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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Cylicins are testis-specific proteins, which are exclusively expressed during spermiogenesis. In mice and humans, two Cylicins, the gonosomal X-linked Cylicin 1 (Cylc1/CYLC1) and the autosomal Cylicin 2 (Cylc2/CYLC2) genes, have been identified. Cylicins are cytoskeletal proteins with an overall positive charge due to lysine-rich repeats. While Cylicins have been localized in the acrosomal region of round spermatids, they resemble a major component of the calyx within the perinuclear theca at the posterior part of mature sperm nuclei. However, the role of Cylicins during spermiogenesis has not yet been investigated. Here, we applied CRISPR/Cas9-mediated gene editing in zygotes to establish Cylc1- and Cylc2-deficient mouse lines as a model to study the function of these proteins. Cylc1 deficiency resulted in male subfertility, whereas Cylc2-/-, Cylc1-/yCylc2+/-, and Cylc1-/yCylc2-/- males were infertile. Phenotypical characterization revealed that loss of Cylicins prevents proper calyx assembly during spermiogenesis. This results in decreased epididymal sperm counts, impaired shedding of excess cytoplasm, and severe structural malformations, ultimately resulting in impaired sperm motility. Furthermore, exome sequencing identified an infertile man with a hemizygous variant in CYLC1 and a heterozygous variant in CYLC2, displaying morphological abnormalities of the sperm including the absence of the acrosome. Thus, our study highlights the relevance and importance of Cylicins for spermiogenic remodeling and male fertility in human and mouse, and provides the basis for further studies on unraveling the complex molecular interactions between perinuclear theca proteins required during spermiogenesis.
