GDGT cyclization proteins identify the dominant archaeal sources of tetraether lipids in the ocean

Zeng, Zhirui; Liu, Xiao-Lei; Farley, Kristen R.; Wei, Jeremy H.; Metcalf, William W.; Summons, Roger E.; Welander, Paula V.

doi:10.1073/pnas.1909306116

GDGT cyclization proteins identify the dominant archaeal sources of tetraether lipids in the ocean

Journal Article · Mon Oct 07 00:00:00 EDT 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1909306116· OSTI ID:1569769

; Liu, Xiao-Lei; Farley, Kristen R.; Wei, Jeremy H.; ; ;

Glycerol dibiphytanyl glycerol tetraethers (GDGTs) are distinctive archaeal membrane-spanning lipids with up to eight cyclopentane rings and/or one cyclohexane ring. The number of rings added to the GDGT core structure can vary as a function of environmental conditions, such as changes in growth temperature. This physiological response enables cyclic GDGTs preserved in sediments to be employed as proxies for reconstructing past global and regional temperatures and to provide fundamental insights into ancient climate variability. Yet, confidence in GDGT-based paleotemperature proxies is hindered by uncertainty concerning the archaeal communities contributing to GDGT pools in modern environments and ambiguity in the environmental and physiological factors that affect GDGT cyclization in extant archaea. To properly constrain these uncertainties, a comprehensive understanding of GDGT biosynthesis is required. Here in this paper, we identify 2 GDGT ring synthases, GrsA and GrsB, essential for GDGT ring formation in Sulfolobus acidocaldarius. Both proteins are radical S-adenosylmethionine proteins, indicating that GDGT cyclization occurs through a free radical mechanism. In addition, we demonstrate that GrsA introduces rings specifically at the C-7 position of the core GDGT lipid, while GrsB cyclizes at the C-3 position, suggesting that cyclization patterns are differentially controlled by 2 separate enzymes and potentially influenced by distinct environmental factors. Finally, phylogenetic analyses of the Grs proteins reveal that marine Thaumarchaeota, and not Euryarchaeota, are the dominant source of cyclized GDGTs in open ocean settings, addressing a major source of uncertainty in GDGT-based paleotemperature proxy applications.

View Journal Article

Research Organization:: Univ. of Illinois at Urbana-Champaign, IL (United States)

Sponsoring Organization:: National Science Foundation (NSF); Simons Collaboration on the Origins of Life (SCOL); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: FG02-02ER15296

OSTI ID:: 1569769

Alternate ID(s):: OSTI ID: 1595769

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 45 Vol. 116; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (43)

