IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-53590-x.html
   My bibliography  Save this article

Conserved autism-associated genes tune social feeding behavior in C. elegans

Author

Listed:
  • Mara H. Cowen

    (University of Pennsylvania
    University of Pennsylvania
    Perelman School of Medicine)

  • Dustin Haskell

    (University of Pennsylvania)

  • Kristi Zoga

    (University of Pennsylvania)

  • Kirthi C. Reddy

    (Salk Institute)

  • Sreekanth H. Chalasani

    (Salk Institute)

  • Michael P. Hart

    (University of Pennsylvania
    Perelman School of Medicine)

Abstract

Animal foraging is an essential and evolutionarily conserved behavior that occurs in social and solitary contexts, but the underlying molecular pathways are not well defined. We discover that conserved autism-associated genes (NRXN1(nrx-1), NLGN3(nlg-1), GRIA1,2,3(glr-1), GRIA2(glr-2), and GLRA2,GABRA3(avr-15)) regulate aggregate feeding in C. elegans, a simple social behavior. NRX-1 functions in chemosensory neurons (ADL and ASH) independently of its postsynaptic partner NLG-1 to regulate social feeding. Glutamate from these neurons is also crucial for aggregate feeding, acting independently of NRX-1 and NLG-1. Compared to solitary counterparts, social animals show faster presynaptic release and more presynaptic release sites in ASH neurons, with only the latter requiring nrx-1. Disruption of these distinct signaling components additively converts behavior from social to solitary. Collectively, we find that aggregate feeding is tuned by conserved autism-associated genes through complementary synaptic mechanisms, revealing molecular principles driving social feeding.

