Caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategies
- Northeastern University, United States
- University of Pittsburgh School of Medicine, United States
- Centre for Genomic Regulation, Spain
Abstract
Hydrogen peroxide is the preeminent chemical weapon that organisms use for combat. Individual cells rely on conserved defenses to prevent and repair peroxide-induced damage, but whether similar defenses might be coordinated across cells in animals remains poorly understood. Here, we identify a neuronal circuit in the nematode Caenorhabditis elegans that processes information perceived by two sensory neurons to control the induction of hydrogen peroxide defenses in the organism. We found that catalases produced by Escherichia coli, the nematode's food source, can deplete hydrogen peroxide from the local environment and thereby protect the nematodes. In the presence of E. coli, the nematode's neurons signal via TGFβ-insulin/IGF1 relay to target tissues to repress expression of catalases and other hydrogen peroxide defenses. This adaptive strategy is the first example of a multicellular organism modulating its defenses when it expects to freeload from the protection provided by molecularly orthologous defenses from another species.
Data availability
Aligned mRNA-seq read files were made available under Sequence Read Archive (SRA) SUB7234259. All data generated or analysed during this study are included in the manuscript and supporting files.
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Gene expression in adult C. elegans daf-7 null mutantsSequence Read Archive, SUB7234259.
Article and author information
Author details
Nicholas Edward Stroustrup
Funding
National Science Foundation (1750065)
- Javier Apfeld
National Institutes of Health (R01AG051659)
- Arjumand Ghazi
Northeastern University (Tier 1 award)
- Javier Apfeld
MEIC Excelencia award (BFU2017-88615-P)
- Nicholas Edward Stroustrup
the CERCA Programme/Generalitat de Catalunya, and European Research Council under the European Union's Horizon 2020 research and innovation programme (852201)
- Nicholas Edward Stroustrup
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Oliver Hobert, Howard Hughes Medical Institute, Columbia University, United States
Version history
- Received: February 20, 2020
- Accepted: April 21, 2020
- Accepted Manuscript published: May 5, 2020 (version 1)
- Version of Record published: May 11, 2020 (version 2)
Copyright
© 2020, Schiffer et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategies
eLife 9:e56186.
https://doi.org/10.7554/eLife.56186
Further reading
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During Caenorhabditis elegans development, multiple cells migrate long distances or extend processes to reach their final position and/or attain proper shape. The Wnt signalling pathway stands out as one of the major coordinators of cell migration or cell outgrowth along the anterior-posterior body axis. The outcome of Wnt signalling is fine-tuned by various mechanisms including endocytosis. In this study, we show that SEL-5, the C. elegans orthologue of mammalian AP2-associated kinase AAK1, acts together with the retromer complex as a positive regulator of EGL-20/Wnt signalling during the migration of QL neuroblast daughter cells. At the same time, SEL-5 in cooperation with the retromer complex is also required during excretory canal cell outgrowth. Importantly, SEL-5 kinase activity is not required for its role in neuronal migration or excretory cell outgrowth, and neither of these processes is dependent on DPY-23/AP2M1 phosphorylation. We further establish that the Wnt proteins CWN-1 and CWN-2 together with the Frizzled receptor CFZ-2 positively regulate excretory cell outgrowth, while LIN-44/Wnt and LIN-17/Frizzled together generate a stop signal inhibiting its extension.
