Molecular physiology of chemical defenses in a poison frog

Author:

Caty Stephanie N.1,Alvarez-Buylla Aurora1ORCID,Byrd Gary D.2ORCID,Vidoudez Charles2ORCID,Roland Alexandre B.3ORCID,Tapia Elicio E.4ORCID,Budnik Bogdan5,Trauger Sunia A.2ORCID,Coloma Luis A.4ORCID,O'Connell Lauren A.1

Affiliation:

1. Department of Biology, Stanford University, Stanford, CA 94305, USA

2. Small Molecule Mass Spectrometry Facility, Harvard University, Cambridge, MA 02138, USA

3. Center for Systems Biology, Harvard University, Cambridge, Massachusetts, USA

4. Centro Jambatu de Investigación y Conservación de Anfibios, Fundación Otonga, San Rafael, Quito, Ecuador

5. Proteomics Mass Spectrometry Facility, Harvard University, Cambridge, MA 02138, USA

Abstract

Poison frogs sequester small molecule lipophilic alkaloids from their diet of leaf litter arthropods for use as chemical defenses against predation. Although the dietary acquisition of chemical defenses in poison frogs is well-documented, the physiological mechanisms of alkaloid sequestration has not been investigated. Here, we used RNA sequencing and proteomics to determine how alkaloids impact mRNA or protein abundance in the Little Devil Frog (Oophaga sylvatica) and compared wild caught chemically defended frogs to laboratory frogs raised on an alkaloid-free diet. To understand how poison frogs move alkaloids from their diet to their skin granular glands, we focused on measuring gene expression in the intestines, skin, and liver. Across these tissues, we found many differentially expressed transcripts involved in small molecule transport and metabolism, as well as sodium channels and other ion pumps. We then used proteomic approaches to quantify plasma proteins, where we found several protein abundance differences between wild and laboratory frogs, including the amphibian neurotoxin binding protein saxiphilin. Finally, because many blood proteins are synthesized in the liver, we used thermal proteome profiling as an untargeted screen for soluble proteins that bind the alkaloid decahydroquinoline. Using this approach, we identified several candidate proteins that interact with this alkaloid, including saxiphilin. These transcript and protein abundance patterns suggest the presence of alkaloids influences frog physiology and that small molecule transport proteins may be involved in toxin bioaccumulation in dendrobatid poison frogs.

Funder

National Science Foundation

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

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