Ring Index: A new strategy to evaluate the integrity of TEX ₈₆ paleothermometry : QUALITY CONTROL FOR TEX Zhang, Yi Ge; Pagani, Mark; Wang, Zhengrong Paleoceanography, Vol. 31, Issue 2 https://doi.org/10.1002/2015PA002848	journal	February 2016
Novel archaeal tetraether lipids with a cyclohexyl ring identified in Fayetteville Green Lake, NY, and other sulfidic lacustrine settings : Identification of novel archaeal tetraethers with a cyclohexyl ring Liu, Xiao-Lei; De Santiago Torio, Ana; Bosak, Tanja Rapid Communications in Mass Spectrometry, Vol. 30, Issue 10 https://doi.org/10.1002/rcm.7549	journal	April 2016
Sulfolobus: A new genus of sulfur-oxidizing bacteria living at low pH and high temperature Brock, Thomas D.; Brock, Katherine M.; Belly, Robert T. Archiv fur Mikrobiologie, Vol. 84, Issue 1, p. 54-68 https://doi.org/10.1007/BF00408082	journal	January 1972
Characterization of the precursor of tetraether lipid biosynthesis in the thermoacidophilic archaeon Thermoplasma acidophilum Nemoto, Naoki; Shida, Yasuo; Shimada, Haruo Extremophiles, Vol. 7, Issue 3 https://doi.org/10.1007/s00792-003-0315-x	journal	February 2003
Effect of growth temperature on ether lipid biochemistry in Archaeoglobus fulgidus Lai, Denton; Springstead, James R.; Monbouquette, Harold G. Extremophiles, Vol. 12, Issue 2 https://doi.org/10.1007/s00792-007-0126-6	journal	December 2007
Temperature and pH controls on glycerol dibiphytanyl glycerol tetraether lipid composition in the hyperthermophilic crenarchaeon Acidilobus sulfurireducens Boyd, Eric S.; Pearson, Ann; Pi, Yundan Extremophiles, Vol. 15, Issue 1 https://doi.org/10.1007/s00792-010-0339-y	journal	December 2010
13C-NMR assignments and biosynthetic data for the ether lipids of Caldariella de Rosa, Mario; de Rosa, Salvatore; Gambacorta, Agata Phytochemistry, Vol. 16, Issue 12 https://doi.org/10.1016/0031-9422(77)80094-0	journal	January 1977
Chemical structure of the ether lipids of thermophilic acidophilic bacteria of the Caldariella group de Rosa, Mario; de Rosa, Salvatore; Gambacorta, Agata Phytochemistry, Vol. 16, Issue 12 https://doi.org/10.1016/0031-9422(77)80105-2	journal	January 1977
Effects of temperature on ether lipid composition of Caldariella acidophila De Rosa, Mario; Esposito, Enrico; Gambacorta, Agata Phytochemistry, Vol. 19, Issue 5 https://doi.org/10.1016/0031-9422(80)85120-X	journal	January 1980
The lipids of archaebacteria De Rosa, Mario; Gambacorta, Agata Progress in Lipid Research, Vol. 27, Issue 3 https://doi.org/10.1016/0163-7827(88)90011-2	journal	January 1988
Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures? Schouten, Stefan; Hopmans, Ellen C.; Schefuß, Enno Earth and Planetary Science Letters, Vol. 204, Issue 1-2 https://doi.org/10.1016/S0012-821X(02)00979-2	journal	November 2002
Importance of the isopropylidene terminal of geranylgeranyl group for the formation of tetraether lipid in methanogenic archaea Eguchi, Tadashi; Nishimura, Yuji; Kakinuma, Katsumi Tetrahedron Letters, Vol. 44, Issue 16 https://doi.org/10.1016/S0040-4039(03)00627-0	journal	April 2003
Lipids of marine Archaea: Patterns and provenance in the water-column and sediments Turich, Courtney; Freeman, Katherine H.; Bruns, Mary Ann Geochimica et Cosmochimica Acta, Vol. 71, Issue 13 https://doi.org/10.1016/j.gca.2007.04.013	journal	July 2007
The organic geochemistry of glycerol dialkyl glycerol tetraether lipids: A review Schouten, Stefan; Hopmans, Ellen C.; Sinninghe Damsté, Jaap S. Organic Geochemistry, Vol. 54 https://doi.org/10.1016/j.orggeochem.2012.09.006	journal	January 2013
Predominance of parallel glycerol arrangement in archaeal tetraethers from marine sediments: Structural features revealed from degradation products Liu, Xiao-Lei; Lipp, Julius S.; Birgel, Daniel Organic Geochemistry, Vol. 115 https://doi.org/10.1016/j.orggeochem.2017.09.009	journal	January 2018