Suggested Citation

  • Mara H. Cowen & Dustin Haskell & Kristi Zoga & Kirthi C. Reddy & Sreekanth H. Chalasani & Michael P. Hart, 2024. "Conserved autism-associated genes tune social feeding behavior in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53590-x
    DOI: 10.1038/s41467-024-53590-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-53590-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-53590-x?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. Michael P. Hart & Oliver Hobert, 2018. "Neurexin controls plasticity of a mature, sexually dimorphic neuron," Nature, Nature, vol. 553(7687), pages 165-170, January.
    2. Vincenzo Salpietro & Christine L. Dixon & Hui Guo & Oscar D. Bello & Jana Vandrovcova & Stephanie Efthymiou & Reza Maroofian & Gali Heimer & Lydie Burglen & Stephanie Valence & Erin Torti & Moritz Hac, 2019. "AMPA receptor GluA2 subunit defects are a cause of neurodevelopmental disorders," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    3. Mario de Bono & David M. Tobin & M. Wayne Davis & Leon Avery & Cornelia I. Bargmann, 2002. "Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli," Nature, Nature, vol. 419(6910), pages 899-903, October.
    4. Jesse M. Gray & David S. Karow & Hang Lu & Andy J. Chang & Jennifer S. Chang & Ronald E. Ellis & Michael A. Marletta & Cornelia I. Bargmann, 2004. "Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue," Nature, Nature, vol. 430(6997), pages 317-322, July.
    5. Julian C Evans & Teri B Jones & Julie Morand-Ferron & Jonathan PruittHandling editor, 2018. "Dominance and the initiation of group feeding events: the modifying effect of sociality," Behavioral Ecology, International Society for Behavioral Ecology, vol. 29(2), pages 448-458.
    6. Mia-Lana Lührs & Melanie Dammhahn & Peter Kappeler, 2013. "Editor's choice Strength in numbers: males in a carnivore grow bigger when they associate and hunt cooperatively," Behavioral Ecology, International Society for Behavioral Ecology, vol. 24(1), pages 21-28.
    7. Shingo Hiroki & Hikari Yoshitane & Hinako Mitsui & Hirofumi Sato & Chie Umatani & Shinji Kanda & Yoshitaka Fukada & Yuichi Iino, 2022. "Molecular encoding and synaptic decoding of context during salt chemotaxis in C. elegans," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    8. Daniel Witvliet & Ben Mulcahy & James K. Mitchell & Yaron Meirovitch & Daniel R. Berger & Yuelong Wu & Yufang Liu & Wan Xian Koh & Rajeev Parvathala & Douglas Holmyard & Richard L. Schalek & Nir Shavi, 2021. "Connectomes across development reveal principles of brain maturation," Nature, Nature, vol. 596(7871), pages 257-261, August.
    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. Kaia J. Tombak & Severine B. S. W. Hex & Daniel I. Rubenstein, 2024. "New estimates indicate that males are not larger than females in most mammal species," Nature Communications, Nature, vol. 15(1), pages 1-7, December.
    2. Zhihao Zheng & Christopher S. Own & Adrian A. Wanner & Randal A. Koene & Eric W. Hammerschmith & William M. Silversmith & Nico Kemnitz & Ran Lu & David W. Tank & H. Sebastian Seung, 2024. "Fast imaging of millimeter-scale areas with beam deflection transmission electron microscopy," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    3. Kate L. Laskowski & David Bierbach & Jolle W. Jolles & Carolina Doran & Max Wolf, 2022. "The emergence and development of behavioral individuality in clonal fish," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    4. Chenxi Lin & Yuxin Shan & Zhongyi Wang & Hui Peng & Rong Li & Pingzhou Wang & Junyan He & Weiwei Shen & Zhengxing Wu & Min Guo, 2024. "Molecular and circuit mechanisms underlying avoidance of rapid cooling stimuli in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Noa Deshe & Yifat Eliezer & Lihi Hoch & Eyal Itskovits & Eduard Bokman & Shachaf Ben-Ezra & Alon Zaslaver, 2023. "Inheritance of associative memories and acquired cellular changes in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Laurens Broeckx & Lotte Frooninckx & Laurien Slegers & Siebe Berrens & Isabelle Noyens & Sarah Goossens & Geert Verheyen & Ann Wuyts & Sabine Van Miert, 2021. "Growth of Black Soldier Fly Larvae Reared on Organic Side-Streams," Sustainability, MDPI, vol. 13(23), pages 1-20, November.
    7. Hyunsoo Yim & Daniel T. Choe & J. Alexander Bae & Myung-kyu Choi & Hae-Mook Kang & Ken C. Q. Nguyen & Soungyub Ahn & Sang-kyu Bahn & Heeseung Yang & David H. Hall & Jinseop S. Kim & Junho Lee, 2024. "Comparative connectomics of dauer reveals developmental plasticity," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    8. Saurabh Thapliyal & Isabel Beets & Dominique A. Glauser, 2023. "Multisite regulation integrates multimodal context in sensory circuits to control persistent behavioral states in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    9. Leon Avery & Brian Ingalls & Catherine Dumur & Alexander Artyukhin, 2021. "A Keller-Segel model for C elegans L1 aggregation," PLOS Computational Biology, Public Library of Science, vol. 17(7), pages 1-25, July.
    10. Dániel L. Barabási & Taliesin Beynon & Ádám Katona & Nicolas Perez-Nieves, 2023. "Complex computation from developmental priors," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    11. Zhongyu Chen & Yuguo Yu & Xiangyang Xue, 2023. "A Connectome-Based Digital Twin Caenorhabditis elegans Capable of Intelligent Sensorimotor Behavior," Mathematics, MDPI, vol. 11(11), pages 1-23, May.
    12. Kiya W. Govek & Patrick Nicodemus & Yuxuan Lin & Jake Crawford & Artur B. Saturnino & Hannah Cui & Kristi Zoga & Michael P. Hart & Pablo G. Camara, 2023. "CAJAL enables analysis and integration of single-cell morphological data using metric geometry," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    13. Ichiro Aoki & Luca Golinelli & Eva Dunkel & Shripriya Bhat & Erschad Bassam & Isabel Beets & Alexander Gottschalk, 2024. "Hierarchical regulation of functionally antagonistic neuropeptides expressed in a single neuron pair," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    14. Francesca Coraggio & Mahak Bhushan & Spyridon Roumeliotis & Francesca Caroti & Carlo Bevilacqua & Robert Prevedel & Georgia Rapti, 2024. "Age-progressive interplay of HSP-proteostasis, ECM-cell junctions and biomechanics ensures C. elegans astroglial architecture," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    15. Wendy Xueyi Wang & Julie L. Lefebvre, 2022. "Morphological pseudotime ordering and fate mapping reveal diversification of cerebellar inhibitory interneurons," Nature Communications, Nature, vol. 13(1), pages 1-21, 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_s41467-024-53590-x. 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.