Marine mollusc shells enclose a wealth of information on coastal organisms and their environment. Their life history traits as well as (palaeo-) environmental conditions, including temperature, food availability, salinity and pollution, can be traced through the analysis of their shell (micro-) structure and biogeochemical composition. Adding to this list, the DNA entrapped in shell carbonate biominerals potentially offers a novel and complementary proxy both for reconstructing palaeoenvironments and tracking mollusc evolutionary trajectories. Here, we assess this potential by applying DNA extraction, high-throughput shotgun DNA sequencing and metagenomic analyses to marine mollusc shells spanning the last ~7,000 years. We report successful DNA extraction from shells, including a variety of ancient specimens, and find that DNA recovery is highly dependent on their biomineral structure, carbonate layer preservation and disease state. We demonstrate positive taxonomic identification of mollusc species using a combination of mitochondrial DNA genomes, barcodes, genome-scale data and metagenomic approaches. We also find shell biominerals to contain a diversity of microbial DNA from the marine environment. Finally, we reconstruct genomic sequences of organisms closely related to the Vibrio tapetis bacteria from Manila clam shells previously diagnosed with Brown Ring Disease. Our results reveal marine mollusc shells as novel genetic archives of the past, which opens new perspectives in ancient DNA research, with the potential to reconstruct the evolutionary history of molluscs, microbial communities and pathogens in the face of environmental changes. Other future applications include conservation of endangered mollusc species and aquaculture management.

The shells of marine mollusks represent promising metagenomic archives of the past, adding to bones, teeth, hairs, and environmental samples most commonly examined in ancient DNA research. Seminal work has established that DNA recovery from marine mollusk shells depends on their microstructure, preservation and disease state, and that authentic ancient DNA could be retrieved from specimens as old as 7,000 years. Here, we significantly push the temporal limit for shell DNA recovery to ≥100,000 years with the successful genetic characterization of one Portlandia arctica and one Mytilus mussel sample collected within a dated permafrost layer from the Taimyr Peninsula, Russia. We expand the analysis of ancient DNA in carbonate shells to a larger number of genera (Arctica, Cernuella, Crassostrea, Dreissena, Haliotis, Lymnaea, Margaritifera, Pecten, Ruditapes, Venerupis) from marine, freshwater and terrestrial environments. We demonstrate that DNA from ancient shells can provide sufficient resolution for taxonomic, phylogenetic and/or population assignment. Our results confirm mollusk shells as long-term DNA reservoirs, opening new avenues for the investigation of environmental changes, commercial species management, biological invasion, and extinction. This is especially timely in light of modern threats to biodiversity and ecosystems.

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