A Novel Approach to Characterize the Lipidome of Marine Archaeon Nitrosopumilus maritimus by Ion Mobility Mass Spectrometry

Abstract

Archaea are differentiated from the other two domains of life by their biomolecular characteristics. One such characteristic is the unique structure and composition of their lipids. Characterization of the whole set of lipids in a biological system (the lipidome) remains technologically challenging. This is because the lipidome is innately complex, and not all lipid species are extractable, separable, or ionizable by a single analytical method. Furthermore, lipids are structurally and chemically diverse. Many lipids are isobaric or isomeric and often indistinguishable by the measurement of mass or even their fragmentation spectra. Here we developed a novel analytical protocol based on liquid chromatography ion mobility mass spectrometry to enhance the coverage of the lipidome and characterize the conformations of archaeal lipids by their collision cross-sections (CCSs). The measurements of ion mobility revealed the gas-phase ion chemistry of representative archaeal lipids and provided further insights into their attributions to the adaptability of archaea to environmental stresses. A comprehensive characterization of the lipidome of mesophilic marine thaumarchaeon, Nitrosopumilus maritimus (strain SCM1) revealed potentially an unreported phosphate- and sulfate-containing lipid candidate by negative ionization analysis. It was the first time that experimentally derived CCS values of archaeal lipids were reported. Discrimination of crenarchaeol and its proposed stereoisomer was, however, not achieved with the resolving power of the SYNAPT G2 ion mobility system, and a high-resolution ion mobility system may be required for future work. Structural and spectral libraries of archaeal lipids were constructed in non-vendor-specific formats and are being made available to the community to promote research of Archaea by lipidomics.

Lipidomic chemotaxonomy aligned with phylogeny of Halobacteria

“…Recent advances in lipidomics with high-resolution mass spectrometry (HRMS) have significantly improved the detection coverage, sensitivity, and throughput. This enables the analysis of a larger number of lipids in a single run (Tsugawa et al, 2020), which have continuously enhanced our knowledge of archaeal lipidome (Knappy et al, 2009;Law et al, 2021). Remarkably, the structural diversity and chemotaxonomic potential have been carefully examined with HRMS-based lipidomic approach for Thaumarchaeota (Elling et al, 2017), halo(alkali)philic methanogens and Halobacteria (Bale et al, 2019).…”

The 3D ultrastructural morphology of a marine ammonia-oxidizing archaeon

“…Previous studies have delved into various aspects of Nitrosopumilus maritimus SCM1, including its physiology like ammonium oxidation, stress adaptation, carbon fixation, genome, metabolome, lipidome, evolution and ecology (Abby et al, 2020; Hodgskiss et al, 2023; Kim et al, 2019; Kitzinger et al, 2020, 2019; Kraft et al, 2022; Law et al, 2021a, 2021b; Leavitt et al, 2023; Li et al, 2018; Martens-Habbena et al, 2009; Qin et al, 2020, 2018, 2014; Walker et al, 2010; Wan et al, 2023; Yang et al, 2021). However, our knowledge of its cellular structure remains limited.…”

Membrane plasticity induced by myo-inositol derived archaeal lipids: chemical synthesis and biophysical characterization

“…5,7 Additionally, the composition of the polar head groups is known to change under different growth conditions but has not been well-documented. 8 The number and diversity of polar head groups that have been detected in Archaea is quite high and due to limitations in current methodologies used in lipid extraction and characterization, 9 there are likely many head groups that have yet to be identified. Changes in lipid polar head group composition help the membrane remain in a functional state by maintaining the proper membrane parameters such as fluidity and permeability under “extreme” conditions.…”