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Molecular Physiology of Chemical Defenses in a Poison Frog Stephanie N

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Molecular Physiology of Chemical Defenses in a Poison Frog Stephanie N © 2019. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2019) 222, jeb204149. doi:10.1242/jeb.204149 RESEARCH ARTICLE Molecular physiology of chemical defenses in a poison frog Stephanie N. Caty1, Aurora Alvarez-Buylla1, Gary D. Byrd2, Charles Vidoudez2, Alexandre B. Roland3, Elicio E. Tapia4, Bogdan Budnik5, Sunia A. Trauger2, Luis A. Coloma4 and Lauren A. O’Connell1,* ABSTRACT (Savitzky et al., 2012). Invertebrates can also sequester small Poison frogs sequester small molecule lipophilic alkaloids from their molecule toxins from their diet, and this process has been diet of leaf litter arthropods for use as chemical defenses against documented in beetles, moths and butterflies (Trigo, 2010; predation. Although the dietary acquisition of chemical defenses in Petschenka and Agrawal, 2016). Many decades of research have poison frogs is well documented, the physiological mechanisms of focused on cataloging the small molecules sequestered by vertebrates alkaloid sequestration has not been investigated. Here, we used RNA and documenting the trophic relationships of these chemically sequencing and proteomics to determine how alkaloids impact defended animals and their prey (Savitzky et al., 2012). mRNA or protein abundance in the little devil frog (Oophaga The ability to sequester small molecule toxins from dietary sylvatica), and compared wild-caught chemically defended frogs sources has evolved many times in frogs, including Neotropical with laboratory frogs raised on an alkaloid-free diet. To understand dendrobatids and bufonids, Malagasy mantellids, Australian how poison frogs move alkaloids from their diet to their skin granular myobatrachids (Pseudophryne) and Cuban eleutherodactylids glands, we focused on measuring gene expression in the intestines, (Saporito et al., 2011). These frogs uptake lipophilic alkaloids skin and liver. Across these tissues, we found many differentially from arthropod prey items, store them in skin granular glands and expressed transcripts involved in small molecule transport and secrete them as a defensive response (Santos et al., 2016). In order to metabolism, as well as sodium channels and other ion pumps. We utilize diet-derived toxins, frogs may be resistant to alkaloids they then used proteomic approaches to quantify plasma proteins, where are accumulating through mutations in target proteins. Many we found several protein abundance differences between wild and alkaloids target voltage-gated sodium channels and nicotinic laboratory frogs, including the amphibian neurotoxin binding protein acetylcholine receptors in the nervous system, and some studies saxiphilin. Finally, because many blood proteins are synthesized in have found ion channel mutations that confer toxin resistance in the liver, we used thermal proteome profiling as an untargeted screen poison frogs (Santos et al., 2016; Tarvin et al., 2016, 2017; Wang for soluble proteins that bind the alkaloid decahydroquinoline. Using and Wang, 1998). Detailed information on binding properties of a this approach, we identified several candidate proteins that interact wide range of poison frog alkaloids in many different ion channel with this alkaloid, including saxiphilin. These transcript and protein types is lacking, as early studies focused on a few types of alkaloids abundance patterns suggest that the presence of alkaloids influences and ion channels. Despite the progress in understanding the frog physiology and that small molecule transport proteins may be evolution of autoresistance and chemical defenses in poison frogs, involved in toxin bioaccumulation in dendrobatid poison frogs. no study has examined other molecular aspects of physiology that allows toxin sequestration. KEY WORDS: Alkaloids, Sequestration, Oophaga sylvatica, To accomplish the sequestration of alkaloids, poison frogs Saxiphilin, Dendrobatidae, RNA sequencing, Proteomics, Plasma selectively move these small molecules from the gastrointestinal tract to the skin glands for storage. In many animals, toxic compounds INTRODUCTION are unable to pass through the intestinal wall for absorption owing to a Many organisms, from microbes to vertebrates, have chemical series of membrane transporters in the gut epithelium. These defenses to guard against predation. Although microbes and plants transporters bind compounds and move them either into circulation produce secondary metabolites that can serve as toxins (Burja et al., or back into the intestinal lumen for excretion (Steffansen et al., 2001; Gershenzon, 1999), most animals cannot synthesize small 2004). Once absorbed in the intestines, lipophilic compounds can be molecule toxins themselves. Although