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Resolving a Piece of the Archaeal Lipid Puzzle COMMENTARY Ann Pearsona,1

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Resolving a Piece of the Archaeal Lipid Puzzle COMMENTARY Ann Pearsona,1 COMMENTARY Resolving a piece of the archaeal lipid puzzle COMMENTARY Ann Pearsona,1 Lipid membranes are common to all cells, despite archaea, in which it is observed that a higher fractional occurring in many different forms across Earth’s great abundance of cyclopentane rings is associated with biotic diversity. Among the most distinctive mem- higher growth temperature (1, 11). Refined calibra- branes are those formed by the archaea, whose lipids tions of the TEX86 index and its response to upper are characterized by sn-2,3-glycerol stereochemistry ocean temperatures have made it a key tool for the (in contrast to sn-1,2-glycerol in bacteria and eukarya), paleoclimate community (12). isoprenoid rather than acetyl hydrophobic chains, and However, archaeal groups in addition to Thaumarch- frequent occurrence as membrane-spanning macrocycle aeota also make cyclopentane-containing GDGTs, includ- structures (1). The membrane-spanning lipids consist ing the Crenarchaeota and many divisions of Euryarchaeota of mixed assemblages of structural isomers contain- (Fig. 1A). In particular, the surface-dwelling Marine ingupto8internalcyclopentanerings(GDGT-0 Group II (MG-II) Euryarchaeota have been suggested through GDGT-8 [glycerol dibiphytanyl glycerol tet- to be GDGT sources (13). This would affect TEX86 raethers with zero to 8 rings]) (Fig. 1). Many aspects of signals if their ring distributions have different physio- the biosynthesis of these unusual structures remain un- logical controls compared to Thaumarchaeota. Such known, but, in PNAS, Zeng et al. (2) take an important differences in lipid response might be expected, be- step forward by revealing genes encoding for 2 enzymes cause, to date, the known ammonia-oxidizing Thau- involved in synthesis of the cyclopentane moieties. Pin- marchaeota are obligate autotrophs residing near pointing these genes is critical not only for understand- the base of the photic zone (9, 14), while the uncul- ing archaeal biosynthetic pathways but also for resolving tured MG-II is suggested to be heterotrophic, occupy- questions about the primary sources of the GDGTs that ing a different niche space at shallower depths (15). are widely detected in the environment. Lack of knowledge about GDGT synthesis has Some history is as follows: In 1992, observations inhibited resolution of this problem and contributes from independent disciplines yielded the remarkable to ambiguity about the taxonomic sources of these conclusion that archaea—often considered “extremo- lipids in marine systems. philes”—must be widespread in the world’s oceans. By identifying 2 unique S-adenosylmethionine A suite of C40 isoprenoid hydrocarbons of archaeal (SAM) proteins required for the formation of cyclo- origin was found in sediments apparently not associ- pentane rings—which they call GDGT ring synthases ated with hydrothermal or methanogenic activity (3), GrsA and GrsB—Zeng et al. (2) open a window into and gene sequences of archaea were discovered resolving the taxonomic question, while also provid- in some of the earliest universal amplicon libraries ing an opportunity to understand more about both the (4, 5). This confluence launched a new era of research physiological functions and biosynthetic mechanisms that identified the central role of ammonia-oxidizing of such rings. Notably, they report that open ocean Thaumarchaeota in the marine nitrogen cycle. Carbon metagenomes and MG-II metagenome-assembled isotopic analyses (6), detection of archaeal ribosomal genomes (MAGs) yield a low diversity of Grs se- RNA (7) and ammonia monooxygenase (amoA) genes quences, all of which are affiliated with Thaumarch- (8), and isolation of the first pure culture (9) collectively aeota (i.e., no instances in MG-II MAGs). If this result established their physiology and global importance, holds, it is good news for the TEX86 proxy, which while the high preservation potential of GDGTs in ma- assumes marine sedimentary GDGTs mainly derive rine sediments led to development of a new lipid- from planktonic Thaumarchaeota (11, 12). However, al- based paleothermometer called TEX86 (10). TEX86 is though DNA sequence identification provides taxo- a proportionality index of GDGTs formulated by anal- nomic assignment, it raises questions about temporal ogy to the lipid composition of cultured thermophilic or spatial adequacy of sampling, and potential taxonomic aDepartment of Earth and Planetary Sciences, Harvard University, Cambridge, MA 02138 Author contributions: A.P. wrote the paper. The author declares no competing interest. Published under the PNAS license. See companion article on page 22505. 