Oceanomics: Shedding light on genome size reduction dynamics and global distribution of marine photosynthetic picoeukaryotes

Abstract

Despite their reduced cell size (<3 μm), marine Photosynthetic Picoeukaryotes (PPEs) constitute a substantial part of the picophytoplankton biomass production in the open ocean. However, current knowledge about their ecological function and diversity are outstandingly limited, especially compared to prokaryotes. Additionally, the reduced cell size of PPE is matched with a reduction in genome size. The reason for genome size reduction in PPE is unclear but a prerequisite to understating their role in the environment. My dissertation focuses on comparative genomics and metagenomics of PPEs to shed light on their distribution, diversity, metabolomic capacities and their genome size reduction dynamics. Chapter 1 introduces PPEs as rare free-living eukaryotes subsets having undergone genome size reduction, presents an exhaustive literature review regarding their functional diversity, and provides a contextual theoretical framework for the following chapters. Chapters 2 depicts different potential evolutionary forces that shape genome size reduction of PPEs. Here, we carry out an in-depth functional comparative genomics analysis of 16 single-celled photosynthetic algae, based on orthologous genes identification. Consistent with the Black Queen Hypothesis (BQH), pathways involved with soluble metabolites such as amino acids and carotenoids are preferentially lost in PPEs, while biosynthetic pathways involved with insoluble metabolites, such as lipids are preferentially retained. Likewise, a significant positive correlation between proteome size and the number of DNA repair genes, and various genetic information processes was observed, which is consistent with the Proteomic Constraint Hypothesis (PCH). Together, this analysis provides evidence the genome reduction in PPE is adaptive and promoted by natural selection. In chapter 3 (manuscript 2), we have conducted an exhaustive comparative metagenomic analysis of 93 marine metagenomes to unveil the global abundance, diversity relative meta-metabolomic contribution of PPEs to the overall microbial ecosystem. Remarkably, results showed that PPEs represent a minor fraction of the picoplankton assemblages, and negatively correlated with sampling depth. The distribution pattern of PPE taxa was subsequently correlated with vertical, geographical, and environmental components, although most of the PPE assemblage variation (49%) remained unexplained. Finally, in this thesis, we have implemented a comparative metabolomic networks analysis which provides a meaningful understanding of PPE metabolomic capacities at genomic and metagenomic scale.