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Untangling eco-evolutionary impacts on diatom genomes over timescales relevant to current climate change

Periodic Reporting for period 3 - DIATOMIC (Untangling eco-evolutionary impacts on diatom genomes over timescales relevant to current climate change)

Reporting period: 2022-11-01 to 2024-04-30

Diatoms are major contributors of primary production in the ocean and participate in carbon sequestration over geologically relevant timescales. As key components of the Earth’s carbon cycle and marine food webs we need to understand the eco-evolutionary underpinnings of their ecological success to forecast their fate in a future ocean impacted by anthropogenic change. Genomes and epigenomes from model diatoms, as well as hundreds of transcriptomes from multiple species, have revealed genetic and epigenetic processes regulating gene expression in response to changing environments. The Tara Oceans survey has in parallel generated resources to explore diatom abundance, diversity and gene expression in the world’s ocean in widely contrasting conditions. DIATOMIC is building on these resources to understand how evolutionary and ecological processes combine to influence diatom adaptations to their environment at unprecedented spatiotemporal scales. To examine these processes over timescales relevant to current climate change, DIATOMIC includes the pioneering exploration of ancient diatom DNA from the sub-seafloor to reveal the genetic and epigenetic bases of speciation and adaptation that have impacted their ecological success during the last 100,000 years, when Earth experienced major climatological events and an increase in anthropogenic impacts. As a model for exploring eco-evolutionary processes in the past and contemporary ocean we are focusing primarily on Chaetoceros because this diatom genus is ancient, ubiquitous, abundant and contributes significantly to carbon export. Key findings are additionally being supported by lab-based studies using the diatom Phaeodactylum for which exemplar molecular tools exist. Specifically, the project is addressing:
1. What molecular features characterize genome evolution in diatoms?
2. Which processes determine diatom metapopulation structure?
3. What can ancient DNA tell us about diatom adaptations to environmental change in the past?
During the first half of the project we have disentangled the evolutionary origins of diatom genes, in particular defining those derived from the original endosymbiotic partners of diatoms and related organisms, as well as from stochastic horizontal gene transfer from other organisms during diatom evolution (Dorrell et al. 2021). Many of the latter encode secreted proteins, and we propose that remodelling of the secretome by horizontally acquired genes may be a central paradigm in eukaryotic cell evolution. In parallel, we have used the remarkable new resource comprising metagenome-assembled genomes (MAGs) from eukaryotes generated by our colleagues at Genoscope (Delmont et al. 2022) to explore diatom genome structure, in particular from Chaetoceros species. The Chaetoceros genus is the most abundant in the global ocean (Pierella Karlusich et al. 2020), so our work has enabled a detailed study of population genomic structure, in particular in the Arctic Ocean. Finally, we have established protocols for analysis of ancient DNA from diatoms in marine sediments (Armbrecht et al. 2021). We have also identified a set of sediment cores, notably from Arctic and Antarctic, and are now using them to explore changes in diatom populations in response to climatic changes over the past 100,000 years.
Accomplishments to date include the generation and characterization of metagenome-assembled genomes (MAGs) from diatoms, including one giant 3 gigabase MAG from the Antarctic diatom Odontella weissflogii (Delmont et al. 2022). These MAGs are now being used for population genomics, aiming to understand mechanisms of molecular evolution underpinning adaptive mechanisms in diatoms. A second accomplishment has been our progress in defining the evolutionary origins of diatom genes, in particular those derived from the endosymbiotic partners at the origin of diatom evolution, and those derived from horizontal gene transfer from other organisms, notably bacteria (Dorrell et al. 2021). Finally, we have established protocols for analysis of ancient DNA from diatoms in marine sediments up to 15,000 years old (Armbrecht et al. 2021). These will be deployed on a set of sediment cores that cover the last 10,000-100,000 years during the remaining duration of the project.