Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism
Abstract Background Energy homeostasis is essential for the adaptation of animals to their environment and some wild animals keep low metabolism adaptive to their low-nutrient dietary supply. Giant panda is such a typical low-metabolic mammal exhibiting species specialization of extremely low daily...
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BMC
2023-10-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-023-01691-2 |
| _version_ | 1797451457227653120 |
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| author | Shangchen Yang Tianming Lan Rongping Wei Ling Zhang Lin Lin Hanyu Du Yunting Huang Guiquan Zhang Shan Huang Minhui Shi Chengdong Wang Qing Wang Rengui Li Lei Han Dan Tang Haimeng Li Hemin Zhang Jie Cui Haorong Lu Jinrong Huang Yonglun Luo Desheng Li Qiu-Hong Wan Huan Liu Sheng-Guo Fang |
| author_facet | Shangchen Yang Tianming Lan Rongping Wei Ling Zhang Lin Lin Hanyu Du Yunting Huang Guiquan Zhang Shan Huang Minhui Shi Chengdong Wang Qing Wang Rengui Li Lei Han Dan Tang Haimeng Li Hemin Zhang Jie Cui Haorong Lu Jinrong Huang Yonglun Luo Desheng Li Qiu-Hong Wan Huan Liu Sheng-Guo Fang |
| author_sort | Shangchen Yang |
| collection | DOAJ |
| description | Abstract Background Energy homeostasis is essential for the adaptation of animals to their environment and some wild animals keep low metabolism adaptive to their low-nutrient dietary supply. Giant panda is such a typical low-metabolic mammal exhibiting species specialization of extremely low daily energy expenditure. It has low levels of basal metabolic rate, thyroid hormone, and physical activities, whereas the cellular bases of its low metabolic adaptation remain rarely explored. Results In this study, we generate a single-nucleus transcriptome atlas of 21 organs/tissues from a female giant panda. We focused on the central metabolic organ (liver) and dissected cellular metabolic status by cross-species comparison. Adaptive expression mode (i.e., AMPK related) was prominently displayed in the hepatocyte of giant panda. In the highest energy-consuming organ, the heart, we found a possibly optimized utilization of fatty acid. Detailed cell subtype annotation of endothelial cells showed the uterine-specific deficiency of blood vascular subclasses, indicating a potential adaptation for a low reproductive energy expenditure. Conclusions Our findings shed light on the possible cellular basis and transcriptomic regulatory clues for the low metabolism in giant pandas and helped to understand physiological adaptation response to nutrient stress. |
| first_indexed | 2024-03-09T14:54:55Z |
| format | Article |
| id | doaj.art-256129ae92f0468a8060b2ffd8aad1f3 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-03-09T14:54:55Z |
| publishDate | 2023-10-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-256129ae92f0468a8060b2ffd8aad1f32023-11-26T14:14:17ZengBMCBMC Biology1741-70072023-10-0121111710.1186/s12915-023-01691-2Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolismShangchen Yang0Tianming Lan1Rongping Wei2Ling Zhang3Lin Lin4Hanyu Du5Yunting Huang6Guiquan Zhang7Shan Huang8Minhui Shi9Chengdong Wang10Qing Wang11Rengui Li12Lei Han13Dan Tang14Haimeng Li15Hemin Zhang16Jie Cui17Haorong Lu18Jinrong Huang19Yonglun Luo20Desheng Li21Qiu-Hong Wan22Huan Liu23Sheng-Guo Fang24MOE Key Laboratory of Biosystems Homeostasis & Protection, State Conservation Centre for Gene Resources of Endangered Wildlife, College of Life Sciences, Zhejiang UniversityState Key Laboratory of Agricultural Genomics, BGI-ShenzhenKey Laboratory of State Forestry and Grassland Administration (State Park Administration) on Conservation Biology of Rare Animals in the Giant Panda National Park, China Conservation and Research Center for the Giant PandaChina Wildlife Conservation AssociationDepartment of Biomedicine, Aarhus UniversityMOE Key Laboratory of Biosystems Homeostasis & Protection, State Conservation Centre for Gene Resources of Endangered Wildlife, College of Life Sciences, Zhejiang UniversityChina National GeneBank, BGI-ShenzhenKey Laboratory of State Forestry and Grassland Administration (State Park Administration) on Conservation Biology of Rare Animals in the Giant Panda National Park, China Conservation and Research Center for the Giant PandaKey Laboratory of State Forestry and Grassland Administration (State Park Administration) on Conservation Biology of Rare Animals in the Giant Panda National Park, China Conservation and Research Center for the Giant PandaState Key Laboratory of Agricultural