Crenarchaeol

Last updated
Crenarchaeol
Crenarchaeol.svg
Names
IUPAC name
[(9S,12S,16S,24S,28R,31R,35S,43S,46S,50S,58S,62R,65R)-12-(Hydroxymethyl)-9,16,24,28,31,35,43,50,58,62,65-undecamethyl-11,14,45,48-tetraoxahexacyclo[63.3.1.12,5.120,23.136,39.154,57]triheptacontan-46-yl]methanol
Identifiers
3D model (JSmol)
ChemSpider
PubChem CID
  • C[C@@H]1CCC[C@@H](C2CCC(C2)CCC[C@@H](COC[C@@H](OC[C@H](CCCC3CCC(C3)C4CCC[C@@](C4)(CC[C@@H](CCC[C@@H](C5CCC(C5)CCC[C@@H](COC[C@@H](OC[C@H](CCCC6CCC(C6)[C@H](CCC[C@H](CC1)C)C)C)CO)C)C)C)C)C)CO)C)C
Properties
C82H154O6
Molar mass 1236.128 g·mol−1
Except where otherwise noted, data are given for materials in their standard state (at 25 °C [77 °F], 100 kPa).

Crenarchaeol is a glycerol biphytanes glycerol tetraether (GDGT) biological membrane lipid. Together with archaeol, crenarcheol comprises a major component of archaeal membranes. [1] Archaeal membranes are distinct from those of bacteria and eukaryotes because they contain isoprenoid GDGTs instead of diacyl lipids, which are found in the other domains (bacteria, procarya). It has been proposed that GDGT membrane lipids are an adaptation to the high temperatures present in the environments that are home to extremophile archaea [2]

Discovery and distribution

Archaeal GDGTs were first detected in pelagic waters. [3] Unknown GDGTs were also found in marine sediments [4] and isolated from Cenarchaeum symbiosum , [5] a marine ammonia-oxidizing archaeon that lives in symbiosis with sponges.

Following the discovery of GDGTs outside of hydrothermal environments, crenarchaeol was first identified as the major GDGT component in surface sediments and extracts from C. symbiosum by two-dimensional nuclear magnetic resonance (2D-NMR) spectroscopy. [6] It was named for the phylum Crenarchaeota (now Thermoproteota), to which the ammonia-oxidizing pelagic archaea that produce crenarchaeol were thought to belong before it was proposed that the Marine Group I Crenarchaeota be considered a distinct phylum, Thaumarchaeota (now Nitrososphaerota). [7]

Crenarchaeol was originally thought to be produced only in pelagic ocean environments, but researchers have since discovered that it is also produced by archaea living in high temperature environments including hot springs like this one. Opal Pool YNP2 filtered noise.jpg
Crenarchaeol was originally thought to be produced only in pelagic ocean environments, but researchers have since discovered that it is also produced by archaea living in high temperature environments including hot springs like this one.

Occurrence in ammonia oxidizing organisms

Crenarchaeol has been proposed as a biomarker for pelagic ammonia-oxidizing archaea (AOA). [2] Crenarchaeol is produced by AOA belonging to the phylum Nitrososphaerota (formerly classified as the Marine Group 1 Crenarchaeota). It has been confirmed to be produced by pure cultures of the pelagic mesothermic C. symbiosum [6] and Nitrosopumilus maritimus , [8] as well as the moderately thermophilic Nitrososphaera gargensis [2] and the hyperthermophilic Candidatus Nitrosocaldus yellowstonii. [9] The discovery that crenarchaeol in Ca.N. yellowstonii and N. gargensis disproved the previous consensus that crenarchaeol was specific to mesothermic Nitrososphaerota and suggests that it is found more broadly within the phylum.


In biology

Chemistry and function

Structurally, the molecule consists of two long hydrocarbon chains that extend through the cell membrane and are bound on each to glycerol through ether linkage.

