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GDGT Cyclization Proteins Identify the Dominant Archaeal Sources of Tetraether Lipids in the Ocean

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GDGT Cyclization Proteins Identify the Dominant Archaeal Sources of Tetraether Lipids in the Ocean GDGT cyclization proteins identify the dominant archaeal sources of tetraether lipids in the ocean Zhirui Zenga,1, Xiao-Lei Liub,1, Kristen R. Farleyc, Jeremy H. Weia, William W. Metcalfc,d, Roger E. Summonse, and Paula V. Welandera,2 aDepartment of Earth System Science, Stanford University, Stanford, CA 94305; bDepartment of Geosciences, University of Oklahoma, Norman, OK 73019; cDepartment of Microbiology, University of Illinois Urbana–Champaign, Urbana, IL 61801; dInstitute for Genomic Biology, University of Illinois Urbana– Champaign, Urbana, IL 61801; and eDepartment of Earth, Atmospheric and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139 Edited by Katherine H. Freeman, Pennsylvania State University, University Park, PA, and approved September 18, 2019 (received for review May 29, 2019) Glycerol dibiphytanyl glycerol tetraethers (GDGTs) are distinctive be correlated with overlying sea surface temperatures (7, 8). archaeal membrane-spanning lipids with up to eight cyclopentane Given the ubiquity of GDGTs in marine sediments and their rings and/or one cyclohexane ring. The number of rings added to resistance to diagenetic alterations, these proxies are potentially the GDGT core structure can vary as a function of environmental powerful paleoclimatology tools that allow for reconstruction of conditions, such as changes in growth temperature. This physiolog- past temperature changes, providing insight into Earth system ical response enables cyclic GDGTs preserved in sediments to be dynamics deep in geologic time (9). employed as proxies for reconstructing past global and regional However, a robust assessment of GDGT-based proxies is temperatures and to provide fundamental insights into ancient hampered by a variety of unresolved factors, including the influ- climate variability. Yet, confidence in GDGT-based paleotempera- ence of environmental factors other than temperature on in- ture proxies is hindered by uncertainty concerning the archaeal creased tetraether cyclization (9–13) and ambiguity in the archaeal communities contributing to GDGT pools in modern environments taxa contributing to GDGT pools in marine ecosystems (14, 15). and ambiguity in the environmental and physiological factors that Specifically, applications of TEX86 assume that mesophilic Marine affect GDGT cyclization in extant archaea. To properly constrain Group I (MG-I) Thaumarchaeota are the dominant source of these uncertainties, a comprehensive understanding of GDGT cyclic GDGTs in the pelagic zone (9). However, studies have EARTH, ATMOSPHERIC, biosynthesis is required. Here, we identify 2 GDGT ring synthases, shown that MG-II Euryarchaeota are abundant in near-surface AND PLANETARY SCIENCES GrsA and GrsB, essential for GDGT ring formation in Sulfolobus waters (14, 15), and some have suggested that marine acidocaldarius . Both proteins are radical S-adenosylmethionine Euryarchaeota are significant contributors to ocean cyclic GDGT proteins, indicating that GDGT cyclization occurs through a free pools at shallower depths (13, 16). A mixed archaeal population radical mechanism. In addition, we demonstrate that GrsA intro- producing cyclized GDGTs in the marine water column could duces rings specifically at the C-7 position of the core GDGT lipid, significantly affect TEX -based temperature estimates, especially while GrsB cyclizes at the C-3 position, suggesting that cycliza- 86 if GDGT distribution patterns reflect changes in archaeal com- MICROBIOLOGY tion patterns are differentially controlled by 2 separate enzymes munity structure rather than changes in temperature. Therefore, and potentially influenced by distinct environmental factors. Fi- constraining the archaeal sources of GDGTs in the open oceans is nally, phylogenetic analyses of the Grs proteins reveal that marine critical but has been difficult, as there are currently no MG-II 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 Significance applications. Archaea synthesize distinctive membrane-spanning lipids (GDGTs) GDGT | radical SAM | Sulfolobus | paleotemperature proxies that are readily preserved in ancient sediments and utilized as paleotemperature proxies to reconstruct sea surface temperatures ’ rchaea are distinct from bacteria and eukaryotes in many deep in Earth s past. However, properly interpreting GDGT-based Arespects, including, most prominently, the chemistry of their biomarker proxies requires an accurate assessment of the archaea membrane lipids. While bacterial and eukaryotic lipids are com- that contribute to GDGT pools in modern environments and of the proteins necessary for synthesizing GDGTs. In this study, we posed of fatty acid bilayers, archaeal membranes comprise identify 2 radical SAM proteins in Sulfolobus