Glycerol configurations of environmental GDGTs investigated using a selective sn2 ether cleavage protocol Liu, Xiao-Lei; Russell, David A.; Bonfio, Claudia Organic Geochemistry, Vol. 128 https://doi.org/10.1016/j.orggeochem.2018.12.003	journal	February 2019
Radical S -Adenosylmethionine Enzymes Broderick, Joan B.; Duffus, Benjamin R.; Duschene, Kaitlin S. Chemical Reviews, Vol. 114, Issue 8 https://doi.org/10.1021/cr4004709	journal	January 2014
Biosynthesis of isoprenoid membranes in the methanogenic archaebacterium Methanospirillum hungatei Poulter, C. Dale.; Aoki, Tadashi.; Daniels, Lacy. Journal of the American Chemical Society, Vol. 110, Issue 8 https://doi.org/10.1021/ja00216a041	journal	April 1988
Adaptations to energy stress dictate the ecology and evolution of the Archaea Valentine, David L. Nature Reviews Microbiology, Vol. 5, Issue 4 https://doi.org/10.1038/nrmicro1619	journal	March 2007
A re-evaluation of the archaeal membrane lipid biosynthetic pathway Villanueva, Laura; Damsté, Jaap S. Sinninghe; Schouten, Stefan Nature Reviews Microbiology, Vol. 12, Issue 6 https://doi.org/10.1038/nrmicro3260	journal	May 2014
A phylogenomic and ecological analysis of the globally abundant Marine Group II archaea (Ca. Poseidoniales ord. nov.) Rinke, Christian; Rubino, Francesco; Messer, Lauren F. The ISME Journal, Vol. 13, Issue 3 https://doi.org/10.1038/s41396-018-0282-y	journal	October 2018
Biosynthesis of 15,16-dimethyltriacontanedioic acid (diabolic acid) from [16-2H3]- and [14-2H2]-palmitic acids Fitz, Wolfgang; Arigoni, Duilio Journal of the Chemical Society, Chemical Communications, Issue 20 https://doi.org/10.1039/c39920001533	journal	January 1992
Identification of a methylase required for 2-methylhopanoid production and implications for the interpretation of sedimentary hopanes Welander, P. V.; Coleman, M. L.; Sessions, A. L. Proceedings of the National Academy of Sciences, Vol. 107, Issue 19 https://doi.org/10.1073/pnas.0912949107	journal	April 2010
Planktonic Euryarchaeota are a significant source of archaeal tetraether lipids in the ocean Lincoln, Sara A.; Wai, Brenner; Eppley, John M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 27 https://doi.org/10.1073/pnas.1409439111	journal	June 2014
Are Marine Group II Euryarchaeota significant contributors to tetraether lipids in the ocean? Schouten, S.; Villanueva, L.; Hopmans, E. C. Proceedings of the National Academy of Sciences, Vol. 111, Issue 41 https://doi.org/10.1073/pnas.1416176111	journal	September 2014
Reply to Schouten et al.: Marine Group II planktonic Euryarchaeota are significant contributors to tetraether lipids in the ocean Lincoln, S. A.; Wai, B.; Eppley, J. M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 41 https://doi.org/10.1073/pnas.1416736111	journal	September 2014
Confounding effects of oxygen and temperature on the TEX ₈₆ signature of marine Thaumarchaeota Qin, Wei; Carlson, Laura T.; Armbrust, E. Virginia Proceedings of the National Academy of Sciences, Vol. 112, Issue 35 https://doi.org/10.1073/pnas.1501568112	journal	August 2015
Influence of ammonia oxidation rate on thaumarchaeal lipid composition and the TEX ₈₆ temperature proxy Hurley, Sarah J.; Elling, Felix J.; Könneke, Martin Proceedings of the National Academy of Sciences, Vol. 113, Issue 28 https://doi.org/10.1073/pnas.1518534113	journal	June 2016
Calditol-linked membrane lipids are required for acid tolerance in Sulfolobus acidocaldarius Zeng, Zhirui; Liu, Xiao-Lei; Wei, Jeremy H. Proceedings of the National Academy of Sciences, Vol. 115, Issue 51 https://doi.org/10.1073/pnas.1814048115	journal	December 2018
IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes Chen, I-Min A.; Chu, Ken; Palaniappan, Krishna Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky901	journal	October 2018
