a fragmentary insight into the effects of anthropogenic impacts. It is highly challenging to reconstruct, with a holistic view, the state of the ecosystems from the preindustrial period to the present day, covering all biological components, from prokaryotes to multicellular eukaryotes. Here, we used sedimentary ancient DNA (sedaDNA) archives encompassing all trophic levels of biodiversity to reconstruct the two century-natural history in Bagnoli-Coroglio (Gulf of Pozzuoli, Tyrrhenian Sea), one of the most polluted marine-coastal sites in Europe. The site was characterized by seagrass meadows and high eukaryotic diversity until the beginning of the 20th century. Then, the ecosystem completely changed, with seagrasses and associated fauna as well as diverse groups of planktonic and benthic protists being replaced by low diversity biota dominated by dinophyceans and infaunal metazoan species. The sedaDNA analysis revealed a five-phase evolution of the area, where changes appear as the result of a multi-level cascade effect of impacts associated with industrial activities, urbanization, water circulation and land-use changes. The sedaDNA allowed to infer reference conditions that must be considered when restoration actions are to be implemented.

Environmental DNA (eDNA) metabarcoding of marine sediments has revealed large amounts of sequences assigned to planktonic taxa. How this planktonic eDNA is delivered on the seafloor and preserved in the sediment is not well understood. We address these questions by comparing metabarcoding and microfossil foraminifera assemblages in sediment cores taken off Newfoundland across a strong ecological gradient. We detected planktonic foraminifera eDNA down to 30 cm and observed that the planktonic/benthic amplicon ratio changed with depth. The relative proportion of planktonic foraminiferal amplicons remained low from the surface down to 10 cm, likely due to the presence of DNA from living benthic foraminifera. Below 10 cm, the relative proportion of planktonic foraminifera amplicons rocketed, likely reflecting the higher proportion of planktonic eDNA in the DNA burial flux. In addition, the microfossil and metabarcoding assemblages showed a congruent pattern indicating that planktonic foraminifera eDNA is deposited without substantial lateral advection and preserves regional biogeographical patterns, indicating deposition by a similar mechanism as the foraminiferal shells. Our study shows that the planktonic eDNA preserved in marine sediments has the potential to record climatic and biotic changes in the pelagic community with the same spatial and temporal resolution as microfossils.