Functional genomics analysis reveals the biosynthesis pathways of important cellular components (alginate and fucoidan) of Saccharina

Although alginate and fucoidan are unique cellular components and have important biological significance in brown algae, and many possible involved genes are present in brown algal genomes, their functions and regulatory mechanisms have not been fully revealed. Both polysaccharides may play important roles in the evolution of multicellular brown algae, but specific and in-depth studies are still limited. In this study, a functional genomics analysis of alginate and fucoidan biosynthesis routes was conducted in Saccharina, and the key events in these pathways in brown algae were identified. First, genes from different sources, including eukaryotic hosts via endosymbiotic gene transfer and bacteria via horizontal gene transfer, were combined to build a complete pathway framework. Then, a critical event occurred to drive these pathways to have real function: one of the mannose-6-phosphate isomerase homologs that arose by gene duplication subsequently adopted the function of the mannose-1-phosphate guanylyltransferase (MGP) gene, which was absent in algal genomes. Further, downstream pathway genes proceeded with gene expansions and complex transcriptional mechanisms, which may be conducive to the synthesis of alginate and fucoidan with diverse structures and contents depending on the developmental stage, tissue structure, and environmental conditions. This study revealed the alginate and fucoidan synthesis pathways and all included genes from separate phylogenetic sources in brown algae. Enzyme assays confirmed the function of key genes and led to the determination of a substitute for the missing MPG. All gene families had constitutively expressed member(s) to maintain the basic synthesis; and the gene function differentiation, enzyme characterization and gene expression regulation differences separated brown algae from other algae lineages and were considered to be the major driving forces for sophisticated system evolution of brown algae.