1Email: [email protected]. First published October 18, 2019. www.pnas.org/cgi/doi/10.1073/pnas.1916583116 PNAS | November 5, 2019 | vol. 116 | no. 45 | 22423–22425 Downloaded by guest on September 30, 2021 A GDGTs B no rings cyclopentane ? cyclohexane Euryarchaeota Thaumarchaeota ? ? Thermoplasmatales C Fig. 1. (A) GDGTs containing cyclopentane rings are widely distributed among the archaea. (B) GDGTs are membrane-spanning tetraether lipids with 2 C40 isoprenoid chains (R, R’), each containing zero to 4 cyclopentane rings (and sometimes a cyclohexane ring, not shown). Tetraethers are formed from the diether precursor, DGGGP, in which the phosphate is replaced by an alternative polar group (X) before tetraether formation. (C) The sequence of biosynthetic steps leading from 2×[DGGGP] → GDGT remains unknown, but a plausible order would be tetraether synthesis using an MSS, a step that requires the Δ14-15 double bond (22); GrsA and GrsB in sequence, as shown by Zeng et al. (2); and final saturation by GGR, which targets double bonds in the order Δ2, Δ6, Δ10 (23). differences with respect to cellular growth rate or activity. Copy outcome (different physicochemical membrane properties) may be numbers do not equal production rates, and, now that the GDGT under evolutionary and environmental selection. The preference be- ring synthases have been identified, more work will be needed to tween these 2 steps may be regulated by many variables affecting demonstrate in situ activity. More information may also be available cellular homeostasis, including not only temperature (1, 11) but also through data mining of existing metagenomes and metatranscrip- other factors that affect transmembrane potential, including environ- tomes from other types of environments. mental pH, Eh, substrate availability, and growth rate (17–19). The The identification by Zeng et al. (2) of GrsA and GrsB in the resulting assemblage of GDGT-0 through GDGT-8 affects membrane genetically tractable thermophile Sulfolobus acidocaldarius also stiffness and diffusive properties, including the rate at which trans- may result in better understanding of the physiological controls membrane potential is dissipated (20). Sulfolobus provides a model on biosynthesis of ring-containing GDGTs. Formation of a variable experimental system to test how GDGT production responds to number of rings reflects the balance between 2 categories of environmental pressures. reactions: saturation by the enzyme geranylgeranyl reductase Finally, many questions remain about the complete biosyn- (GGR) vs. ring formation by GrsA/GrsB (Fig. 1). Double-bond re- thesis of GDGT core structures. Zeng et al. (2) demonstrate that ductions by GGR require the organisms to dedicate net reducing GrsA acts prior to GrsB but decline to speculate on whether cy- power to the process, whereas internal cyclization does not clization occurs before or after saturation by GGR. However, given change the oxidation state. Because the extremophile nature of the presence of geranylgeranyl chains in the intermediate struc- archaea can be described as adaptation to chronic energy stress ture digeranylgeranylglycerol phosphate (DGGGP) (Fig. 1B), I (16), this balance is particularly relevant—both the biosynthetic pres- suggest a reasonable hypothesis is that GrsA/GrsB would act sure for ring synthesis (less demand for electron donor) and the beforeGGRtoexploittheexisting double bonds: A typical 22424 | www.pnas.org/cgi/doi/10.1073/pnas.1916583116 Pearson Downloaded by guest on September 30, 2021 mechanism of SAM enzymes is free radical formation at an sp3 the type of enzyme and the preferred substrates for GrsA and carbon, followed by internal attack on an sp2 carbon (21). If true, GrsB, Zeng et al. (2) provide evidence for a testable, albeit still this order provides a framework in which to unite additional, in- quite speculative, GDGT biosynthesis scheme having the order dependent observations. Zeng et al. (2) note that the substrate- MSS, GrsA, GrsB, GGR (Fig. 1). specific behavior of GrsA and GrsB appears to require prior for- Of course, I have conspicuously neglected any mention of mation of a membrane-spanning tetraether. Here, I call this step the unusual cyclohexane ring (24) that occurs in the GDGTs of “MSS” to indicate a hypothetical membrane-spanning synthase. Thaumarchaeota—it is a mystery that reminds us how many more The terminal (Δ14-15) double bond apparently is required for the secrets the archaea have yet to reveal and a reminder that there is MSS reaction, and the intermediate may again be a carbon radical much more work still ahead. (22) (Fig. 1C). Together, these observations imply that diether condensation and ring formation begin at the hydrophobic ends Acknowledgments of DGGGP and proceed in the direction of the glycerol moiety. In Felix Elling and William Leavitt are thanked for thoughtful discussions. A.P. contrast, saturation
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