Genome of <i>Halimeda opuntia</i> reveals differentiation of subgenomes and molecular bases of multinucleation and calcification in algae

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 <i>Halimeda opuntia</i>, 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 <i>H. opuntia</i> 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 <i>H. opuntia</i> 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.

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2024-09-20
DOI
https://doi.org/10.1073/pnas.2403222121
Citations
5
Primary Topic
Marine and coastal plant biology
Type
article
Field-Weighted Citation Impact
2.40

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article

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

Chengcheng Shi, Chris Bowler, David A. Hutchins, Qiang Lin et al.
5 citations
Proceedings of the National Academy of Sciences
Marine and coastal plant biology
2.40
article

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

Chengcheng Shi, Chris Bowler, David A. Hutchins, Qiang Lin, Jingtian Wang, Guangyi Fan, Zhangliang Wei, Bo Zhang, Hao Zhang, Yanhong Zhang, Senjie Lin, Xin Wang, Xiaochuan Liu, Da‐Zhi Wang, Meng Qu, Haiyan Yu, Fangfang Yang, Lijuan Long, Jianping Yin, Jun Sun, Yuhong Liu
article en
5 citations

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 <i>Halimeda opuntia</i>, 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 <i>H. opuntia</i> 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 <i>H. opuntia</i> 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.

Proceedings of the National Academy of SciencesVol. 121(39)
University of Southern California (US), Centre National de la Recherche Scientifique (FR), University of Connecticut (US), Inserm (FR), Xiamen University (CN), Chinese Academy of Sciences (CN), China University of Geosciences (CN), Institute of Oceanology (CN), South China Sea Institute Of Oceanology (CN), Institut de Biologie de l'École Normale Supérieure (FR), University of Chinese Academy of Sciences (CN)
Gordon and Betty Moore Foundation, National Natural Science Foundation of China, Chinese Academy of Sciences, South China Sea Institute of Oceanology, Chinese Academy of Sciences, National Key Research and Development Program of China
Life below water
Openalex Percentile: Top 12%
Marine and coastal plant biology
2.40
DOIOpen Access PDFOpenAlex
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