Tibetan terrestrial and aquatic ecosystems collapsed with cryosphere loss inferred from sedimentary ancient metagenomics.

Glacier and permafrost shrinkage and land-use intensification threaten mountain wildlife and affect nature conservation strategies. Here, we present paleometagenomic records of terrestrial and aquatic taxa from the southeastern Tibetan Plateau covering the last 18,000 years to help understand the complex alpine ecosystem dynamics. We infer that steppe-meadow became woodland at 14 ka (cal BP) controlled by cryosphere loss, further driving a herbivore change from wild yak to deer. These findings weaken the hypothesis of top-down control by large herbivores in the terrestrial ecosystem. We find a turnover in the aquatic communities at 14 ka, transitioning from glacier-related (blue-green) algae to abundant nonglacier-preferring picocyanobacteria, macrophytes, fish, and otters. There is no evidence for substantial effects of livestock herding in either ecosystem. Using network analysis, we assess the stress-gradient hypothesis and reveal that root hemiparasitic and cushion plants are keystone taxa. With ongoing cryosphere loss, the protection of their habitats is likely to be of conservation benefit on the Tibetan Plateau.

Marine ecosystem shifts with deglacial sea-ice loss inferred from ancient DNA shotgun sequencing.

Sea ice is a key factor for the functioning and services provided by polar marine ecosystems. However, ecosystem responses to sea-ice loss are largely unknown because time-series data are lacking. Here, we use shotgun metagenomics of marine sedimentary ancient DNA off Kamchatka (Western Bering Sea) covering the last ~20,000 years. We traced shifts from a sea ice-adapted late-glacial ecosystem, characterized by diatoms, copepods, and codfish to an ice-free Holocene characterized by cyanobacteria, salmon, and herring. By providing information about marine ecosystem dynamics across a broad taxonomic spectrum, our data show that ancient DNA will be an important new tool in identifying long-term ecosystem responses to climate transitions for improvements of ocean and cryosphere risk assessments. We conclude that continuing sea-ice decline on the northern Bering Sea shelf might impact on carbon export and disrupt benthic food supply and could allow for a northward expansion of salmon and Pacific herring.

Larix species range dynamics in Siberia since the Last Glacial captured from sedimentary ancient DNA.

Climate change is expected to cause major shifts in boreal forests which are in vast areas of Siberia dominated by two species of the deciduous needle tree larch (Larix). The species differ markedly in their ecosystem functions, thus shifts in their respective ranges are of global relevance. However, drivers of species distribution are not well understood, in part because paleoecological data at species level are lacking. This study tracks Larix species distribution in time and space using target enrichment on sedimentary ancient DNA extracts from eight lakes across Siberia. We discovered that Larix sibirica, presently dominating in western Siberia, likely migrated to its northern distribution area only in the Holocene at around 10,000 years before present (ka BP), and had a much wider eastern distribution around 33 ka BP. Samples dated to the Last Glacial Maximum (around 21 ka BP), consistently show genotypes of L. gmelinii. Our results suggest climate as a strong determinant of species distribution in Larix and provide temporal and spatial data for species projection in a changing climate.

Comparative Repeat Profiling of Two Closely Related Conifers (Larix decidua and Larix kaempferi) Reveals High Genome Similarity With Only Few Fast-Evolving Satellite DNAs.

In eukaryotic genomes, cycles of repeat expansion and removal lead to large-scale genomic changes and propel organisms forward in evolution. However, in conifers, active repeat removal is thought to be limited, leading to expansions of their genomes, mostly exceeding 10 giga base pairs. As a result, conifer genomes are largely littered with fragmented and decayed repeats. Here, we aim to investigate how the repeat landscapes of two related conifers have diverged, given the conifers' accumulative genome evolution mode. For this, we applied low-coverage sequencing and read clustering to the genomes of European and Japanese larch, Larix decidua (Lamb.) Carrière and Larix kaempferi (Mill.), that arose from a common ancestor, but are now geographically isolated. We found that both Larix species harbored largely similar repeat landscapes, especially regarding the transposable element content. To pin down possible genomic changes, we focused on the repeat class with the fastest sequence turnover: satellite DNAs (satDNAs). Using comparative bioinformatics, Southern, and fluorescent in situ hybridization, we reveal the satDNAs' organizational patterns, their abundances, and chromosomal locations. Four out of the five identified satDNAs are widespread in the Larix genus, with two even present in the more distantly related Pseudotsuga and Abies genera. Unexpectedly, the EulaSat3 family was restricted to L. decidua and absent from L. kaempferi, indicating its evolutionarily young age. Taken together, our results exemplify how the accumulative genome evolution of conifers may limit the overall divergence of repeats after speciation, producing only few repeat-induced genomic novelties.

