Chemotaxonomic characterisation of the thaumarchaeal lipidome

Felix J Elling, Martin Könneke (Corresponding Author), Graeme W Nicol, Michaela Stieglmeier, Barbara Bayer, Eva Spieck, José R de la Torre, Kevin W Becker, Michael Thomm, James I Prosser, Gerhard J Herndl, Christa Schleper, Kai-Uwe Hinrichs

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102 Citations (Scopus)
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Abstract

Thaumarchaeota are globally distributed and abundant microorganisms occurring in diverse habitats and thus represent a major source of archaeal lipids. The scope of lipids as taxonomic markers in microbial ecological studies is limited by the scarcity of comparative data on the membrane lipid composition of cultivated representatives, including the phylum Thaumarchaeota. Here, we comprehensively describe the core and intact polar lipid (IPL) inventory of ten ammonia‐oxidising thaumarchaeal cultures representing all four characterized phylogenetic clades. IPLs of these thaumarchaeal strains are generally similar and consist of membrane‐spanning, glycerol dibiphytanyl glycerol tetraethers with monoglycosyl, diglycosyl, phosphohexose and hexose‐phosphohexose headgroups. However, the relative abundances of these IPLs and their core lipid compositions differ systematically between the phylogenetic subgroups, indicating high potential for chemotaxonomic distinction of thaumarchaeal clades. Comparative lipidomic analyses of 19 euryarchaeal and crenarchaeal strains suggested that the lipid methoxy archaeol is synthesized exclusively by Thaumarchaeota and may thus represent a diagnostic lipid biomarker for this phylum. The unprecedented diversity of the thaumarchaeal lipidome with 118 different lipids suggests that membrane lipid composition and adaptation mechanisms in Thaumarchaeota are more complex than previously thought and include unique lipids with as yet unresolved properties.

Original languageEnglish
Pages (from-to)2681-2700
Number of pages20
JournalEnvironmental Microbiology
Volume19
Issue number7
Early online date19 May 2017
DOIs
Publication statusPublished - Jul 2017

Bibliographical note

Acknowledgements
The authors thank the two anonymous reviewers for providing valuable comments that helped improve an earlier version of this manuscript. We thank J.S. Lipp and L.P. Wormer for assistance with UPLC-MS analysis. R. Bittner (University of Vienna), J. Ross (University of Aberdeen), and V. Russell (San Francisco State University) are thanked for assistance with cultivation and lipid analysis. We thank M.Y. Kellermann for providing extracts of H. volcanii and H. lacusprofundi. The study was funded by the Deutsche Forschungsgemeinschaft through the Gottfried Wilhelm Leibniz Prize awarded to K.-U. Hinrichs (Hi 616-14-1) and grant Inst 144/300-1 (LC-qToF system), and the Heisenberg fellowship awarded to M. Konneke KO 3651/3-1). Procedures for the analysis of lipids were implemented through research funded by the European Research Council under the European Union’s Seventh Framework Programme–‘‘Ideas’’, ERC grant agreement No. 247153 (Advanced Grant DARCLIFE; PI: K.-U.H.). B. Bayer and G.J. Herndl were supported by the Austrian Science Fund (FWF) project: I486 B09 and the European Research Council under the European Community’s Seventh Framework Program (FP7/2007-2013)/ERC grant agreement No. 268595 (MEDEA project) to GJH. M. Stieglmeier was supported by the Austrian Science Fund (FWF) project P25369-B22 granted to CS.

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