Identification and structure of glycerol dibiphytanyl glycerol tetraether synthase Cody Lloyd 1 , David F. Iwig 2 , Bo Wang 2 , Amie K. Boal 1,2 and Squire J. Booker 1,2,3 1 Department of Biochemistry and Molecular Biology, Pennsylvania State University, USA, 2 The Howard Hughes Medical Institute, Pennsylvania State University, USA, 3 Department of Chemistry, Pennsylvania State University, USA Archaea synthesize isoprenoid-based ether-linked membrane lipids, which enable them to withstand extreme environmental conditions, such as high temperatures, high salinity, and low or high pH values. 1,2 In some archaea, such as Methanocaldococcus jannaschii , these lipids are further modified by forming carbon-carbon bonds between the termini of two lipid tails within one glycerophospholipid to generate the macrocyclic archaeol, or forming two carbon-carbon bonds between the termini of two lipid tails from two glycerophospholipids to generate the macrocycle glycerol dibiphytanyl glycerol tetraether (GDGT). GDGT contains two 40-carbon lipid chains (biphytanyl chains) that span both leaflets of the membrane, providing enhanced stability to extreme conditions. 3 How these specialized lipids are formed has puzzled scientists for decades. 4 The reaction necessitates coupling of two completely inert sp 3 -hybridized carbon centers, which, to our knowledge, has not been observed in nature. Herein, we show that the gene product of mj0619 from Methanocaldococcus jannaschii , which encodes a radical S -adenosylmethionine enzyme, is responsible for biphytanyl chain formation during synthesis of both the macrocyclic archaeol and GDGT membrane lipids. 5 Structures of the enzyme show the presence of four metallocofactors: three [Fe 4 S 4 ] clusters and one mononuclear rubredoxin-like iron ion. In vitro activity determinations show that Csp 3 -Csp 3 bond formation takes place on fully saturated archaeal lipid substrates. Our results not only establish the biosynthetic route for tetraether formation, but enhance the use of GDGT as an ecological proxy in GDGT-based paleoclimatology indices. 6-9 References 1. Jain, S., Caforio, A. & Driessen, A. J. Biosynthesis of archaeal membrane ether lipids. Front Microbiol 5 , 641, doi:10.3389/ fmicb.2014.00641 (2014). 2. Caforio, A. & Driessen, A. J. M. Archaeal phospholipids: Structural properties and biosynthesis. Biochim Biophys Acta Mol Cell Biol Lipids 1862 , 1325-1339, doi:10.1016/j.bbalip.2016.12.006 (2017). 3. Koga, Y. & Morii, H. Biosynthesis of ether-type polar lipids in archaea and evolutionary considerations. Microbiol Mol Biol Rev 71 , 97-120, doi:10.1128/MMBR.00033-06 (2007). 4. Villanueva, L., Damste, J. S. & Schouten, S. A re-evaluation of the archaeal membrane lipid biosynthetic pathway. Nat Rev Microbiol 12 , 438-448, doi:10.1038/nrmicro3260 (2014). 5. Comita, P. B., Gagosian, R. B., Pang, H. & Costello, C. E. Structural elucidation of a unique macrocyclic membrane lipid from a new, extremely thermophilic, deep-sea hydrothermal vent archaebacterium, Methanococcus jannaschii. J Biol Chem 259 , 15234-15241 (1984). 6. Zell, C. et al. Impact of seasonal hydrological variation on the distributions of tetraether lipids along the Amazon River in the central Amazon basin: implications for the MBT/CBT paleothermometer and the BIT index. Front Microbiol 4 , 228, doi:10.3389/fmicb.2013.00228 (2013). 7. Wang, J. X., Xie, W., Zhang, Y. G., Meador, T. B. & Zhang, C. L. Evaluating Production of Cyclopentyl Tetraethers by Marine Group II Euryarchaeota in the Pearl River Estuary and Coastal South China Sea: Potential Impact on the TEX86 Paleothermometer. Front Microbiol 8 , 2077, doi:10.3389/fmicb.2017.02077 (2017). 8. Castañeda, I. S. & Schouten, S. A review of molecular organic proxies for examining modern and ancient lacustrine environments. Quaternary Science Reviews 30 , 2851-2891, doi:10.1016/j.quascirev.2011.07.009 (2011). 9. Wang, M., Zheng, Z., Zong, Y., Man, M. & Tian, L. Sci Rep 9 , 2761, doi:10.1038/s41598-019-39147-9 (2019).
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