skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Abstract

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 bymore » 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.« less

Authors:
ORCiD logo; ; ; ; ORCiD logo; ORCiD logo; ORCiD logo
Publication Date:
Research Org.:
Univ. of Illinois at Urbana-Champaign, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division; National Science Foundation (NSF); Simons Collaboration on the Origins of Life (SCOL)
OSTI Identifier:
1569769
Alternate Identifier(s):
OSTI ID: 1595769
Grant/Contract Number:  
FG02-02ER15296; 511568; 1752564
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 45; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; GDGT; radical SAM; Sulfolobus; paleotemperature proxies

Citation Formats

Zeng, Zhirui, Liu, Xiao-Lei, Farley, Kristen R., Wei, Jeremy H., Metcalf, William W., Summons, Roger E., and Welander, Paula V. GDGT cyclization proteins identify the dominant archaeal sources of tetraether lipids in the ocean. United States: N. p., 2019. Web. doi:10.1073/pnas.1909306116.
Zeng, Zhirui, Liu, Xiao-Lei, Farley, Kristen R., Wei, Jeremy H., Metcalf, William W., Summons, Roger E., & Welander, Paula V. GDGT cyclization proteins identify the dominant archaeal sources of tetraether lipids in the ocean. United States. doi:10.1073/pnas.1909306116.
Zeng, Zhirui, Liu, Xiao-Lei, Farley, Kristen R., Wei, Jeremy H., Metcalf, William W., Summons, Roger E., and Welander, Paula V. Mon . "GDGT cyclization proteins identify the dominant archaeal sources of tetraether lipids in the ocean". United States. doi:10.1073/pnas.1909306116.
@article{osti_1569769,
title = {GDGT cyclization proteins identify the dominant archaeal sources of tetraether lipids in the ocean},
author = {Zeng, Zhirui and Liu, Xiao-Lei and Farley, Kristen R. and Wei, Jeremy H. and Metcalf, William W. and Summons, Roger E. and Welander, Paula V.},
abstractNote = {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.},
doi = {10.1073/pnas.1909306116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 45,
volume = 116,
place = {United States},
year = {2019},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1073/pnas.1909306116

Citation Metrics:
Cited by: 8 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota
journal, October 2002

  • Damsté, Jaap S. Sinninghe; Schouten, Stefan; Hopmans, Ellen C.
  • Journal of Lipid Research, Vol. 43, Issue 10
  • DOI: 10.1194/jlr.M200148-JLR200

Versatile Genetic Tool Box for the Crenarchaeote Sulfolobus acidocaldarius
journal, January 2012

  • Wagner, Michaela; van Wolferen, Marleen; Wagner, Alexander
  • Frontiers in Microbiology, Vol. 3
  • DOI: 10.3389/fmicb.2012.00214

Characterization of the precursor of tetraether lipid biosynthesis in the thermoacidophilic archaeon Thermoplasma acidophilum
journal, February 2003


Radical S -Adenosylmethionine Enzymes
journal, January 2014

  • Broderick, Joan B.; Duffus, Benjamin R.; Duschene, Kaitlin S.
  • Chemical Reviews, Vol. 114, Issue 8
  • DOI: 10.1021/cr4004709

Biosynthesis of 15,16-dimethyltriacontanedioic acid (diabolic acid) from [16-2H3]- and [14-2H2]-palmitic acids
journal, January 1992

  • Fitz, Wolfgang; Arigoni, Duilio
  • Journal of the Chemical Society, Chemical Communications, Issue 20
  • DOI: 10.1039/c39920001533

Biosynthesis of isoprenoid membranes in the methanogenic archaebacterium Methanospirillum hungatei
journal, April 1988

  • Poulter, C. Dale.; Aoki, Tadashi.; Daniels, Lacy.
  • Journal of the American Chemical Society, Vol. 110, Issue 8
  • DOI: 10.1021/ja00216a041

13C-NMR assignments and biosynthetic data for the ether lipids of Caldariella
journal, January 1977


A re-evaluation of the archaeal membrane lipid biosynthetic pathway
journal, May 2014

  • Villanueva, Laura; Damsté, Jaap S. Sinninghe; Schouten, Stefan
  • Nature Reviews Microbiology, Vol. 12, Issue 6
  • DOI: 10.1038/nrmicro3260

Effect of growth temperature on ether lipid biochemistry in Archaeoglobus fulgidus
journal, December 2007


Community Genomics Among Stratified Microbial Assemblages in the Ocean's Interior
journal, January 2006


A phylogenomic and ecological analysis of the globally abundant Marine Group II archaea (Ca. Poseidoniales ord. nov.)
journal, October 2018


Sulfolobus: A new genus of sulfur-oxidizing bacteria living at low pH and high temperature
journal, January 1972

  • Brock, Thomas D.; Brock, Katherine M.; Belly, Robert T.
  • Archiv fur Mikrobiologie, Vol. 84, Issue 1, p. 54-68
  • DOI: 10.1007/BF00408082

Effects of temperature on ether lipid composition of Caldariella acidophila
journal, January 1980


An Analysis of Thaumarchaeota Populations from the Northern Gulf of Mexico
journal, January 2013

