Effects of fruit toxins on intestinal and microbial β-glucosidase activities of seed-predating and seed-dispersing rodents (Acomys spp.)

Kevin D. Kohl, Michal Samuni-Blank, Petros Lymberakis, Patrice Kurnath, Ido Izhaki, Zeev Arad, William H. Karasov, M. Denise Dearing

Research output: Contribution to journalArticlepeer-review

Abstract

Plant secondary compounds (PSCs) have profound influence on the ecological interaction between plants and their consumers. Glycosides, a class of PSC, are inert in their intact form and become toxic on activation by either plant β-glucosidase enzymes or endogenous β-glucosidases produced by the intestine of the plant-predator or its microbiota. Many insect herbivores decrease activities of endogenous β-glucosidases to limit toxin exposure. However, such an adaptation has never been investigated in nonmodel mammals. We studied three species of spiny mice (Acomys spp.) that vary in their feeding behavior of the glycoside-rich fruit of Ochradenus baccatus. Two species, the common (Acomys cahirinus) and Crete (Acomys minous) spiny mice, behaviorally avoid activating glycosides, while the golden spiny mouse (Acomys russatus) regularly consumes activated glycosides. We fed each species a nontoxic diet of inert glycosides or a toxic diet of activated fruit toxins and investigated the responses of intestinal and microbial β-glucosidase activities. We found that individuals feeding on activated toxins had lower intestinal β-glucosidase activity and that the species that behaviorally avoid activating glycosides also had lower intestinal β-glucosidase activity regardless of treatment. The microbiota represented a larger source of toxin liberation, and the toxin-adapted species (golden spiny mouse) exhibited almost a fivefold increase in microbial β-glucosidase when fed activated toxins, while other species showed slight decreases. These results are contrary to those in insects, where glycoside-adapted species have lower β-glucosidase activity. The glycoside-adapted golden spiny mouse may have evolved tolerance mechanisms such as enhanced detoxification rather than avoidance mechanisms.

Original languageEnglish
Pages (from-to)198-205
Number of pages8
JournalPhysiological and Biochemical Zoology
Volume89
Issue number3
DOIs
StatePublished - 1 May 2016

Bibliographical note

Funding Information:
Support for this study was available through grants from the U.S.-Israel Bi-National Science Foundation Grant (2006043), Israel Science Foundation (189/08), Middle East Regional Cooperation (TA-MOU-08 M28-013), and National Science Foundation (IOS 0817527, DEB 1210094, DEB 1342615, and DBI 1400456).

Publisher Copyright:
© 2016 by The University of Chicago. All rights reserved.

Keywords

  • Acomys
  • Digestion
  • Glycosides
  • Gut microbes
  • Plant secondary compounds
  • Plantanimal interactions

ASJC Scopus subject areas

  • Physiology
  • Biochemistry
  • Animal Science and Zoology

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