IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-023-44186-y.html
   My bibliography  Save this article

Integrative single-cell characterization of a frugivorous and an insectivorous bat kidney and pancreas

Author

Listed:
  • Wei E. Gordon

    (University of California, San Francisco
    University of California, San Francisco
    Menlo College)

  • Seungbyn Baek

    (Yonsei University)

  • Hai P. Nguyen

    (University of California, San Francisco
    University of California, San Francisco)

  • Yien-Ming Kuo

    (University of California, San Francisco)

  • Rachael Bradley

    (University of California, San Francisco
    University of California, San Francisco)

  • Sarah L. Fong

    (University of California, San Francisco
    University of California, San Francisco)

  • Nayeon Kim

    (Yonsei University)

  • Alex Galazyuk

    (Northeast Ohio Medical University)

  • Insuk Lee

    (Yonsei University
    Pohang University of Science and Technology (POSTECH))

  • Melissa R. Ingala

    (Fairleigh Dickinson University)

  • Nancy B. Simmons

    (American Museum of Natural History)

  • Tony Schountz

    (Colorado State University)

  • Lisa Noelle Cooper

    (Northeast Ohio Medical University)

  • Ilias Georgakopoulos-Soares

    (The Pennsylvania State University College of Medicine)

  • Martin Hemberg

    (Brigham and Women’s Hospital and Harvard Medical School)

  • Nadav Ahituv

    (University of California, San Francisco
    University of California, San Francisco)

Abstract

Frugivory evolved multiple times in mammals, including bats. However, the cellular and molecular components driving it remain largely unknown. Here, we use integrative single-cell sequencing (scRNA-seq and scATAC-seq) on insectivorous (Eptesicus fuscus; big brown bat) and frugivorous (Artibeus jamaicensis; Jamaican fruit bat) bat kidneys and pancreases and identify key cell population, gene expression and regulatory differences associated with the Jamaican fruit bat that also relate to human disease, particularly diabetes. We find a decrease in loop of Henle and an increase in collecting duct cells, and differentially active genes and regulatory elements involved in fluid and electrolyte balance in the Jamaican fruit bat kidney. The Jamaican fruit bat pancreas shows an increase in endocrine and a decrease in exocrine cells, and differences in genes and regulatory elements involved in insulin regulation. We also find that these frugivorous bats share several molecular characteristics with human diabetes. Combined, our work provides insights from a frugivorous mammal that could be leveraged for therapeutic purposes.