  • Tolar, Bradley B.; King, Gary M.; Hollibaugh, James T.
  • Frontiers in Microbiology, Vol. 4
  • DOI: 10.3389/fmicb.2013.00072

Adaptations to energy stress dictate the ecology and evolution of the Archaea
journal, March 2007


Influence of ammonia oxidation rate on thaumarchaeal lipid composition and the TEX 86 temperature proxy
journal, June 2016

  • Hurley, Sarah J.; Elling, Felix J.; Könneke, Martin
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 28
  • DOI: 10.1073/pnas.1518534113

The lipids of archaebacteria
journal, January 1988


Chemical structure of the ether lipids of thermophilic acidophilic bacteria of the Caldariella group
journal, January 1977


Importance of the isopropylidene terminal of geranylgeranyl group for the formation of tetraether lipid in methanogenic archaea
journal, April 2003


Identification of a methylase required for 2-methylhopanoid production and implications for the interpretation of sedimentary hopanes
journal, April 2010

  • Welander, P. V.; Coleman, M. L.; Sessions, A. L.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 19
  • DOI: 10.1073/pnas.0912949107

Different Biosynthetic Pathways to Fosfomycin in Pseudomonas syringae and Streptomyces Species
journal, May 2012

  • Kim, Seung Young; Ju, Kou-San; Metcalf, William W.
  • Antimicrobial Agents and Chemotherapy, Vol. 56, Issue 8
  • DOI: 10.1128/AAC.06478-11

Confounding effects of oxygen and temperature on the TEX 86 signature of marine Thaumarchaeota
journal, August 2015

  • Qin, Wei; Carlson, Laura T.; Armbrust, E. Virginia
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 35
  • DOI: 10.1073/pnas.1501568112

Elucidation of the B urkholderia cenocepacia hopanoid biosynthesis pathway uncovers functions for conserved proteins in hopanoid-producing bacteria : Hopanoid biosynthesis in
journal, June 2014

  • Schmerk, Crystal L.; Welander, Paula V.; Hamad, Mohamad A.
  • Environmental Microbiology, Vol. 17, Issue 3
  • DOI: 10.1111/1462-2920.12509

Lipids of marine Archaea: Patterns and provenance in the water-column and sediments
journal, July 2007

  • Turich, Courtney; Freeman, Katherine H.; Bruns, Mary Ann
  • Geochimica et Cosmochimica Acta, Vol. 71, Issue 13
  • DOI: 10.1016/j.gca.2007.04.013

Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures?
journal, November 2002

  • Schouten, Stefan; Hopmans, Ellen C.; Schefuß, Enno
  • Earth and Planetary Science Letters, Vol. 204, Issue 1-2
  • DOI: 10.1016/S0012-821X(02)00979-2

Ring Index: A new strategy to evaluate the integrity of TEX 86 paleothermometry : QUALITY CONTROL FOR TEX
journal, February 2016

  • Zhang, Yi Ge; Pagani, Mark; Wang, Zhengrong
  • Paleoceanography, Vol. 31, Issue 2
  • DOI: 10.1002/2015PA002848

Biosynthesis of Ether-Type Polar Lipids in Archaea and Evolutionary Considerations
journal, March 2007

  • Koga, Y.; Morii, H.
  • Microbiology and Molecular Biology Reviews, Vol. 71, Issue 1, p. 97-120
  • DOI: 10.1128/MMBR.00033-06

IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes
journal, October 2018

  • Chen, I-Min A.; Chu, Ken; Palaniappan, Krishna
  • Nucleic Acids Research, Vol. 47, Issue D1
  • DOI: 10.1093/nar/gky901

Glycerol configurations of environmental GDGTs investigated using a selective sn2 ether cleavage protocol
journal, February 2019


Reply to Schouten et al.: Marine Group II planktonic Euryarchaeota are significant contributors to tetraether lipids in the ocean
journal, September 2014

  • Lincoln, S. A.; Wai, B.; Eppley, J. M.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 41
  • DOI: 10.1073/pnas.1416736111

Disaggregation of Methanosarcina spp. and Growth as Single Cells at Elevated Osmolarity
journal, January 1993


Biosynthesis of archaeal membrane ether lipids
journal, January 2014


Are Marine Group II Euryarchaeota significant contributors to tetraether lipids in the ocean?
journal, September 2014

  • Schouten, S.; Villanueva, L.; Hopmans, E. C.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 41
  • DOI: 10.1073/pnas.1416176111

The organic geochemistry of glycerol dialkyl glycerol tetraether lipids: A review
journal, January 2013


Planktonic Euryarchaeota are a significant source of archaeal tetraether lipids in the ocean
journal, June 2014

  • Lincoln, Sara A.; Wai, Brenner; Eppley, John M.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 27
  • DOI: 10.1073/pnas.1409439111

Marine Group II Archaea, potentially important players in the global ocean carbon cycle
journal, October 2015

  • Zhang, Chuanlun L.; Xie, Wei; Martin-Cuadrado, Ana-Belen
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.01108

Calditol-linked membrane lipids are required for acid tolerance in Sulfolobus acidocaldarius
journal, December 2018

  • Zeng, Zhirui; Liu, Xiao-Lei; Wei, Jeremy H.
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 51
  • DOI: 10.1073/pnas.1814048115