Genome of Halimeda opuntia reveals differentiation of subgenomes and molecular bases of multinucleation and calcification in algae

• 成果类型: Article
• 署名作者: Zhang, Hao; Wang, Xin; Qu, Meng; Yu, Haiyan; Yin, Jianping; Liu, Xiaochuan; Liu, Yuhong; Zhang, Bo; Zhang, Yanhong; Wei, Zhangliang; Yang, Fangfang; Wang, Jingtian; Shi, Chengcheng; Fan, Guangyi; Sun, Jun; Long, Lijuan; Hutchins, David A.; Bowler, Chris; Lin, Senjie; Wang, Dazhi; Lin, Qiang
• 署名单位: Chinese Academy of Sciences; South China Sea Institute of Oceanology, CAS; Chinese Academy of Sciences; South China Sea Institute of Oceanology, CAS; Xiamen University; Beijing Genomics Institute (BGI); China University of Geosciences; University of Southern California; Institut National de la Sante et de la Recherche Medicale (Inserm); Universite PSL; Ecole Normale Superieure (ENS); Centre National de la Recherche Scientifique (CNRS); University of Connecticut; Chinese Academy of Sciences; University of Chinese Academy of Sciences, CAS
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-11123
• DOI: 10.1073/pnas.2403222121
• 发表日期: 2024-09-24
• 关键词: ocean acidification; coral-reefs; green; nuclear; EVOLUTION; chlorophyta; proteins; polysaccharides; quantification; bryopsidales

摘要

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 extra- cellular 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.