The nematode C. elegans senses airborne sound

Adam J Iliff; Can Wang; Elizabeth A Ronan; Alison E Hake; Yuling Guo; Xia Li; Xinxing Zhang; Maohua Zheng; Jianfeng Liu; Karl Grosh; R Keith Duncan; X Z Shawn Xu

doi:10.1016/j.neuron.2021.08.035

The nematode C. elegans senses airborne sound

Neuron. 2021 Nov 17;109(22):3633-3646.e7. doi: 10.1016/j.neuron.2021.08.035. Epub 2021 Sep 22.

Authors

Adam J Iliff¹, Can Wang², Elizabeth A Ronan¹, Alison E Hake³, Yuling Guo², Xia Li¹, Xinxing Zhang¹, Maohua Zheng¹, Jianfeng Liu⁴, Karl Grosh⁵, R Keith Duncan⁶, X Z Shawn Xu⁷

Affiliations

¹ Life Sciences Institute, University of Michigan, Ann Arbor, MI 48109, USA; Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, MI 48109, USA.
² Life Sciences Institute, University of Michigan, Ann Arbor, MI 48109, USA; Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, MI 48109, USA; College of Life Science and Technology, Key Laboratory of Molecular Biophysics of MOE, Huazhong University of Science and Technology, Wuhan, Hubei 430074, China.
³ Department of Mechanical Engineering, University of Michigan, Ann Arbor, MI 48109, USA.
⁴ College of Life Science and Technology, Key Laboratory of Molecular Biophysics of MOE, Huazhong University of Science and Technology, Wuhan, Hubei 430074, China.
⁵ Department of Mechanical Engineering, University of Michigan, Ann Arbor, MI 48109, USA; Department of Biomedical Engineering, University of Michigan, Ann Arbor, MI 48109, USA.
⁶ Department of Otolaryngology-Head and Neck Surgery, University of Michigan, Ann Arbor, MI 48109, USA.
⁷ Life Sciences Institute, University of Michigan, Ann Arbor, MI 48109, USA; Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, MI 48109, USA. Electronic address: shawnxu@umich.edu.

Abstract

Unlike olfaction, taste, touch, vision, and proprioception, which are widespread across animal phyla, hearing is found only in vertebrates and some arthropods. The vast majority of invertebrate species are thus considered insensitive to sound. Here, we challenge this conventional view by showing that the earless nematode C. elegans senses airborne sound at frequencies reaching the kHz range. Sound vibrates C. elegans skin, which acts as a pressure-to-displacement transducer similar to vertebrate eardrum, activates sound-sensitive FLP/PVD neurons attached to the skin, and evokes phonotaxis behavior. We identified two nAChRs that transduce sound signals independently of ACh, revealing an unexpected function of nAChRs in mechanosensation. Thus, the ability to sense airborne sound is not restricted to vertebrates and arthropods as previously thought, and might have evolved multiple times independently in the animal kingdom, suggesting convergent evolution. Our studies also demonstrate that animals without ears may not be presumed to be sound insensitive.

Keywords: ENaC; Piezo; TMC; TRP; audition; auditory; channel; mechanosensitive; mechanosensory; mechanotransduction.

Publication types

Research Support, N.I.H., Extramural

MeSH terms

Animals
Caenorhabditis elegans Proteins* / physiology
Caenorhabditis elegans* / physiology
Mechanotransduction, Cellular / physiology
Proprioception
Touch / physiology

Substances

Caenorhabditis elegans Proteins

Abstract

Publication types

MeSH terms

Substances

Grants and funding