Long-read genome sequencing reveals the evolution, diversity, and adaptation of algae

Algae are a diverse group of predominantly photosynthetic eukaryotes that play a crucial role in ecosystems and have significant economic application. Algae, as ancient organisms, are polyphyletic and do not share a common ancestor across multiple branches of the tree of life. Most algae are ecologically important phytoplankton as primary producers. However, some algae can become heterotrophic or obligate parasitic, and even harmful by causing protothecosis or producing toxins that lead to harmful algal blooms (HABs). Genome sequencing is the most effective approach for enhancing our understanding of the extensive diversity and evolutionary mechanisms that have occurred in algae. In this PhD thesis, I have employed 11 algal genomes to comprehensively investigate the evolutionary dynamics, diversity patterns, and adaptive mechanisms of algae by integrating available genomic data.
My PhD thesis investigates three distinct clades of algae: 1) Five diatom species were sequenced using long reads, demonstrating their specific evolutionary patterns, high diversity, and successful ecological adaptations. The pelagic diatom Pleurosigma pacificum exhibits the largest genome size, the lowest GC content, and the highest percentage of Horizontal Gene Transfer (HGT) percentage among published diatoms. The expansion of chlorophyll a/c proteins most likely facilitates the adaptation of P. pacificum to high light conditions in pelagic environments. The extreme diversity and functional diversification of diatom genomes are primarily driven by long terminal repeats (LTR) retrotransposons. In comparison to other algae, diatoms exhibit a significantly higher abundance of InterPro domains, including heat shock factor, helicase-associated proteins, silicon transporter, sulfotransferase and so on. HGT serves as a common mechanism utilized by diatoms to enhance their adaptive capabilities. 2) The four high quality genomes of genus Prototheca were applied to the study of obligate heterotrophs and pathogenicity. The genetics, pathogenicity, and differentially expressed genes of two newly sequenced strains of P. wickerhamii were identified. In the genus Prototheca, both the nuclear and plastid genomes exhibited a reduction, characterized by the loss of photosynthesis-related genes as well as carotenoid oxygenase and pheophorbide an oxygenase. Malate synthase and isocitrate lyase, which have been horizontally transferred from bacteria, may play a crucial role in carbon and nitrogen metabolism as well as the pathogenicity of Prototheca and non-photosynthetic organisms. 3) Two genomes of harmful algal bloom species Prymnesium parvum displayed high number of polyketide synthase (PKSs) genes. Repeat expanded and horizontal gene transfer may be two contributing factors to the high number of PKS genes found in P. parvum. The expanded gene family analysis revealed the involvement of starch and sucrose metabolism, sulfur metabolism, energy metabolism, and ABC transporters in the evolutionary process of P. parvum.
In a summary, the genome sequences of free-living autotrophic, mixotrophic, heterotrophic, and obligate parasitic and toxic algae reveal their high diversity, specific characteristics, and adaptive traits. These newly sequenced high-quality genomes will serve as valuable resources for ecological, genetic, and toxicological studies, as well as investigations into pathogenicity, horizontal gene transfer, diversity, and evolutionary adaptations of algae.