Suggested Citation

  • Wei E. Gordon & Seungbyn Baek & Hai P. Nguyen & Yien-Ming Kuo & Rachael Bradley & Sarah L. Fong & Nayeon Kim & Alex Galazyuk & Insuk Lee & Melissa R. Ingala & Nancy B. Simmons & Tony Schountz & Lisa N, 2024. "Integrative single-cell characterization of a frugivorous and an insectivorous bat kidney and pancreas," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44186-y
    DOI: 10.1038/s41467-023-44186-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-44186-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-44186-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Parker C. Wilson & Yoshiharu Muto & Haojia Wu & Anil Karihaloo & Sushrut S. Waikar & Benjamin D. Humphreys, 2022. "Multimodal single cell sequencing implicates chromatin accessibility and genetic background in diabetic kidney disease progression," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    2. Jessica H. Arbour & Abigail A. Curtis & Sharlene E. Santana, 2019. "Signatures of echolocation and dietary ecology in the adaptive evolution of skull shape in bats," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    3. Zhen Miao & Michael S. Balzer & Ziyuan Ma & Hongbo Liu & Junnan Wu & Rojesh Shrestha & Tamas Aranyi & Amy Kwan & Ayano Kondo & Marco Pontoglio & Junhyong Kim & Mingyao Li & Klaus H. Kaestner & Katalin, 2021. "Single cell regulatory landscape of the mouse kidney highlights cellular differentiation programs and disease targets," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    4. Jiyoung Kim & Jengmin Kang & Ye-Lim Kang & Jongmin Woo & Youngsoo Kim & June Huh & Jong-Wan Park, 2020. "Ketohexokinase-A acts as a nuclear protein kinase that mediates fructose-induced metastasis in breast cancer," Nature Communications, Nature, vol. 11(1), pages 1-20, December.
    5. Marta Perez-Frances & Léon van Gurp & Maria Valentina Abate & Valentina Cigliola & Kenichiro Furuyama & Eva Bru-Tari & Daniel Oropeza & Taïna Carreaux & Yoshio Fujitani & Fabrizio Thorel & Pedro L. He, 2021. "Pancreatic Ppy-expressing γ-cells display mixed phenotypic traits and the adaptive plasticity to engage insulin production," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    6. Blue B. Lake & Rajasree Menon & Seth Winfree & Qiwen Hu & Ricardo Melo Ferreira & Kian Kalhor & Daria Barwinska & Edgar A. Otto & Michael Ferkowicz & Dinh Diep & Nongluk Plongthongkum & Amanda Knoten , 2023. "An atlas of healthy and injured cell states and niches in the human kidney," Nature, Nature, vol. 619(7970), pages 585-594, July.
    7. Joseph O. Lamontagne & Hui Zhang & Alia M. Zeid & Karin Strittmatter & Alicia D. Rocha & Trevor Williams & Sheryl Zhang & Alexander G. Marneros, 2022. "Transcription factors AP-2α and AP-2β regulate distinct segments of the distal nephron in the mammalian kidney," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    8. Rachel K. Lex & Weiqiang Zhou & Zhicheng Ji & Kristin N. Falkenstein & Kaleigh E. Schuler & Kathryn E. Windsor & Joseph D. Kim & Hongkai Ji & Steven A. Vokes, 2022. "GLI transcriptional repression is inert prior to Hedgehog pathway activation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Rebecca A. Haeusler & Kirsten Hartil & Bhavapriya Vaitheesvaran & Isabel Arrieta-Cruz & Colette M. Knight & Joshua R. Cook & Helene L. Kammoun & Mark A. Febbraio & Roger Gutierrez-Juarez & Irwin J. Ku, 2014. "Integrated control of hepatic lipogenesis versus glucose production requires FoxO transcription factors," Nature Communications, Nature, vol. 5(1), pages 1-8, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Nicolas Ledru & Parker C. Wilson & Yoshiharu Muto & Yasuhiro Yoshimura & Haojia Wu & Dian Li & Amish Asthana & Stefan G. Tullius & Sushrut S. Waikar & Giuseppe Orlando & Benjamin D. Humphreys, 2024. "Predicting proximal tubule failed repair drivers through regularized regression analysis of single cell multiomic sequencing," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Haojia Wu & Eryn E. Dixon & Qiao Xuanyuan & Juanru Guo & Yasuhiro Yoshimura & Chitnis Debashish & Anezka Niesnerova & Hao Xu & Morgane Rouault & Benjamin D. Humphreys, 2024. "High resolution spatial profiling of kidney injury and repair using RNA hybridization-based in situ sequencing," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Yuzhou Chang & Jixin Liu & Yi Jiang & Anjun Ma & Yao Yu Yeo & Qi Guo & Megan McNutt & Jordan E. Krull & Scott J. Rodig & Dan H. Barouch & Garry P. Nolan & Dong Xu & Sizun Jiang & Zihai Li & Bingqiang , 2024. "Graph Fourier transform for spatial omics representation and analyses of complex organs," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    4. Li-Kai Chu & Xu Cao & Lin Wan & Qiang Diao & Yu Zhu & Yu Kan & Li-Li Ye & Yi-Ming Mao & Xing-Qiang Dong & Qian-Wei Xiong & Ming-Cui Fu & Ting Zhang & Hui-Ting Zhou & Shi-Zhong Cai & Zhou-Rui Ma & Ssu-, 2023. "Autophagy of OTUD5 destabilizes GPX4 to confer ferroptosis-dependent kidney injury," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    5. Jonas Engesser & Robin Khatri & Darius P. Schaub & Yu Zhao & Hans-Joachim Paust & Zeba Sultana & Nariaki Asada & Jan-Hendrik Riedel & Varshi Sivayoganathan & Anett Peters & Anna Kaffke & Saskia-Lariss, 2024. "Immune profiling-based targeting of