TY - JOUR
T1 - Advancing responsible genomic analyses of ancient mollusc shells
AU - Martin-Roy, Raphaël
AU - Thyrring, Jakob
AU - Mata, Xavier
AU - Bangsgaard, Pernille
AU - Bennike, Ole
AU - Christiansen, Gunvor
AU - Funder, Svend
AU - Gotfredsen, Anne Birgitte
AU - Gregersen, Kristian Murphy
AU - Hansen, Camilla Haarby
AU - Ilsøe, Peter Carsten
AU - Klassen, Lutz
AU - Kristensen, Inge Kjær
AU - Ravnholt, Gerd Bindesbøl
AU - Marin, Frédéric
AU - Sarkissian, Clio Der
N1 - Publisher Copyright:
© 2024 Public Library of Science. All rights reserved.
PY - 2024/5
Y1 - 2024/5
N2 - The analysis of the DNA entrapped in ancient shells of molluscs has the potential to shed light on the evolution and ecology of this very diverse phylum. Ancient genomics could help reconstruct the responses of molluscs to past climate change, pollution, and human subsistence practices at unprecedented temporal resolutions. Applications are however still in their infancy, partly due to our limited knowledge of DNA preservation in calcium carbonate shells and the need for optimized methods for responsible genomic data generation. To improve ancient shell genomic analyses, we applied high-throughput DNA sequencing to 27 Mytilus mussel shells dated to ~111–6500 years Before Present, and investigated the impact, on DNA recovery, of shell imaging, DNA extraction protocols and shell sub-sampling strategies. First, we detected no quantitative or qualitative deleterious effect of micro-computed tomography for recording shell 3D morphological information prior to sub-sampling. Then, we showed that double-digestion and bleach treatment of shell powder prior to silica-based DNA extraction improves shell DNA recovery, also suggesting that DNA is protected in preservation niches within ancient shells. Finally, all layers that compose Mytilus shells, i.e., the nacreous (aragonite) and prismatic (calcite) carbonate layers, with or without the outer organic layer (periostracum) proved to be valuable DNA reservoirs, with aragonite appearing as the best substrate for genomic analyses. Our work contributes to the understanding of long-term molecular preservation in biominerals and we anticipate that resulting recommendations will be helpful for future efficient and responsible genomic analyses of ancient mollusc shells.
AB - The analysis of the DNA entrapped in ancient shells of molluscs has the potential to shed light on the evolution and ecology of this very diverse phylum. Ancient genomics could help reconstruct the responses of molluscs to past climate change, pollution, and human subsistence practices at unprecedented temporal resolutions. Applications are however still in their infancy, partly due to our limited knowledge of DNA preservation in calcium carbonate shells and the need for optimized methods for responsible genomic data generation. To improve ancient shell genomic analyses, we applied high-throughput DNA sequencing to 27 Mytilus mussel shells dated to ~111–6500 years Before Present, and investigated the impact, on DNA recovery, of shell imaging, DNA extraction protocols and shell sub-sampling strategies. First, we detected no quantitative or qualitative deleterious effect of micro-computed tomography for recording shell 3D morphological information prior to sub-sampling. Then, we showed that double-digestion and bleach treatment of shell powder prior to silica-based DNA extraction improves shell DNA recovery, also suggesting that DNA is protected in preservation niches within ancient shells. Finally, all layers that compose Mytilus shells, i.e., the nacreous (aragonite) and prismatic (calcite) carbonate layers, with or without the outer organic layer (periostracum) proved to be valuable DNA reservoirs, with aragonite appearing as the best substrate for genomic analyses. Our work contributes to the understanding of long-term molecular preservation in biominerals and we anticipate that resulting recommendations will be helpful for future efficient and responsible genomic analyses of ancient mollusc shells.
UR - http://www.scopus.com/inward/record.url?scp=85192591007&partnerID=8YFLogxK
U2 - 10.1371/journal.pone.0302646
DO - 10.1371/journal.pone.0302646
M3 - Journal article
C2 - 38709766
AN - SCOPUS:85192591007
SN - 1932-6203
VL - 19
JO - PLOS ONE
JF - PLOS ONE
IS - 5 May
M1 - e0302646
ER -