Elucidation of the B urkholderia cenocepacia hopanoid biosynthesis pathway uncovers functions for conserved proteins in hopanoid-producing bacteria : Hopanoid biosynthesis in Schmerk, Crystal L.; Welander, Paula V.; Hamad, Mohamad A. Environmental Microbiology, Vol. 17, Issue 3 https://doi.org/10.1111/1462-2920.12509	journal	June 2014
Identification and characterization of Rhodopseudomonas palustris TIE-1 hopanoid biosynthesis mutants: Hopanoid biosynthesis in R. palustris TIE-1 Welander, P. V.; Doughty, D. M.; Wu, C. -H. Geobiology, Vol. 10, Issue 2 https://doi.org/10.1111/j.1472-4669.2011.00314.x	journal	January 2012
Geranylgeranyl reductase involved in the biosynthesis of archaeal membrane lipids in the hyperthermophilic archaeon Archaeoglobus fulgidus: Archaetidic acid-synthesizing archaeal reductase Murakami, Motomichi; Shibuya, Kyohei; Nakayama, Toru FEBS Journal, Vol. 274, Issue 3 https://doi.org/10.1111/j.1742-4658.2006.05625.x	journal	January 2007
Community Genomics Among Stratified Microbial Assemblages in the Ocean's Interior DeLong, E. F. Science, Vol. 311, Issue 5760 https://doi.org/10.1126/science.1120250	journal	January 2006
Different Biosynthetic Pathways to Fosfomycin in Pseudomonas syringae and Streptomyces Species Kim, Seung Young; Ju, Kou-San; Metcalf, William W. Antimicrobial Agents and Chemotherapy, Vol. 56, Issue 8 https://doi.org/10.1128/AAC.06478-11	journal	May 2012
Biosynthesis of Ether-Type Polar Lipids in Archaea and Evolutionary Considerations Koga, Y.; Morii, H. Microbiology and Molecular Biology Reviews, Vol. 71, Issue 1, p. 97-120 https://doi.org/10.1128/MMBR.00033-06	journal	March 2007
Disaggregation of Methanosarcina spp. and Growth as Single Cells at Elevated Osmolarity Sowers, Kevin R.; Boone, Jane E.; Gunsalus, Robert P. Applied and Environmental Microbiology, Vol. 59, Issue 11 https://doi.org/10.1128/aem.59.11.3832-3839.1993	journal	January 1993
Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota Damsté, Jaap S. Sinninghe; Schouten, Stefan; Hopmans, Ellen C. Journal of Lipid Research, Vol. 43, Issue 10 https://doi.org/10.1194/jlr.M200148-JLR200	journal	October 2002
Versatile Genetic Tool Box for the Crenarchaeote Sulfolobus acidocaldarius Wagner, Michaela; van Wolferen, Marleen; Wagner, Alexander Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00214	journal	January 2012
An Analysis of Thaumarchaeota Populations from the Northern Gulf of Mexico Tolar, Bradley B.; King, Gary M.; Hollibaugh, James T. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00072	journal	January 2013
Biosynthesis of archaeal membrane ether lipids Jain, Samta Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00641	journal	January 2014
Marine Group II Archaea, potentially important players in the global ocean carbon cycle Zhang, Chuanlun L.; Xie, Wei; Martin-Cuadrado, Ana-Belen Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01108	journal	October 2015
Comparison of extraction methods for quantitative analysis of core and intact polar glycerol dialkyl glycerol tetraethers (GDGTs) in environmental samples: Extraction methods for quantitative analysis of GDGTs Huguet, Carme; Martens-Habbena, Willm; Urakawa, Hidetoshi Limnology and Oceanography: Methods, Vol. 8, Issue 4 https://doi.org/10.4319/lom.2010.8.127	journal	March 2010

Similar Records

Cyclization of archaeal membrane lipids impacts membrane protein activity and archaellum formation

Journal Article · Sun May 11 20:00:00 EDT 2025 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:2565534

Tetraether archaeal lipids promote long‐term survival in extreme conditions

Journal Article · Sun Feb 18 19:00:00 EST 2024 · Molecular Microbiology · OSTI ID:2308880

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
GDGT
Sulfolobus
paleotemperature proxies
radical SAM

GDGT cyclization proteins identify the dominant archaeal sources of tetraether lipids in the ocean

Citation Formats

References (43)

Similar Records

Related Subjects