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, 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.
more »
« less
Identification of a protein responsible for the synthesis of archaeal membrane-spanning GDGT lipids
Abstract Glycerol dibiphytanyl glycerol tetraethers (GDGTs) are archaeal monolayer membrane lipids that can provide a competitive advantage in extreme environments. Here, we identify a radical SAM protein, tetraether synthase (Tes), that participates in the synthesis of GDGTs. Attempts to generate a tes-deleted mutant in Sulfolobus acidocaldarius were unsuccessful, suggesting that the gene is essential in this organism. Heterologous expression of tes homologues leads to production of GDGT and structurally related lipids in the methanogen Methanococcus maripaludis (which otherwise does not synthesize GDGTs and lacks a tes homolog, but produces a putative GDGT precursor, archaeol). Tes homologues are encoded in the genomes of many archaea, as well as in some bacteria, in which they might be involved in the synthesis of bacterial branched glycerol dialkyl glycerol tetraethers.
more »
« less
- Award ID(s):
- 1752564
- PAR ID:
- 10340796
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 13
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Numerous temperature and environmental proxies are based on glycerol dialkyl glycerol tetraethers (GDGTs), which are membrane lipids commonly found in the water columns and sediments of lakes. The TEX86 temperature proxy is based on isoprenoid GDGTs, which are produced by members of the archaea, and is used to reconstruct lake surface temperature. Branched GDGTs are lipids produced by bacteria and form the basis of the MBT′5ME temperature proxy. Although many outstanding questions still exist regarding proxies based on isoprenoid and branched GDGTs, both compound classes have been relatively well-studied in lakes. More recently, other types of GDGTs and related compounds are increasingly being reported from lacustrine sediments including hydroxylated GDGTs (OH-GDGTs) and glycerol monoalkyl glycerol tetraethers (GMGTs). In the process of generating lacustrine TEX86 or MBT′5ME temperature records, we noted that OH-GDGTs or GMGTs (or both) are frequently present. The RI-OH, based on OH-GDGTs, recently has been proposed as a temperature proxy in lakes while GMGTs are associated with oxygen-deficient environments. Here we examine distributions of OH-GDGTs and GMGTs in a variety of lakes that also have existing TEX86 or MBT’5ME temperature reconstructions. These lakes range from small to large, shallow to deep, tropical to arctic, differ in oxygenation state, and have sedimentary records covering timespans from the Holocene to multiple glacial-interglacial cycles. Study lakes include El’gygytgyn (arctic Russia), Malawi (tropical southeast Africa), Issyk Kul (Kyrgyzstan), Lake 578 (Greenland), and high elevation lakes in the central Andes (South America). We explore the presence/absence of these compounds in contrasting depositional environments and examine their GDGT distributions in relationship to temperature variability, oxic/anoxic conditions, hydroclimate fluctuations, and other geochemical/environmental parameters.more » « less
-
Archaeal membrane lipids are widely used for paleotemperature reconstructions, yet these molecular fossils also bear rich information about ecology and evolution of marine ammonia-oxidizing archaea (AOA). Here we identified thermal and nonthermal behaviors of archaeal glycerol dialkyl glycerol tetraethers (GDGTs) by comparing the GDGT-based temperature index (TEX 86 ) to the ratio of GDGTs with two and three cyclopentane rings (GDGT-2/GDGT-3). Thermal-dependent biosynthesis should increase TEX 86 and decrease GDGT-2/GDGT-3 when the ambient temperature increases. This presumed temperature-dependent (PTD) trend is observed in GDGTs derived from cultures of thermophilic and mesophilic AOA. The distribution of GDGTs in suspended particulate matter (SPM) and sediments collected from above the pycnocline—shallow water samples—also follows the PTD trend. These similar GDGT distributions between AOA cultures and shallow water environmental samples reflect shallow ecotypes of marine AOA. While there are currently no cultures of deep AOA clades, GDGTs derived from deep water SPM and marine sediment samples exhibit nonthermal behavior deviating from the PTD trend. The presence of deep AOA increases the GDGT-2/GDGT-3 ratio and distorts the temperature-controlled correlation between GDGT-2/GDGT-3 and TEX 86 . We then used Gaussian mixture models to statistically characterize these diagnostic patterns of modern AOA ecology from paleo-GDGT records to infer the evolution of marine AOA from the Mid-Mesozoic to the present. Long-term GDGT-2/GDGT-3 trends suggest a suppression of today’s deep water marine AOA during the Mesozoic–early Cenozoic greenhouse climates. Our analysis provides invaluable insights into the evolutionary timeline and the expansion of AOA niches associated with major oceanographic and climate changes.more » « less
