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The Metabolome of Associations between Xylem-Feeding Insects and their Bacterial Symbionts

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Abstract

Metabolomics has increasingly led to important insights in chemical ecology by identifying environmentally relevant small molecules that mediate inter-organismal interactions. Nevertheless, the application of metabolomics to investigate interactions between phytophagous insects and their microbial symbionts remains underutilized. Here, we investigated the metabolomes of the bacteriomes (organs bearing symbiotic bacteria) isolated from natural populations of five species of xylem-feeding insects. We identified three patterns. First, the metabolomes varied among the five species, likely influenced by insect phylogeny, food plant and taxonomic identity of the symbionts. Second, the ratio of glutamine: glutamate in the bacteriomes was 0.7–3.6 to 1, indicative of nitrogen-sufficient metabolism and raising the possibility that the insect sustains nitrogen-enriched status of the bacteriomes despite the nitrogen scarcity of the xylem diet. Finally, bacteriomes from insect species bearing genetically-similar symbionts displayed limited variation in their metabolomes, suggesting that the metabolic pattern of the bacteriome metabolic pools is correlated with the genetic repertoire of the symbionts. Altogether, these metabolomic patterns yield specific hypotheses of underlying processes that are testable by wider sampling of natural populations and experimental study.

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Acknowledgements

We thank Jason Dombroskie (Cornell University Insect Collection) for assistance with insect identification and Frances Blow, Alyssa Bost, Seung H. Chung, Lu Liu, Tadeo Kaweesi and Dantong Zhu for assistance with insect dissections. This study was funded by National Science Foundation grant IOS-1354743.

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  1. Ludmilla Aristilde

    Present address: Department of Civil and Environmental Engineering, McCormick School of Engineering and Applied Science, Northwestern University, Evanston, Il 60208, USA

Authors and Affiliations

  1. Department of Entomology, Cornell University, Comstock Hall, Ithaca, NY, 14853, USA

    Nana Y. D. Ankrah, Freya Q. Zhang & Angela E. Douglas

  2. Department of Biological and Environmental Engineering, Cornell University, Ithaca, NY, 14853, USA

    Rebecca A. Wilkes & Ludmilla Aristilde

  3. Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY, 14853, USA

    Angela E. Douglas

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  1. Nana Y. D. Ankrah
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Contributions

N.Y.D.A., L.A., and A.E.D. designed research; N.Y.D.A. and F.Z. performed research; R.A.W. and L.A. performed mass spectrometry analysis; N.Y.D.A. analyzed data; N.Y.D.A. and A.E.D. wrote the first draft of the paper; manuscript revisions made by all authors.

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Correspondence to Ludmilla Aristilde or Angela E. Douglas.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Figure S1

Absolute quantification of select central carbon, nucleotide and non-proteinogenic amino acid metabolites in the combined bacteriomes of the five insect species. Absolute metabolite concentrations were autoscaled (mean-centered and divided by the standard deviation of each variable) prior to statistical analysis. Significantly different (P < 0.05) samples by Tukey’s HSD posthoc test indicated by different letters. Plots with no letters represent metabolites with missing values that were excluded from analysis of variance (ANOVA). (PDF 514 kb)

Figure S2

Absolute quantification of select central carbon, nucleotide and non-proteinogenic amino acid metabolites in Sulcia- containing bacteriomes of spittlebug species. Absolute metabolite concentrations were autoscaled (mean-centered and divided by the standard deviation of each variable) prior to statistical analysis. Significantly different (P < 0.05) samples by Tukey’s HSD posthoc test indicated by different letters. Plots with no letters represent metabolites with missing values that were excluded from analysis of variance (ANOVA). (PDF 458 kb)

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Ankrah, N.Y.D., Wilkes, R.A., Zhang, F.Q. et al. The Metabolome of Associations between Xylem-Feeding Insects and their Bacterial Symbionts. J Chem Ecol 46, 735–744 (2020). https://doi.org/10.1007/s10886-019-01136-7

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