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De novo biosynthesis of simple aromatic compounds by an arthropod (Archegozetes longisetosus)

Brückner, Adrian and Kaltenpoth, Martin and Heethoff, Michael (2020) De novo biosynthesis of simple aromatic compounds by an arthropod (Archegozetes longisetosus). Proceedings of the Royal Society of London. Series B, Biological Sciences, 287 (1934). Art. No. 20201429. ISSN 0962-8452. PMCID PMC7542773. doi:10.1098/rspb.2020.1429.

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The ability to synthesize simple aromatic compounds is well known from bacteria, fungi and plants, which all share an exclusive biosynthetic route—the shikimic acid pathway. Some of these organisms further evolved the polyketide pathway to form core benzenoids via a head-to-tail condensation of polyketide precursors. Arthropods supposedly lack the ability to synthesize aromatics and instead rely on aromatic amino acids acquired from food, or from symbiotic microorganisms. The few studies purportedly showing de novo biosynthesis via the polyketide synthase (PKS) pathway failed to exclude endosymbiotic bacteria, so their results are inconclusive. We investigated the biosynthesis of aromatic compounds in defence secretions of the oribatid mite Archegozetes longisetosus. Exposing the mites to a diet containing high concentrations of antibiotics removed potential microbial partners but did not affect the production of defensive benzenoids. To gain insights into benzenoid biosynthesis, we fed mites with stable-isotope labelled precursors and monitored incorporation with mass spectrometry. Glucose, malonic acid and acetate, but not phenylalanine, were incorporated into the benzenoids, further evidencing autogenous biosynthesis. Whole-transcriptome sequencing with hidden Markov model profile search of protein domain families and subsequent phylogenetic analysis revealed a putative PKS domain similar to an actinobacterial PKS, possibly indicating a horizontal gene transfer.

Item Type:Article
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URLURL TypeDescription Material CentralArticle
Brückner, Adrian0000-0002-9184-8562
Kaltenpoth, Martin0000-0001-9450-0345
Heethoff, Michael0000-0003-3453-4871
Additional Information:© 2020 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License, which permits unrestricted use, provided the original author and source are credited. Manuscript received 16/06/2020; Manuscript accepted 11/08/2020; Published online 02/09/2020; Published in print 09/09/2020. We thank Roy A. Norton for improving the manuscript and Benjamin Weiss, Dagmar Klebsch and Maximilian Maschler for their technical assistance. We are further grateful to Julian Wagner who helped with bioinformatics. Ethics: There are no legal restrictions on working with mites. Data accessibility: The datasets supporting this article have been uploaded as part of the electronic supplementary material. Authors' contributions: A.B. designed research, performed chemical analysis and transcriptomic work, analysed the data and took lead in drafting the manuscript; M.K. performed molecular and microscopic research, analysed the data and helped drafting the manuscript; M.H. designed research, performed chemical analysis, analysed the data and drafted the manuscript. All authors gave final approval for publication and agree to be held accountable for the work performed therein. The authors declare no conflict of interest. A.B. is a Simons Fellow of the Life Sciences Research Foundation and was previously supported by a PhD scholarship from the German National Academic Foundation. This study was supported by the German Research Foundation (DFG; HE 4593/5-1) to MH, a pilot grant of Caltech's Center for Environmental Microbial Interactions (CEMI; CEMI-19-028) to A.B. and a Consolidator Grant of the European Research Council (ERC CoG 819585 ‘SYMBeetle’) to M.K.
Group:Caltech Center for Environmental Microbial Interactions (CEMI)
Funding AgencyGrant Number
Simons FoundationUNSPECIFIED
Studienstiftung des deutschen VolkesUNSPECIFIED
Deutsche Forschungsgemeinschaft (DFG)HE 4593/5-1
Caltech Center for Environmental Microbial Interactions (CEMI)CEMI-19-028
European Research Council (ERC)819585
Subject Keywords:biosynthetic pathways, Benzenoids, chemical ecology, Oribatid mites, Chemical defence
Issue or Number:1934
PubMed Central ID:PMC7542773
Record Number:CaltechAUTHORS:20200908-154844861
Persistent URL:
Official Citation:Brückner A, Kaltenpoth M, Heethoff M. 2020 De novo biosynthesis of simple aromatic compounds by an arthropod (Archegozetes longisetosus). Proc. R. Soc. B. 287: 20201429;
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:105281
Deposited By: Tony Diaz
Deposited On:08 Sep 2020 23:05
Last Modified:05 Jan 2022 23:05

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