Comparative and evolutionary analyses of algal genomes reveal their adaptive evolution

As the primary producers of oxygen on earth, algae contribute up to 70 percent of oxygen, with green algae and diatoms being the main contributors. Algae are a very diverse group of organisms, ranging in form from single-cell algae to macroscopic algae. It is also imperative to note that algae occupy a very diverse range of habitats. They can be found in marine environments, fresh water lakes, ponds and streams, as well as on and in soil, rocks, ice. However, it has always remained a mystery how algal species have evolved to colonize aquatic and terrestrial environments. With the help of multi-omics data such as genomes, transcriptomes, and metabolomes, I have investigated the adaptive evolution of algae in this PhD thesis.

I have focused on four clades of algae in this thesis. 1) We found a novel phylum within green plants (Viridiplantae), the Prasinodermophyta, that diverged before the split of Chlorophyta and Streptophyta based on analyses of genome-wide data, transcriptome data, and ribosomal DNA data for the unicellular marine plankton Prasinoderma coloniale. In addition, we found some evidence of adaptive evolution based on bioinformatic approaches. This included a significant expansion of LHC (light-harvesting complex) proteins, more efficient carbon fixation mechanisms, and bacterial cell walls, which represent a result of long-term adaptation to low light, nutrient-deprived habitats (deep sea). 2) On the basis of genome-wide data collected from the unicellular freshwater green alga Pedinomonas minor, we identified a large number of horizontal gene transfer events and, most notably, 70 regions with suspected viral origins. We also found evidence of adaptive evolution, including the significant expansion of thermophilic proteases and heat shock factor compared to relatively species. In addition, genes associated with N-Glycan biosynthesis and fatty acid biosynthesis were upregulated in response to abiotic stresses. It has been hypothesized that these characteristics may be a result of P. minor's adaptation to terrestrial environments with droughts and high temperatures. 3) Using genomic data, transcriptomic data, and methylation data for the green algae Chaetophorales, this thesis identified a high number of methylations throughout the genome. There are a large number of genes associated with nucleotide-binding leucine-rich repeat families (NLRs) that are rarely found in other algae. The results may be explained as a result of Chaetophorales adapting to terrestrial/semi-terrestrial habitats for survival, in which they may have to face a significant number of pathogens as well as more threats from biotic and abiotic stress. 4) In regards to the unicellular centric diatom Conticribra weissflogii, we identified the existence of unique carbon-concentrating mechanisms and chitin metabolic processes。We also identified the unique chitin synthase of the central diatom, which may provide appropriate evidence to distinguish the centric diatom from the pennate diatom.

As a summary, this PhD thesis investigates the relationship between genes and environments using genomic and transcriptomic sequencing data of several algal species by phylogenetic and comparative genomics analyses. In light of these findings, we now have an important genetic resource to investigate the adaptive evolution of algae, setting a solid foundation for future research and illuminating the dawn of genomics research.