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SHORT COMMUNICATION
Rapid toxin sequestration modifies poison frog physiology
Lauren A. O'Connell, LS50: Integrated Science Laboratory Course, Jeremy D. O'Connell, Joao A. Paulo, Sunia A. Trauger, Steven P. Gygi, Andrew W. Murray
Journal of Experimental Biology 2021 224: jeb230342 doi: 10.1242/jeb.230342 Published 9 February 2021
Lauren A. O'Connell
1Department of Biology, Stanford University, Stanford, CA 94305, USA
2Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA
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  • ORCID record for Lauren A. O'Connell
  • For correspondence: loconnel@stanford.edu
2Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA
Jeremy D. O'Connell
3Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA
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Joao A. Paulo
3Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA
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Sunia A. Trauger
4Harvard Center for Mass Spectrometry, Harvard University, Cambridge, MA 02138, USA
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Steven P. Gygi
3Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA
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Andrew W. Murray
2Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA
5Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA
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ABSTRACT

Poison frogs sequester chemical defenses from their diet of leaf litter arthropods for defense against predation. Little is known about the physiological adaptations that confer this unusual bioaccumulation ability. We conducted an alkaloid-feeding experiment with the Diablito poison frog (Oophaga sylvatica) to determine how quickly alkaloids are accumulated and how toxins modify frog physiology using quantitative proteomics. Diablito frogs rapidly accumulated the alkaloid decahydroquinoline within 4 days, and dietary alkaloid exposure altered protein abundance in the intestines, liver and skin. Many proteins that increased in abundance with decahydroquinoline accumulation are plasma glycoproteins, including the complement system and the toxin-binding protein saxiphilin. Other protein classes that change in abundance with decahydroquinoline accumulation are membrane proteins involved in small molecule transport and metabolism. Overall, this work shows that poison frogs can rapidly accumulate alkaloids, which alter carrier protein abundance, initiate an immune response, and alter small molecule transport and metabolism dynamics across tissues.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: L.A.O., A.W.M.; Methodology: L.A.O., J.A.P., S.A.T., S.P.G.; Formal analysis: L.A.O.; Investigation: L.A.O., LS50, J.D.O., S.A.T.; Resources: L.A.O., J.A.P., S.A.T., S.P.G., A.W.M.; Data curation: L.A.O.; Writing - original draft: L.A.O., LS50; Writing - review & editing: J.D.O., J.A.P., S.A.T., S.P.G., A.W.M.; Visualization: L.A.O.; Supervision: L.A.O., S.P.G., A.W.M.; Project administration: L.A.O.; Funding acquisition: L.A.O., A.W.M.

  • Funding

    This work was supported a Bauer Fellowship from Harvard University (L.A.O.), the L'Oreal For Women in Science Fellowship (L.A.O.), the National Science Foundation (IOS-1557684 to L.A.O.), a Howard Hughes Medical Institute Professor's Award (520008146 to A.W.M.) and the National Institutes of Health (R01 GM132129 to J.A.P. and GM67945 to S.P.G.). Deposited in PMC for release after 12 months.

  • Data availability

    Mass spectrometry data are available from the PRoteomics IDEntifications (PRIDE) database: PXD021216 (http://www.ebi.ac.uk/pride/archive/projects/PXD021216)

  • Supplementary information

    Supplementary information available online at https://jeb.biologists.org/lookup/doi/10.1242/jeb.230342.supplemental

  • Received June 1, 2020.
  • Accepted December 18, 2020.
  • © 2021. Published by The Company of Biologists Ltd
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Keywords

  • Alkaloids
  • Proteomics
  • Saxiphilin
  • Complement system
  • Cytochrome P450s

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SHORT COMMUNICATION
Rapid toxin sequestration modifies poison frog physiology
Lauren A. O'Connell, LS50: Integrated Science Laboratory Course, Jeremy D. O'Connell, Joao A. Paulo, Sunia A. Trauger, Steven P. Gygi, Andrew W. Murray
Journal of Experimental Biology 2021 224: jeb230342 doi: 10.1242/jeb.230342 Published 9 February 2021
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SHORT COMMUNICATION
Rapid toxin sequestration modifies poison frog physiology
Lauren A. O'Connell, LS50: Integrated Science Laboratory Course, Jeremy D. O'Connell, Joao A. Paulo, Sunia A. Trauger, Steven P. Gygi, Andrew W. Murray
Journal of Experimental Biology 2021 224: jeb230342 doi: 10.1242/jeb.230342 Published 9 February 2021

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