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, 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.

The absence of intact polar lipid-derived GDGTs in marine waters dominated by Marine Group II: Implications for lipid biosynthesis in Archaea

“…Our results strongly contrast those of Lincoln et al 23 , who stated that MGII archaea are able to synthesize archaeal GDGTs and, therefore, contribute substantially to the total archaeal GDGT pool, potentially affecting the paleotemperature proxy TEX 86 . Our results are in agreement with the recent study of Zeng et al 27 who suggested that MGII archaea might not synthesize GDGTs with cyclopentane and -hexane moieties based on the lack of cyclase coding genes in their genomes. Our study goes a step further as our results not only indicate the MGII archaea do not contribute to the GDGTs involved in the TEX 86 proxy, but also do not seem to synthesize any other known archaeal membrane lipids.…”

“…glycerol-1-phosphate (G1P), in (meta)genomes of MGII and MGIII archaea strongly suggested that these Archaea are not able to synthesize 'classical' archaeal membrane lipids 26 . Furthermore, a recent study 27 suggested that MGII archaea do not synthesize GDGTs with cyclopentane moieties. This is based on their genomes that lack the gene encoding the enzyme responsible for the internal cyclization reaction that results in the formation of cyclopentane and -hexane moieties.…”

Late Paleocene – early Eocene Arctic Ocean Sea Surface Temperatures; reassessing biomarker paleothermometry at Lomonosov Ridge

“…Thaumarchaeota, the source of most GDGTs in marine waters (Zeng et al, 2019;Besseling et al, 2020), are ammonium oxidizers (Könneke et al, 2005;Wuchter et al, 2006a), making them independent of light. Although they occur throughout the water column, maximum abundances are at depths <200 m, generally around NO2 maxima (e.g., Karner et al, 2001;Pitcher et al, 2011a).…”

Predominance of hexamethylated 6-methyl branched glycerol dialkyl glycerol tetraethers in the Mariana Trench: source and environmental implication

“…However, one weakness of these proxies is the source uncertainty. Although brGDGTs were assumed to be specific for soil and peat bacteria (Hopmans et al, 2004;Weijers et al, 2007a, b), different compositions of brGDGTs among rivers (Zhang et al, 2012;Zell et al, 2013Zell et al, , 2014a, lakes (Sinninghe Damsté et al, 2009;Tierney and Russell, 2009;Loomis et al, 2011;Buckles et al, 2014), marine waters (Liu et al, 2014;Xie et al, 2014;Zell et al, 2014b), and sediments (Peterse et al, 2009;Zhu et al, 2011;Xiao et al, 2016) suggest multiple sources. Besides temperature and pH, oxygen (Qin et al, 2015) and moisture (Dang et al, 2016a) can also influence the composition of GDGTs.…”