some animals such as snakes circulated by a number of different mechanisms, including binding by and arachnids produce genetically encoded peptide toxins, other carrier proteins in the blood circulation or within lipoprotein particles vertebrate animals, including some amphibians, reptiles and birds, such as chylomicrons in the lymph system (Trevaskis et al., 2008). carry small molecule toxins that are acquired from dietary sources In many animals, dietary compounds in the blood circulatory system are metabolized by the liver, and there is some evidence that poison 1Department of Biology, Stanford University, Stanford, CA 94305, USA. 2Small frogs can metabolize dietary alkaloids. Daly and colleagues (2003) Molecule Mass Spectrometry Facility, Harvard University, Cambridge, MA 02138, suggested that some (but not all) dendrobatid poison frog species can USA. 3Center for Systems Biology, Harvard University, Cambridge, MA 02138, metabolize pumiliotoxin 251D into allopumiliotoxin 267A, although USA. 4Centro Jambatu de Investigación y Conservación de Anfibios, Fundación Otonga, San Rafael, Quito, Ecuador. 5Proteomics Mass Spectrometry Facility, the mechanisms underlying this observation remain unknown. Harvard University, Cambridge, MA 02138, USA. Clearly, coordination across several tissue systems is required for alkaloid sequestration in poison frogs, but the physiological basis for *Author for correspondence ([email protected]) alkaloid bioaccumulation remains unexplored. A.A.-B., 0000-0001-6256-0300; G.D.B., 0000-0002-5437-9293; C.V., 0000- The goal of the present study was to better understand the 0003-0953-7800; A.B.R., 0000-0002-9463-9838; E.E.T., 0000-0001-9005-5328; physiology of acquired chemical defenses in dendrobatid poison S.A.T., 0000-0002-1678-8715; L.A.C., 0000-0003-0158-2455; L.A.O., 0000-0002- 2706-4077 frogs. In surveying the alkaloid profiles of wild-caught little devil frogs (Oophaga sylvatica, Dendrobatidae) and juveniles captured in Received 28 March 2019; Accepted 16 May 2019 the wild but raised in the laboratory on an alkaloid-free diet, we had Journal of Experimental Biology 1 RESEARCH ARTICLE Journal of Experimental Biology (2019) 222, jeb204149. doi:10.1242/jeb.204149 an opportunity to examine physiological differences associated with the method reported by Saporito and colleagues (2010b). Briefly, chemical defenses. We compared gene expression in the intestines, analyses were performed on a Waters Quattro Micro system liver and skin, as well as plasma protein abundance in wild-caught (Beverly, MA, USA) with an Agilent 6890N GC (Palo Alto, CA, chemically defended frogs and laboratory frogs raised on an USA). Each total ion chromatogram was reviewed and alkaloid alkaloid-free diet. To further functionally identify proteins that may responses were characterized from their mass spectra and retention bind toxins for transport, we performed a thermal proteome times. The extensive database developed by Daly and colleagues profiling assay using liver protein lysate from a laboratory-reared (2005) was used to identify alkaloids by matching major mass frog. As toxins are acquired from the diet and transported to the skin spectrum peaks and relative retention times using D3-nicotine as a granular glands for storage, we expected that the presence of toxins reference. AMDIS (NIST) was used in conjunction with the would cause an increase in expression of genes associated with database to identify candidate alkaloid peaks. Those peaks were small molecule transport or metabolism. then manually inspected and the confirmed alkaloid peaks were then integrated. Unidentifiable compounds were removed from data MATERIALS AND METHODS analysis. The relative abundance values were normalized by Field collection of Oophaga sylvatica nicotine and were visualized using the heatmap.2 R function in Little devil (or diablito) frogs [Oophaga sylvatica (Funkhouser the gplots package. A representative extracted ion chromatogram 1956) N=13] were collected during the day near the Otokiki Reserve for each group was normalized to the same scale to create a visual (GPS coordinates: latitude 0.91075, longitude −78.57555, altitude overview. All GC/MS data are available from the Dryad Digital 704 m) maintained by WIKIRI/Fundación Otonga in northwestern Repository (Caty et al., 2019; doi:10.5061/dryad.4cs9573). Ecuador in July 2013 (Roland et al., 2017). Frogs were individually stored in plastic bags with air and vegetation for 2–5 h. In the Reference transcriptome evening the same day of capture, adult frogs (over 1 yr of age; five To build a reference transcriptome for gene expression analyses, we females and three males) were anesthetized with a topical sequenced tissues from a single O. sylvatica. We isolated intestines, application of 20% benzocaine to the ventral belly and euthanized liver and dorsal
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