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Primary Metabolism co-Opted for Defensive Chemical Production in the Carabid Beetle, Harpalus pensylvanicus

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An Author Correction to this article was published on 31 March 2021

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Abstract

Of the approximately one million described insect species, ground beetles (Coleoptera: Carabidae) have long captivated the attention of evolutionary biologists due to the diversity of defensive compounds they synthesize. Produced using defensive glands in the abdomen, ground beetle chemicals represent over 250 compounds including predator-deterring formic acid, which has evolved as a defensive strategy at least three times across Insecta. Despite being a widespread method of defense, formic acid biosynthesis is poorly understood in insects. Previous studies have suggested that the folate cycle of one-carbon (C1) metabolism, a pathway involved in nucleotide biosynthesis, may play a key role in defensive-grade formic acid production in ants. Here, we report on the defensive gland transcriptome of the formic acid-producing ground beetle Harpalus pensylvanicus. The full suite of genes involved in the folate cycle of C1 metabolism are significantly differentially expressed in the defensive glands of H. pensylvanicus when compared to gene expression profiles in the rest of the body. We also find support for two additional pathways potentially involved in the biosynthesis of defensive-grade formic acid, the kynurenine pathway and the methionine salvage cycle. Additionally, we have found an array of differentially expressed genes in the secretory lobes involved in the biosynthesis and transport of cofactors necessary for formic acid biosynthesis, as well as genes presumably involved in the detoxification of secondary metabolites including formic acid. We also provide insight into the evolution of the predominant gene family involved in the folate cycle (MTHFD) and suggest that high expression of folate cycle genes rather than gene duplication and/or neofunctionalization may be more important for defensive-grade formic acid biosynthesis in H. pensylvanicus. This provides the first evidence in Coleoptera and one of a few examples in Insecta of a primary metabolic process being co-opted for defensive chemical biosynthesis. Our results shed light on potential mechanisms of formic acid biosynthesis in the defensive glands of a ground beetle and provide a foundation for further studies into the evolution of formic acid-based chemical defense strategies in insects.

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Acknowledgements

We thank Yuka Imamura and Kimberly Moran for their assistance with RNA extraction, library preparation, and RNA-Seq. We would also like to thank Wendy Moore, Reilly McManus, Kipling Will, Sean Perez, and Aman Gill for thoughtful discussion on Carabidae biology and chemical defense mechanisms. Additionally, we thank Wendy Moore, Kipling Will, Kylie Bocklund, Chloe P. Drummond, Katie Nolan, Kadeem Gilbert, Arthi Bala, Dana Roberts, Jonah Ulmer, and István Mikó for discussion and critique of this project, its results, and interpretation. This work was supported by the National Science Foundation [DEB 1762760, 1556898].

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Authors and Affiliations

  1. Department of Entomology, The Pennsylvania State University, 501 ASI Building, University Park, PA, 16802, USA

    Adam M. Rork & Tanya Renner

  2. Department of Chemistry and Chemical Biology, Stevens Institute of Technology, Hoboken, NJ, 07030, USA

    Sihang Xu & Athula Attygalle

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  1. Adam M. Rork
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Correspondence to Adam M. Rork.

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The original online version of this article was revised: Modifications have been made to the sentences under Methods and figures 1-5 captions.

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Rork, A.M., Xu, S., Attygalle, A. et al. Primary Metabolism co-Opted for Defensive Chemical Production in the Carabid Beetle, Harpalus pensylvanicus. J Chem Ecol 47, 334–349 (2021). https://doi.org/10.1007/s10886-021-01253-2

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  • DOI: https://doi.org/10.1007/s10886-021-01253-2

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