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Published April 26, 2012 | Published
Journal Article Open

The cGMP Signaling Pathway Affects Feeding Behavior in the Necromenic Nematode Pristionchus pacificus

Abstract

Background: The genetic tractability and the species-specific association with beetles make the nematode Pristionchus pacificus an exciting emerging model organism for comparative studies in development and behavior. P. pacificus differs from Caenorhabditis elegans (a bacterial feeder) by its buccal teeth and the lack of pharyngeal grinders, but almost nothing is known about which genes coordinate P. pacificus feeding behaviors, such as pharyngeal pumping rate, locomotion, and fat storage. Methodology/Principal Findings: We analyzed P. pacificus pharyngeal pumping rate and locomotion behavior on and off food, as well as on different species of bacteria (Escherichia coli, Bacillus subtilis, and Caulobacter crescentus). We found that the cGMP-dependent protein kinase G (PKG) Ppa-EGL-4 in P. pacificus plays an important role in regulating the pumping rate, mouth form dimorphism, the duration of forward locomotion, and the amount of fat stored in intestine. In addition, Ppa-EGL-4 interacts with Ppa-OBI-1, a recently identified protein involved in chemosensation, to influence feeding and locomotion behavior. We also found that C. crescentus NA1000 increased pharyngeal pumping as well as fat storage in P. pacificus. Conclusions: The PKG EGL-4 has conserved functions in regulating feeding behavior in both C. elegans and P. pacificus nematodes. The Ppa-EGL-4 also has been co-opted during evolution to regulate P. pacificus mouth form dimorphism that indirectly affect pharyngeal pumping rate. Specifically, the lack of Ppa-EGL-4 function increases pharyngeal pumping, time spent in forward locomotion, and fat storage, in part as a result of higher food intake. Ppa-OBI-1 functions upstream or parallel to Ppa-EGL-4. The beetle-associated omnivorous P. pacificus respond differently to changes in food state and food quality compared to the exclusively bacteriovorous C. elegans.

Additional Information

© 2012 Kroetz et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received October 13, 2011; Accepted March 5, 2012; Published April 26, 2012 Editor: Anne C. Hart, Brown University, United States of America. Funding: This work was supported by Minority Access to Research Careers (MARC) and Caltech's MURF (Minority Undergraduate Research Fellowship) to SMK, HHMI to JS and PWS, and National Institutes of Health grant SC2GM089602 awarded to RLH. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank S. Murray for help with C. crescentus and B. subtilis strains as well as C. van Buskirk for critically reading the manuscript. Author Contributions: Conceived and designed the experiments: RLH JS. Performed the experiments: SMK JY JS. Analyzed the data: SMK RLH JY JS. Contributed reagents/materials/analysis tools: RLH PWS. Wrote the paper: RLH JS PWS.

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