-
Archaea produce unique membrane-spanning lipids (MSLs), termed glycerol dialkyl glycerol tetraethers (GDGTs), which aid in adaptive responses to various environmental challenges. GDGTs can be modified through cyclization, cross-linking, methylation, hydroxylation, and desaturation, resulting in structurally distinct GDGT lipids. Here, we report the identification of radical SAM proteins responsible for two of these modifications—a glycerol monoalkyl glycerol tetraether (GMGT) synthase (Gms), responsible for covalently cross-linking the two hydrocarbon tails of a GDGT to produce GMGTs, and a GMGT methylase (Gmm), capable of methylating the core hydrocarbon tail. Heterologous expression of Gms proteins from various archaea inThermococcus kodakarensisresults in the production of GMGTs in two isomeric forms. Further, coexpression of Gms and Gmm produces mono- and dimethylated GMGTs and minor amounts of trimethylated GMGTs with only trace GDGT methylation. Phylogenetic analyses reveal the presence of Gms homologs in diverse archaeal genomes spanning all four archaeal superphyla and in multiple bacterial phyla with the genetic potential to synthesize fatty acid–based MSLs, demonstrating that GMGT production may be more widespread than previously appreciated. We demonstrate GMGT production in three Gms-encoding archaea, identifying an increase in GMGTs in response to elevated temperature in twoArchaeoglobusspecies and the production of GMGTs with up to six rings inVulcanisaeta distributa.The occurrence of such highly cyclized GMGTs has been limited to environmental samples and their detection in culture demonstrates the utility of combining genetic, bioinformatic, and lipid analyses to identify producers of distinct archaeal membrane lipids.more » « less
-
Numerous temperature and environmental proxies are based on glycerol dialkylglycerol tetraethers (GDGTs), which are membrane lipids commonly found in thewater columns and sediments of lakes. The TEX86 temperature proxy is based onisoprenoid GDGTs, which are produced by members of the archaea, and is used toreconstruct lake surface temperature. Branched GDGTs are lipids produced bybacteria and form the basis of the MBT′5ME temperature proxy. Although manyoutstanding questions still exist regarding proxies based on isoprenoid and branchedGDGTs, both compound classes have been relatively well-studied in lakes. Morerecently, other types of GDGTs and related compounds are increasingly beingreported from lacustrine sediments including hydroxylated GDGTs (OH-GDGTs) andglycerol monoalkyl glycerol tetraethers (GMGTs). In the process of generating lacustrine TEX86 or MBT′5ME temperature records, we noted that OH-GDGTs orGMGTs (or both) are frequently present. The RI-OH, based on OH-GDGTs, recentlyhas been proposed as a temperature proxy in lakes while GMGTs are associatedwith oxygen-deficient environments. Here we examine distributions of OH-GDGTs and GMGTs in a variety of lakes that also have existing TEX86 or MBT′5ME temperature reconstructions. These lakes range from small to large, shallow to deep,tropical to arctic, differ in oxygenation state, and have sedimentary records coveringtimespans from the Holocene to multiple glacial-interglacial cycles. Study lakesinclude El’gygytgyn (arctic Russia), Malawi (tropical southeast Africa), Issyk Kul(Kyrgyzstan), Lake 578 (Greenland), and high elevation lakes in the central Andes (South America). We explore the presence/absence of these compounds incontrasting depositional environments and examine their GDGT distributions inrelationship to temperature variability, oxic/anoxic conditions, hydroclimatefluctuations, and other geochemical/environmental parameters.more » « less
An official website of the United States government

