Published March 6, 2024 | Version Published
Journal Article Open

Dietary E. coli promotes age-dependent chemotaxis decline in C. elegans

Abstract

An animal’s ability to sense odors declines during aging, and its olfactory drive is tuned by internal states such as satiety. However, whether internal states modulate an age-dependent decline in odor sensation is unknown. To address this issue, we utilized the nematode Caenorhabditis elegans and compared their chemotaxis abilities toward attractive odorants when aged under different dietary conditions. Feeding with the standard laboratory diet, Escherichia coli attenuated the chemotaxis ability toward diacetyl, isoamyl alcohol, and benzaldehyde when aged. On the other hand, feeding with either the lactic acid bacteria Lactobacillus reuteri or food deprivation selectively maintained the chemotaxis ability toward diacetyl. Our results suggest that ingestion of E. coli causes age-dependent chemotaxis decline. The changes in the chemotaxis behavior are attributed to the different expressions of diacetyl receptor odr-10, and the chemotaxis behavior of aged animals under food deprivation is shown to be dependent on daf-16. Our study demonstrates the molecular mechanism of how diet shapes the trajectory of age-dependent decline in chemosensory behaviors.

Copyright and License

© The Author(s) 2024. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Acknowledgement

This work was supported by Megmilk Snow Brand Company, JSPS KAKENHI, Grant Number JP 21K06014, and JST FOREST Program, Grant Number JPMJFR 214V. We thank members of the Nutritional Neuroscience laboratory and the Mori laboratory for their comments on the manuscript and Wei Huang and Pauline Rouillard for technical support. Some strains were provided by the CGC, funded by the NIH Office of Research Infrastructure Programs (P40 OD010440), and by the Mitani laboratory of the National Bioresource Project of Japan.

Contributions

These authors contributed equally: Nadia Suryawinata and Rikuou Yokosawa.

N.S., K.H.C.T., A.L.L., I.M., and K.N. conceived and initiated the project; N.S., R.Y., K.H.C.T., A.L.L., and R.S. performed the experiments; N.S., R.Y., K.H.C.T., A.L.L., and R.S. analyzed the data; R.Y. performed the statistical analyses and prepared graphical illustrations; N.S., K.N. wrote the manuscript; I.M. and K.N. provided the resource. K.N. acquired funding. All authors reviewed the manuscript prior to submission.

Data Availability

All data analyzed for this article and supplementary information are made available in this published article. Source data are provided in this paper.

Conflict of Interest

The authors declare no competing interests.

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Additional details

Identifiers

Funding

Megmilk Snow Brand
Japan Society for the Promotion of Science
JP21K06014
Japan Science and Technology Agency
JPMJFR 214V
National Institutes of Health
P40 OD010440
RIKEN BioResource Research Center