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Genome-enabled dissection of marine diatom ecophysiology

Final Report Summary - DIATOMITE (Genome-enabled dissection of marine diatom ecophysiology)

Diatoms are the most successful group of eukaryotic phytoplankton in the modern ocean. Recently completed whole genome sequences from two species, Thalassiosira pseudonana and Phaeodactylum tricornutum, have revealed a wealth of information about the evolutionary origins and metabolic adaptations that may have led to their ecological success. A major finding is that they have acquired genes both from their endosymbiotic ancestors and by horizontal gene transfer from marine bacteria. This unique melting pot of genes encodes novel capacities for metabolic management, for example allowing the integration of a urea cycle into a photosynthetic cell. The project has built on these previous findings to address the current gap in knowledge about the physiological functions of diatom gene products and about the evolutionary mechanisms that have led to diatom success in contemporary oceans. We have exploited genome-enabled approaches to pioneer a range of unexplored research topics addressing:
1. How has diatom evolution enabled interactions between chloroplasts and mitochondria that have provided diatoms with physiological and metabolic innovations?
We have demonstrated that photosynthesis in diatoms is configured differently to all other photosynthetic organisms studied to date. In particular, exchange of electrons and energy between chloroplasts and mitochondria allow more performant photosynthetic processes. We have also revealed novel aspects of primary metabolism in diatoms, in particular for the utilization of nitrogen and iron, enabled by diatom-specific gene products whose functions have been revealed during the course of this project. We have also defined for the first time the ancient chloroplast proteome of stramenopiles, the deep rooting branch of the eukaryotic tree of life where diatoms are found.
2. What are the relative contributions of DNA sequence variation and epigenetic processes in diatom adaptive dynamics?
We have generated the first epigenome from any stramenopile organism, consisting of genome-wide DNA methylation profiles and eight post-translational histone modifications. In addition to the original genome sequence from the experimental model diatom Phaeodactylum tricornutum reported in 2008, we have generated genome sequences from ten different ecotypes isolated at different times and locations around the world over the last hundred years. From these new resources we have revealed that allele-specific gene expression is a pervasive feature of diploid diatom genomes, which is highly novel with respect to other organisms studied to date, and have revealed a range of genes under positive selection.
As a result of this project we have been able to identify sentinel genes that have driven major physiological and metabolic innovations in diatoms, and have explored the mechanisms that have selected and molded them during diatom evolution. By building new and deeper knowledge about the fundamentals of diatom metabolism, it has emerged that our textbook understanding of carbon and nitrogen metabolism requires revision. Additionally, mechanisms underpinning why diatoms dominate in many contemporary ocean settings have emerged. Our studies have exploited the availability in P. tricornutum of genome and epigenome maps, ecotypes with differential capacities to adapt to different conditions, and distinct morphotypes that can be induced to change shape by ecologically relevant stimuli, as well as powerful reverse genetics techniques such as CRISPR/Cas9 technologies. Our work has further benefited from the Tara Oceans project, which represents the largest DNA sequencing effort ever performed for the oceans. As well as generating the most comprehensive picture to date of plankton ecosystems in the global ocean, we have defined global diatom diversity and abundance patterns, discovered a range of interactions with other organisms, and explored how they are transported by ocean currents and how they influence major biogeochemical processes such as the biological carbon pump. By embracing multiple technologies from cell and molecular biology to oceanography we have crossed multiple scales and have generated significant knowledge about the physiological processes underpinning the success of diatoms in contemporary marine ecosystems.