acidocaldarius that isoprenoidal bilayers that may be fused to form unique 86 carbon are required to produce these molecules. Bioinformatics analyses membrane-spanning structures known as glycerol dibiphytanyl of these GDGT ring synthesis proteins reveal that Thaumarchaeota glycerol tetraethers (GDGTs) (1). GDGTs are further modified are the dominant source of cyclized GDGTs in the open ocean, through the insertion of up to 8 cyclopentyl moieties at the C-7 and allowing us to constrain one factor of uncertainty in the application C-3 positions of each of the biphytanyl chains (Fig. 1), cross-linking of GDGT-based paleotemperature proxies. of the 2 biphytanyl chains, and inclusion of a cyclohexane ring at C-11 believed to be specific to taxa within the Thaumarchaeota Author contributions: Z.Z., X.-L.L., K.R.F., R.E.S., and P.V.W. designed research; Z.Z., X.-L.L., phylum (2). It is proposed that archaea modify their GDGTs as a and K.R.F. performed research; X.-L.L., K.R.F., J.H.W., and W.W.M. contributed new re- way to adjust membrane rigidity in response to changes in envi- agents/analytic tools; Z.Z., X.-L.L., J.H.W., W.W.M., R.E.S., and P.V.W. analyzed data; and ronmental temperature, pH, and/or salinity and that these modifi- Z.Z., X.-L.L., K.R.F., J.H.W., W.W.M., R.E.S., and P.V.W. wrote the paper. cations provide a protective effect under fluctuating environmental The authors declare no competing interest. conditions (3). Several studies have specifically documented a re- This article is a PNAS Direct Submission. lationship between growth temperature and GDGT cyclization (4– Published under the PNAS license. 6), and this association is the basis for a variety of GDGT-based 1Z.Z. and X.-L.L. contributed equally to this work. 2 paleoenvironmental proxies, such as the TEX86 (Tetraether Index To whom correspondence may be addressed. Email: [email protected]. of 86 carbons) sea surface temperature proxy. This index, and other This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. related parameters such as the Ring Index, allow the occurrence of 1073/pnas.1909306116/-/DCSupplemental. cyclic GDGTs and their isomers in marine surface sediments to www.pnas.org/cgi/doi/10.1073/pnas.1909306116 PNAS Latest Articles | 1of7 Downloaded by guest on September 30, 2021 A B detected in marine systems that would be applicable to TEX86 HO S. acidocaldarius proxies, it does produce GDGTs with up to 8 cyclopentyl rings O O WT 4 4 (Fig. 1A), and it is one of a few genetically tractable archaeal O O 3 OH 5 model systems (21). Our studies revealed that deletion of grsA 2 GDGT-0 2 1 0 6 and grsB in S. acidocaldarius results in complete loss of GDGT 0 cyclization. In addition, we demonstrate that each tetraether Cyclization? 4 ∆grsA (saci_1585) cyclization protein inserts cyclopentane rings at specific locations 0 HO on the GDGT core lipid and provide insight into the overall O 2 O biochemical mechanism of GDGT synthesis. Finally, bioinformatics O O 1 OH ) 6 0 analyses show that Grs homologs in marine systems are domi- GDGT-1 4 ∆grsB (saci_0240) nated by MG-I Thaumarchaeota species and validate the underlying HO 4 O TEX86 assumption that Thaumarchaeota, and not Euryarchaeota, O 3 O 2 are the dominant contributors to cyclic GDGT pools in the O 2 OH 0 1 GDGT-2 0 surface ocean. HO O 4 ∆grsA∆grsB Results O O Relative intensity (×10 0 Identification of 2 GDGT Cyclization Proteins in S. acidocaldarius. To O 2 GDGT-3 OH identify potential GDGT cyclization candidate proteins, we first HO 0 O hypothesized that the introduction of cyclopentane rings into the O O ∆grsA∆grsB +p1561-grsB-grsA GDGT core structure would require a free radical mechanism, 4 O 6 most likely carried out by a radical S-adenosylmethionine (SAM) GDGT-4 OH 0 HO 1 5 8 protein. The radical SAM protein family encompasses a wide class O 2 2 3 4 7 500× O of enzymes that generate a deoxyadenosyl radical to initiate a di- 0 O verse set of otherwise difficult chemical reactions (22). We have O 19 21 23 25 27 29 31 33 GDGT-5 OH HO previously shown that radical SAM proteins are critical for fine- O Time (min) O C tuning of various lipid structures, including formation of the non- M. acetivorans O hydrolyzable calditol head group in the membrane lipids of S. O 2 OH WT + pJK031A acidocaldarius and modifications to hopanoid lipids in bacteria (23– GDGT-6 ) HO 5 O 0 26). Both modifications involve formation of new C−C bonds at 10 1 O otherwise unreactive carbon atoms. The S. acidocaldarius genome O 0 C3 contains 18 annotated radical SAMs (Pfam: 04055), and we O HO C7 GDGT-7 O OH WT + pJK031A-grsA-grsB searched for homologs of each of these proteins that were present C7’ 2 0 O C3’ in the genomes of archaea that produce cyclic GDGTs and absent 1 C3’ O 1 from those that produce only GDGT-0 or which do not produce C7’ Relative intensity (× 2 GDGT-8 O 0 any GDGTs at all. This analysis resulted in 3 GDGT ring synthase C7 OH C3 19 21 23 25 27 29 31 33 (grs) candidate genes: saci_0240, saci_1585,andsaci_1785.
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