Genomics, BGI-ShenzhenKey Laboratory of State Forestry and Grassland Administration (State Park Administration) on Conservation Biology of Rare Animals in the Giant Panda National Park, China Conservation and Research Center for the Giant PandaState Key Laboratory of Agricultural Genomics, BGI-ShenzhenKey Laboratory of State Forestry and Grassland Administration (State Park Administration) on Conservation Biology of Rare Animals in the Giant Panda National Park, China Conservation and Research Center for the Giant PandaCollege of Wildlife Resources, Northeast Forestry UniversityKey Laboratory of State Forestry and Grassland Administration (State Park Administration) on Conservation Biology of Rare Animals in the Giant Panda National Park, China Conservation and Research Center for the Giant PandaState Key Laboratory of Agricultural Genomics, BGI-ShenzhenKey Laboratory of State Forestry and Grassland Administration (State Park Administration) on Conservation Biology of Rare Animals in the Giant Panda National Park, China Conservation and Research Center for the Giant PandaThe Genome Synthesis and Editing Platform, BGI-ShenzhenChina National GeneBank, BGI-ShenzhenLars Bolund Institute of Regenerative Medicine, Qingdao-Europe Advanced Institute for Life Sciences, BGI-QingdaoDepartment of Biomedicine, Aarhus UniversityKey Laboratory of State Forestry and Grassland Administration (State Park Administration) on Conservation Biology of Rare Animals in the Giant Panda National Park, China Conservation and Research Center for the Giant PandaMOE Key Laboratory of Biosystems Homeostasis & Protection, State Conservation Centre for Gene Resources of Endangered Wildlife, College of Life Sciences, Zhejiang UniversityState Key Laboratory of Agricultural Genomics, BGI-ShenzhenMOE Key Laboratory of Biosystems Homeostasis & Protection, State Conservation Centre for Gene Resources of Endangered Wildlife, College of Life Sciences, Zhejiang UniversityAbstract Background Energy homeostasis is essential for the adaptation of animals to their environment and some wild animals keep low metabolism adaptive to their low-nutrient dietary supply. Giant panda is such a typical low-metabolic mammal exhibiting species specialization of extremely low daily energy expenditure. It has low levels of basal metabolic rate, thyroid hormone, and physical activities, whereas the cellular bases of its low metabolic adaptation remain rarely explored. Results In this study, we generate a single-nucleus transcriptome atlas of 21 organs/tissues from a female giant panda. We focused on the central metabolic organ (liver) and dissected cellular metabolic status by cross-species comparison. Adaptive expression mode (i.e., AMPK related) was prominently displayed in the hepatocyte of giant panda. In the highest energy-consuming organ, the heart, we found a possibly optimized utilization of fatty acid. Detailed cell subtype annotation of endothelial cells showed the uterine-specific deficiency of blood vascular subclasses, indicating a potential adaptation for a low reproductive energy expenditure. Conclusions Our findings shed light on the possible cellular basis and transcriptomic regulatory clues for the low metabolism in giant pandas and helped to understand physiological adaptation response to nutrient stress.https://doi.org/10.1186/s12915-023-01691-2Single-nucleus transcriptome atlasGiant pandaLow metabolismEnergy homeostasisAdaptation |
| spellingShingle | Shangchen Yang Tianming Lan Rongping Wei Ling Zhang Lin Lin Hanyu Du Yunting Huang Guiquan Zhang Shan Huang Minhui Shi Chengdong Wang Qing Wang Rengui Li Lei Han Dan Tang Haimeng Li Hemin Zhang Jie Cui Haorong Lu Jinrong Huang Yonglun Luo Desheng Li Qiu-Hong Wan Huan Liu Sheng-Guo Fang Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism BMC Biology Single-nucleus transcriptome atlas Giant panda Low metabolism Energy homeostasis Adaptation |
| title | Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism |
| title_full | Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism |
| title_fullStr | Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism |
| title_full_unstemmed | Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism |
| title_short | Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism |
| title_sort | single nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism |
| topic | Single-nucleus transcriptome atlas Giant panda Low metabolism Energy homeostasis Adaptation |
| url | https://doi.org/10.1186/s12915-023-01691-2 |
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