Understanding the genomic basis of stress adaptation in Picochlorum green algae

Gaining a better understanding of adaptive evolution has become increasingly important to predict the responses of important primary producers in the environment to climate-change driven environmental fluctuations. In my doctoral research, the genomes from four taxa of a naturally robust green algal lineage, Picochlorum (Chlorophyta, Trebouxiphycae) were sequenced to allow a comparative genomic and transcriptomic analysis. The over-arching goal of this work was to investigate environmental adaptations and the origin of haltolerance. Found in environments ranging from brackish estuaries to hypersaline terrestrial environments, this lineage is tolerant of a wide range of fluctuating salinities, light intensities, temperatures, and has a robust photosystem II. The small, reduced diploid genomes (13.4-15.1Mbp) of Picochlorum, indicative of genome specialization to extreme environments, has resulted in an interesting genomic organization, including the clustering of genes in the same biochemical pathway and coregulated genes. Coregulation of co-localized genes in “gene neighborhoods” is more prominent soon after exposure to salinity shock, suggesting a role in the rapid response to salinity stress in Picochlorum. Despite the pressure for genome reduction, key gene gains are seen through gene family expansion of an important SOS1 salt transporter and through bacterium-derived horizontal gene transfer (HGT). Thirteen instance of HGT were identified that display differential acquisition among Picochlorum taxa, indicating an ongoing process in this lineage. The presence of introns, differential expression under salinity shock, and the use of high quality genomes from closely related species provide robust support for the integration of HGT candidates into host nuclear genomes. Transferred genes are potentially functionally relevant and include encoded proteins with roles related to osmolyte production, cell wall metabolism, and metabolic flexibility. A transcriptomic comparison of two sister taxa with very similar genomes, Picochlorum SENEW3 from a brackish lagoon and Picochlorum oklahomensis from a hypersaline salt plain environment was performed under high (1.5 M NaCl) and low salinity (10mM NaCl) shock conditions. This work revealed different regulation responses to salinity shock in terms of osmolyte production, reflecting nitrogen availability in the respective environments, and indicating that the habitat-driven regulation of the existing gene inventory is key to environmental adaptation. These diploid sister taxa also reveal one striking difference between them, levels of haplotype heterozygosity. RNA-seq expression data supports condition-dependent allele-specific gene expression, indicating a functional relevance to maintaining a large divergent allele pool in P. oklahomensis. Overall, Picochlorum has revealed differences in adaptation strategies between seemingly identical species with regard to morphology and gene sequence similarity. My study has provided insights into the adaptive strategies used by eukaryotes with reduced gene inventories that is reflected in selection acting on genome organization, gene regulation, and specialization.