Illuminating the Hawaiian Mesophotic Red Blades: Genomic Insights Uncover Novel Biodiversity and Genomic Novelties in the Evolution of Rhodophyta Associated with the Hawaiian Mesophotic Ecosystems

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2024

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Red algae, or Rhodophyta, play a central role in Hawaiian culture, ecology, and economy. Hawai‘i’s marine research community is deeply committed to scientific exploration, venturing into the lesser-explored twilight reefs known as Mesophotic Ecosystems (MEs), which range from 30 to 150 m in depth. Within these ecosystems, red blades extensively colonize the seafloor, spanning from the sunlit shallows to the light-limited mesophotic zones. Despite the critical roles played by red algae, their biodiversity and evolutionary history remain largely obscured, representing a significant gap in our understanding of Hawaiian marine ecosystems. In response, Chapter 1 of this dissertation undertakes a comprehensive exploration into the mesophotic red blades of Hawai‘i focusing on the orders Gigartinales and Halymeniales, employing a multifaceted approach that integrates morphology, phylogenetics, geography, and environmental factors. This study uncovers the Hawaiian mesophotic reefs as vibrant biodiversity hotspots with distinct floral communities, challenging prevailing assumptions about deep reef refugia and highlighting the vulnerability of these ecosystems. A landmark achievement is the description of four novel species within the genus Croisettea (C. kalaukapuae sp. nov., C. haukoaweo sp. nov., C. ohelouliuli sp. nov. and C. pakualapa sp. nov.), each given culturally resonant Hawaiian names, symbolizing their endemism and cultural significance. This taxonomic breakthrough not only enhances our understanding of red blade diversity thriving in the mesophotic depths but also serves as a critical step towards their conservation and preservation. Chapter 2 of the dissertation employs a taxogenomic approach, utilizing cutting-edge Next-Generation Sequencing (NGS) technologies, advanced computational models, and cyberinfrastructure to reconstruct complete organellar genomes of red blades. This endeavor includes phylogenomic and comparative genomic analyses. The culmination of this study is expressed through two manuscripts, identifying not only a new species (Amalthea mahilanii sp. nov.) but also introducing a new genus (Anunuuluaehu liula gen. et. sp. nov.) to our understanding of red blades. The insights gained shed light on the structural and evolutionary dynamics of red algal organelles, highlighting intriguing phenomena such as genome expansion and fungal-algal associations facilitated by introns. In Chapter 3 of this dissertation, I embarked on an exploratory survey to delve into the structural complexities within the mitochondrial genomes of the order Halymeniales. Contrary to the conventional belief of a 'master circle' structure for mitochondrial DNA in Rhodophyta, this investigation unveiled a diverse array of structures within the mitochondrial genomes of Halymeniales. These structures include circular, tripartite, stem-loop, and linear forms, marking a significant breakthrough in our understanding of mitogenomic diversity within Rhodophyta. This discovery also hints at intriguing possibilities, such as genetic recombination events that may have contributed to the emergence of subgenomic forms. In summary, this dissertation represents a significant leap forward in our understanding of Hawaiian red algae, uncovering new species, expanding genomic resources, and shedding light on the structural complexities of organelle genomes. These findings not only advance scientific knowledge but also have profound implications for the conservation and management of Hawai‘i’s marine ecosystems.

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Molecular biology, Bioinformatics, Evolution & development, bioinformatics, Gigartinales, Halymeniales, NGS, systematics, taxonomy

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252 pages

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