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

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America

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.

Research Organization:
Univ. of Illinois at Urbana-Champaign, IL (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; National Science Foundation (NSF); Simons Collaboration on the Origins of Life (SCOL)
Grant/Contract Number:
FG02-02ER15296; 511568; 1752564
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 Vol. 116 Journal Issue: 45; ISSN 0027-8424
Publisher:
National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 46 works
Citation information provided by
Web of Science

References (43)

Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota journal October 2002
Versatile Genetic Tool Box for the Crenarchaeote Sulfolobus acidocaldarius journal January 2012
Characterization of the precursor of tetraether lipid biosynthesis in the thermoacidophilic archaeon Thermoplasma acidophilum journal February 2003
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 journal April 2016
Radical S -Adenosylmethionine Enzymes journal January 2014
Biosynthesis of 15,16-dimethyltriacontanedioic acid (diabolic acid) from [16-2H3]- and [14-2H2]-palmitic acids journal January 1992
Biosynthesis of isoprenoid membranes in the methanogenic archaebacterium Methanospirillum hungatei journal April 1988
Temperature and pH controls on glycerol dibiphytanyl glycerol tetraether lipid composition in the hyperthermophilic crenarchaeon Acidilobus sulfurireducens journal December 2010
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
Disaggregation of Methanosarcina spp. and Growth as Single Cells at Elevated Osmolarity journal January 1993
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
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
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
The lipids of archaebacteria journal January 1988
Chemical structure of the ether lipids of thermophilic acidophilic bacteria of the Caldariella group journal January 1977
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 journal March 2010
Importance of the isopropylidene terminal of geranylgeranyl group for the formation of tetraether lipid in methanogenic archaea journal April 2003
Identification and characterization of Rhodopseudomonas palustris TIE-1 hopanoid biosynthesis mutants: Hopanoid biosynthesis in R. palustris TIE-1 journal January 2012
Geranylgeranyl reductase involved in the biosynthesis of archaeal membrane lipids in the hyperthermophilic archaeon Archaeoglobus fulgidus: Archaetidic acid-synthesizing archaeal reductase journal January 2007
Identification of a methylase required for 2-methylhopanoid production and implications for the interpretation of sedimentary hopanes journal April 2010
Different Biosynthetic Pathways to Fosfomycin in Pseudomonas syringae and Streptomyces Species journal May 2012
Confounding effects of oxygen and temperature on the TEX 86 signature of marine Thaumarchaeota journal August 2015
Elucidation of the B urkholderia cenocepacia hopanoid biosynthesis pathway uncovers functions for conserved proteins in hopanoid-producing bacteria : Hopanoid biosynthesis in journal June 2014
Lipids of marine Archaea: Patterns and provenance in the water-column and sediments journal July 2007
Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures? journal November 2002
Ring Index: A new strategy to evaluate the integrity of TEX 86 paleothermometry : QUALITY CONTROL FOR TEX journal February 2016
Biosynthesis of Ether-Type Polar Lipids in Archaea and Evolutionary Considerations journal March 2007
IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes journal October 2018
Predominance of parallel glycerol arrangement in archaeal tetraethers from marine sediments: Structural features revealed from degradation products journal January 2018
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
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
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
Marine Group II Archaea, potentially important players in the global ocean carbon cycle journal October 2015
Calditol-linked membrane lipids are required for acid tolerance in Sulfolobus acidocaldarius journal December 2018

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