Significance
Coral reef ecosystems are undergoing significant degradation and reorganization due to ocean warming and acidification. Calcareous algae, crucial primary producers and reef-builders, exhibit diverse morphologies, lifestyles, and adaptative strategies. A significant gap exists, however, in deciphering the genetic basis of algae positioned at an evolutionary crossroad from unicellular to multicellular, from intracellular calcifying to extracellular calcification, and from acidification-sensitive to acidification-tolerant. Genome analysis of the green alga Halimeda opuntia and other algae shed light on unique genetic features associated with multinucleation, cell fragment regeneration, extracellular calcification, and tolerance of CO2 increases in seawater. Our findings advance the understanding of how calcareous algae respond to environmental changes and have implications in regenerative biology, plant grafting, and coral reef conservation and restoration.
Abstract
Algae mostly occur either as unicellular (microalgae) or multicellular (macroalgae) species, both being uninucleate. There are important exceptions, however, as some unicellular algae are multinucleate and macroscopic, some of which inhabit tropical seas and contribute to biocalcification and coral reef robustness. The evolutionary mechanisms and ecological significance of multinucleation and associated traits (e.g., rapid wound healing) are poorly understood. Here, we report the genome of Halimeda opuntia, a giant multinucleate unicellular chlorophyte characterized by interutricular calcification. We achieve a high-quality genome assembly that shows segregation into four subgenomes, with evidence for polyploidization concomitant with historical sea level and climate changes. We further find myosin VIII missing in H. opuntia and three other unicellular multinucleate chlorophytes, suggesting a potential mechanism that may underpin multinucleation. Genome analysis provides clues about how the unicellular alga could survive fragmentation and regenerate, as well as potential signatures for extracellular calcification and the coupling of calcification with photosynthesis. In addition, proteomic alkalinity shifts were found to potentially confer plasticity of H. opuntia to ocean acidification (OA). Our study provides crucial genetic information necessary for understanding multinucleation, cell regeneration, plasticity to OA, and different modes of calcification in algae and other organisms, which has important implications in reef conservation and bioengineering.
Zhang H., Wang X., Qu M. & Lin Q., 2024. Genome of Halimeda opuntia reveals differentiation of subgenomes and molecular bases of multinucleation and calcification in algae. PNAS 121(39): e2403222121. doi: 10.1073/pnas.2403222121. Article (subscription required).