Holocene chloroplast genetic variation of shrubs (Alnus alnobetula, Betula nana, Salix sp.) at the siberian tundra-taiga ecotone inferred from modern chloroplast genome assembly and sedimentary ancient DNA analyses.

Climate warming alters plant composition and population dynamics of arctic ecosystems. In particular, an increase in relative abundance and cover of deciduous shrub species (shrubification) has been recorded. We inferred genetic variation of common shrub species (Alnus alnobetula, Betula nana, Salix sp.) through time. Chloroplast genomes were assembled from modern plants (n = 15) from the Siberian forest-tundra ecotone. Sedimentary ancient DNA (sedaDNA; n = 4) was retrieved from a lake on the southern Taymyr Peninsula and analyzed by metagenomics shotgun sequencing and a hybridization capture approach. For A. alnobetula, analyses of modern DNA showed low intraspecies genetic variability and a clear geographical structure in haplotype distribution. In contrast, B. nana showed high intraspecies genetic diversity and weak geographical structure. Analyses of sedaDNA revealed a decreasing relative abundance of Alnus since 5,400 cal yr BP, whereas Betula and Salix increased. A comparison between genetic variations identified in modern DNA and sedaDNA showed that Alnus variants were maintained over the last 6,700 years in the Taymyr region. In accordance with modern individuals, the variants retrieved from Betula and Salix sedaDNA showed higher genetic diversity. The success of the hybridization capture in retrieving diverged sequences demonstrates the high potential for future studies of plant biodiversity as well as specific genetic variation on ancient DNA from lake sediments. Overall, our results suggest that shrubification has species-specific trajectories. The low genetic diversity in A. alnobetula suggests a local population recruitment and growth response of the already present communities, whereas the higher genetic variability and lack of geographical structure in B. nana may indicate a recruitment from different populations due to more efficient seed dispersal, increasing the genetic connectivity over long distances.

Hybridization capture of larch (Larix Mill.) chloroplast genomes from sedimentary ancient DNA reveals past changes of Siberian forest.

Siberian larch (Larix Mill.) forests dominate vast areas of northern Russia and contribute important ecosystem services to the world. It is important to understand the past dynamics of larches in order to predict their likely response to a changing climate in the future. Sedimentary ancient DNA extracted from lake sediment cores can serve as archives to study past vegetation. However, the traditional method of studying sedimentary ancient DNA-metabarcoding-focuses on small fragments, which cannot resolve Larix to species level nor allow a detailed study of population dynamics. Here, we use shotgun sequencing and hybridization capture with long-range PCR-generated baits covering the complete Larix chloroplast genome to study Larix populations from a sediment core reaching back to 6700 years from the Taymyr region in northern Siberia. In comparison with shotgun sequencing, hybridization capture results in an increase in taxonomically classified reads by several orders of magnitude and the recovery of complete chloroplast genomes of Larix. Variation in the chloroplast reads corroborates an invasion of Larix gmelinii into the range of Larix sibirica before 6700 years ago. Since then, both species have been present at the site, although larch populations have decreased with only a few trees remaining in what was once a forested area. This study demonstrates for the first time that hybridization capture applied directly to ancient DNA of plants extracted from lake sediments can provide genome-scale information and is a viable tool for studying past genomic changes in populations of single species, irrespective of a preservation as macrofossil.