The genome of Nautilus pompilius illuminates eye evolution and biomineralization.

Yang Zhang, Fan Mao, Huawei Mu, Minwei Huang, Yongbo Bao, Lili Wang, Nai-Kei Wong, Shu Xiao, He Dai, Zhiming Xiang, Mingli Ma, Yuanyan Xiong, Ziwei Zhang, Lvping Zhang, Xiaoyuan Song, Fan Wang, Xiyu Mu, Jun Li, Haitao Ma, Yuehuan Zhang, Hongkun Zheng, Oleg Simakov, Ziniu Yu
Author Information
  1. Yang Zhang: Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China. ORCID
  2. Fan Mao: Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China.
  3. Huawei Mu: MOE Key Laboratory for Membraneless Organelles and Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, CAS Key Laboratory of Brain Function and Disease, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, China.
  4. Minwei Huang: Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China. ORCID
  5. Yongbo Bao: Zhejiang Key Laboratory of Aquatic Germplasm Resources, College of Biological and Environmental Sciences, Zhejiang Wanli University, Ningbo, China.
  6. Lili Wang: Biomarker Technologies Corporation, Beijing, China.
  7. Nai-Kei Wong: Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China.
  8. Shu Xiao: Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China. ORCID
  9. He Dai: Biomarker Technologies Corporation, Beijing, China.
  10. Zhiming Xiang: Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China.
  11. Mingli Ma: Biomarker Technologies Corporation, Beijing, China.
  12. Yuanyan Xiong: State Key Laboratory of Biocontrol, College of Life Sciences, Sun Yat-sen University, Guangzhou, China.
  13. Ziwei Zhang: State Key Laboratory of Biocontrol, College of Life Sciences, Sun Yat-sen University, Guangzhou, China. ORCID
  14. Lvping Zhang: Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China.
  15. Xiaoyuan Song: MOE Key Laboratory for Membraneless Organelles and Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, CAS Key Laboratory of Brain Function and Disease, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, China.
  16. Fan Wang: Biomarker Technologies Corporation, Beijing, China.
  17. Xiyu Mu: Biomarker Technologies Corporation, Beijing, China.
  18. Jun Li: Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China.
  19. Haitao Ma: Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China.
  20. Yuehuan Zhang: Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China.
  21. Hongkun Zheng: Biomarker Technologies Corporation, Beijing, China. ORCID
  22. Oleg Simakov: Department of Neuroscience and Developmental Biology, University of Vienna, Vienna, Austria. ORCID
  23. Ziniu Yu: Key Laboratory of Tropical Marine Bio-resources and Ecology and Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China. carlzyu@scsio.ac.cn. ORCID

Abstract

Nautilus is the sole surviving externally shelled cephalopod from the Palaeozoic. It is unique within cephalopod genealogy and critical to understanding the evolutionary novelties of cephalopods. Here, we present a complete Nautilus pompilius genome as a fundamental genomic reference on cephalopod innovations, such as the pinhole eye and biomineralization. Nautilus shows a compact, minimalist genome with few encoding genes and slow evolutionary rates in both non-coding and coding regions among known cephalopods. Importantly, multiple genomic innovations including gene losses, independent contraction and expansion of specific gene families and their associated regulatory networks likely moulded the evolution of the nautilus pinhole eye. The conserved molluscan biomineralization toolkit and lineage-specific repetitive low-complexity domains are essential to the construction of the nautilus shell. The nautilus genome constitutes a valuable resource for reconstructing the evolutionary scenarios and genomic innovations that shape the extant cephalopods.

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Grants

  1. P 30686/Austrian Science Fund FWF

MeSH Term

Animals
Biomineralization
Genome
Humans
Nautilus

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