pathogenic T cells with ustekinumab in ANCA-associated glomerulonephritis," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    6. Wenxu Zhang & Yajuan Li & Anthony A. Fung & Zhi Li & Hongje Jang & Honghao Zha & Xiaoping Chen & Fangyuan Gao & Jane Y. Wu & Huaxin Sheng & Junjie Yao & Dorota Skowronska-Krawczyk & Sanjay Jain & Ling, 2024. "Multi-molecular hyperspectral PRM-SRS microscopy," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Naomi Pode-Shakked & Megan Slack & Nambirajan Sundaram & Ruth Schreiber & Kyle W. McCracken & Benjamin Dekel & Michael Helmrath & Raphael Kopan, 2023. "RAAS-deficient organoids indicate delayed angiogenesis as a possible cause for autosomal recessive renal tubular dysgenesis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    8. Kun Yin & Yiling Xu & Ye Guo & Zhong Zheng & Xinrui Lin & Meijuan Zhao & He Dong & Dianyi Liang & Zhi Zhu & Junhua Zheng & Shichao Lin & Jia Song & Chaoyong Yang, 2024. "Dyna-vivo-seq unveils cellular RNA dynamics during acute kidney injury via in vivo metabolic RNA labeling-based scRNA-seq," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Michael S. Balzer & Tomohito Doke & Ya-Wen Yang & Daniel L. Aldridge & Hailong Hu & Hung Mai & Dhanunjay Mukhi & Ziyuan Ma & Rojesh Shrestha & Matthew B. Palmer & Christopher A. Hunter & Katalin Suszt, 2022. "Single-cell analysis highlights differences in druggable pathways underlying adaptive or fibrotic kidney regeneration," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    10. Dohui Kim & Hyeonji Lim & Jaeseung Youn & Tae-Eun Park & Dong Sung Kim, 2024. "Scalable production of uniform and mature organoids in a 3D geometrically-engineered permeable membrane," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. Xueyan Wu & Hui Ying & Qianqian Yang & Qian Yang & Haoyu Liu & Yilan Ding & Huiling Zhao & Zhihe Chen & Ruizhi Zheng & Hong Lin & Shuangyuan Wang & Mian Li & Tiange Wang & Zhiyun Zhao & Min Xu & Yuhon, 2024. "Transcriptome-wide Mendelian randomization during CD4+ T cell activation reveals immune-related drug targets for cardiometabolic diseases," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    12. Yoshiharu Muto & Eryn E. Dixon & Yasuhiro Yoshimura & Haojia Wu & Kohei Omachi & Nicolas Ledru & Parker C. Wilson & Andrew J. King & N. Eric Olson & Marvin G. Gunawan & Jay J. Kuo & Jennifer H. Cox & , 2022. "Defining cellular complexity in human autosomal dominant polycystic kidney disease by multimodal single cell analysis," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    13. Yashvardhan Jain & Leah L. Godwin & Sripad Joshi & Shriya Mandarapu & Trang Le & Cecilia Lindskog & Emma Lundberg & Katy Börner, 2023. "Segmenting functional tissue units across human organs using community-driven development of generalizable machine learning algorithms," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    14. Keith Siew & Kevin A. Nestler & Charlotte Nelson & Viola D’Ambrosio & Chutong Zhong & Zhongwang Li & Alessandra Grillo & Elizabeth R. Wan & Vaksha Patel & Eliah Overbey & JangKeun Kim & Sanghee Yun & , 2024. "Cosmic kidney disease: an integrated pan-omic, physiological and morphological study into spaceflight-induced renal dysfunction," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    15. Michal Polonsky & Louisa M. S. Gerhardt & Jina Yun & Kari Koppitch & Katsuya Lex Colón & Henry Amrhein & Barbara Wold & Shiwei Zheng & Guo-Cheng Yuan & Matt Thomson & Long Cai & Andrew P. McMahon, 2024. "Spatial transcriptomics defines injury specific microenvironments and cellular interactions in kidney regeneration and disease," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    16. Lele Song & Qinglan Li & Lingbo Xia & Arushi Eesha Sahay & Qi Qiu & Yuanyuan Li & Haitao Li & Kotaro Sasaki & Katalin Susztak & Hao Wu & Liling Wan, 2024. "Single-cell multiomics reveals ENL mutation perturbs kidney developmental trajectory by rewiring gene regulatory landscape," Nature Communications, Nature, vol. 15(1), pages 1-26, December.
    17. Chen-Rui Xia & Zhi-Jie Cao & Xin-Ming Tu & Ge Gao, 2023. "Spatial-linked alignment tool (SLAT) for aligning heterogenous slices," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    18. Lingzhi Li & Ting Xiang & Jingjing Guo & Fan Guo & Yiting Wu & Han Feng & Jing Liu & Sibei Tao & Ping Fu & Liang Ma, 2024. "Inhibition of ACSS2-mediated histone crotonylation alleviates kidney fibrosis via IL-1β-dependent macrophage activation and tubular cell senescence," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    19. Insa M. Schmidt & Aditya L. Surapaneni & Runqi Zhao & Dhairya Upadhyay & Wan-Jin Yeo & Pascal Schlosser & Courtney Huynh & Anand Srivastava & Ragnar Palsson & Taesoo Kim & Isaac E. Stillman & Daria Ba, 2024. "Plasma proteomics of acute tubular injury," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    20. Kian Kalhor & Chien-Ju Chen & Ho Suk Lee & Matthew Cai & Mahsa Nafisi & Richard Que & Carter R. Palmer & Yixu Yuan & Yida Zhang & Xuwen Li & Jinghui Song & Amanda Knoten & Blue B. Lake & Joseph P. Gau, 2024. "Mapping human tissues with highly multiplexed RNA in situ hybridization," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44186-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.