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Lipidomics in archaeal membrane adaptation to environmental stresses and growth conditions: A review of culture-based physiological studies

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Abstract

Membrane lipids are thought to be a crucial part of the homeoviscous adaptation of archaea to extreme conditions. This article reviews the recent lipidomic studies of physiological membrane adaptations of archaea, assesses the biomolecular basis of an organic paleothermometer, TEX86, and contemplates the future directions of archaeal lipidomics. The studies of extremophilic archaea have revealed that at least three different molecular mechanisms are involved in membrane adaptation of archaea: (1) regulation of the number of cyclopentane rings of caldarchaeol, (2) alteration of the diether-to-tetraether lipid ratio, and (3) variation of the proportion of saturated and unsaturated lipids. However, most of the studies have focused on a limited number of archaeal ether-linked lipids, such as glycerol dialkyl glycerol tetraethers (GDGTs), which only represent a fraction of the entire lipidome. Environmental factors such as growth temperature and pH have been most frequently reported, but biotic factors, including growth phases, nutrition, and enzymatic activities affecting the membrane lipid composition are often overlooked. Membrane lipids of mesophilic ammonia-oxidizing marine Thaumarchaeota have been applied in the reconstruction of past sea surface temperatures. However, recent culture-based physiological studies have demonstrated that non-thermal biotic factors, including dissolved oxygen, ammonia oxidation rate and the growth rate, are the main drivers of GDGT cyclization in Nitrosopumilus maritimus. Moreover, other related strains or ecotypes exhibit a markedly different set of stress adaptations. A trend is now developing to examine the whole lipid profile (lipidome) for studies of archaeal physiology and biochemistry related to lipid biosynthesis (lipidomics) to gain a better understanding of the biological mechanisms underpinning the applications of membrane lipid-based proxies in biogeochemical or ecological research.

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Acknowledgements

Special thanks to Tommy J. Phelps and Susan Pfiffner, who provided valuable comments that significantly improved the quality of the paper. This work was supported by National Key R & D Program of China (Grant Nos. 2016YFA0601101 & 2018YFA0605800), the National Natural Science Foundation of China (Grants Nos. 91851210, 41530105 & 41806085), the Key Project of Natural Science Foundation of Guangdong Province (Grants No. 2018B030311016), the Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Southern University of Science and Technology (Grant No. ZDSYS201802081843490), Shenzhen International Collaboration Project (Grant No. GJHZ20180928155004783), and the Laboratory for Marine Geology, Qingdao National Laboratory for Marine Science and Technology (Grant No. MGQNLM-TD201810).

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Authors and Affiliations

  1. Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science & Engineering, Southern University of Science and Technology, Shenzhen, 518055, China

    Kai P. Law, Xinxin Li & Chuanlun Zhang

  2. SUSTech Academy for Advanced Interdisciplinary Studies, Southern University of Science and Technology, Shenzhen, 518055, China

    Kai P. Law

  3. Shanghai Sheshan National Geophysical Observatory and Research Station, Shanghai, 201600, China

    Chuanlun Zhang

Authors
  1. Kai P. Law
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  2. Xinxin Li
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  3. Chuanlun Zhang
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Correspondence to Kai P. Law.

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Law, K.P., Li, X. & Zhang, C. Lipidomics in archaeal membrane adaptation to environmental stresses and growth conditions: A review of culture-based physiological studies. Sci. China Earth Sci. 63, 790–807 (2020). https://doi.org/10.1007/s11430-019-9571-2

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  • DOI: https://doi.org/10.1007/s11430-019-9571-2

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