Like other GDGTs, crenarchaeol is a membrane lipid with distinct hydrophobic and hydrophilic regions. The long, nonpolar hydrocarbon chains are hydrophobic while the ether-linked glycerol head groups are polar and hydrophilic. In most organisms, the cell membrane consists of a lipid bilayer in which phospholipids arrange with their hydrophobic, nonpolar hydrocarbon tails facing inwards towards one another and their hydrophilic, polar head groups facing outwards to associate with the polar environments of the cytoplasm or cell exterior. This organization is promoted by the hydrophobic effect, which makes it energetically favorable for hydrophobic molecules to isolate themselves away from aqueous environments. Because GDGTs have two hydrophilic head groups, they form a lipid monolayer in the cell membrane instead of a bilayer, making GDGT-producing archaea exceptional among all clades of life. [10] Originally, it was believed that GDGT membrane lipids were an adaption to life at high temperatures and acidities. Because the two sides of a monolayer lipid are connected by covalent bonds rather than the weaker intermolecular forces that promote the cohesion of bilayers, they are more stable than typical bilayers. [10] This hypothesis is supported by the observation that some extremophile bacteria synthesize their own membrane-spanning, ether-bound GDGT analogues. [11] The cyclic moieties of GDGTs may also be an adaption to hyperthermal conditions, [6] and the number of rings in a GDGT's long hydrocarbon chains is temperature-dependent. [12] Crenarchaeol has two cyclopentyl moieties on one of its hydrocarbon chains and one cyclohexyl and two cyclopentyl moieties on the other.

However, the discovery that crenarchaeol and other GDGTs are produced by organisms living in mesothermal environments has thrown the hyperthermal-adaptation hypothesis into question. [10] It has been proposed that the distinctive cyclohexyl group of crenarchaeol is an adaption to pelagic life, as it produces a "kink" in one of crenarchaeol's hydrocarbon chains that prevents the membrane lipids from packing tightly, as would be favorable under high temperatures but unfavorable under temperate ones. [6]

Preservation and degradation in sediments

Crenarchaeol are stable for hundreds of millions of years in the environment. It is part of the TEX86 paleothermometer, a temperature proxy for sea surface temperatures that has been used to reconstruct paleoclimate through to the middle Jurassic (~160 Ma). [13]

Crenarchaeol and other GDGTs can be preserved in the environment for hundreds of millions of years [13] under the right conditions. Most GDGTs degrade at between 240 and 300 °C and so are not found in rocks that have undergone heating to temperatures higher than 300 °C. [14] GDGTs undergo degradation when exposed to oxygen but the relative concentrations of sediment GDGTs tends to remain the same even during degradation, meaning that degradation does not interfere with proxies like TEX86 [15] that are based on the ratios of different GDGTs.

TEX86 paleothermometer

The number of rings in GDGT hydrocarbon chains is temperature dependent and provides the basis for the TEX86 paleothermometer, a proxy for measuring ancient sea surface temperature (SST) [16] that relies on measurements of the abundances of crenarchaeol and its isomers. Crenarchaeol has a regioisomer which, based on radiocarbon analysis, may have a different origin than other isoprenoid GDGTs. Possible sources for the regioisomer include benthic archaea and diagenesis of crenarchaeol, as the regioisomer is found in low abundance in surface waters and in cultures of pelagic thaumarchaea. Despite this, if it is excluded from TEX86 calculations, the paleothermometer's correlation with sea surface temperature becomes less apparent, indicating it is a necessary component of TEX86. [17]

Isolation and measurement

GDGTs such as crenarchaeol can be analyzed using high-performance liquid chromatography/ atmospheric pressure chemical ionization-mass spectrometry (HPLC/APCI-MS) following extraction and acid hydrolysis. [18] Acid hydrolysis cleaves the polar head groups from the molecule, leaving the nonpolar chains behind. This is required for chromatography, which is not well suited to analysis of polar molecules. A variety of extraction techniques have been demonstrated to be effective for GDGTs. One common method is extraction by ultrasonication with methanol followed by washes of the nonpolar solvent dichloromethane (DCM). [18] GDGTs have characteristic [M + H]+ - 18 and [M + H]+ - 74 ions [18] that, for crenarchaeol, have masses of 1218 and 1162 Da, respectively. Relative abundances of GDGTs can be determined by integrating the peak areas of their characteristic ions.

Related Research Articles

<span class="mw-page-title-main">Nitrification</span> Biological oxidation of ammonia/ammonium to nitrate

Nitrification is the biological oxidation of ammonia to nitrate via the intermediary nitrite. Nitrification is an important step in the nitrogen cycle in soil. The process of complete nitrification may occur through separate organisms or entirely within one organism, as in comammox bacteria. The transformation of ammonia to nitrite is usually the rate limiting step of nitrification. Nitrification is an aerobic process performed by small groups of autotrophic bacteria and archaea.

A hyperthermophile is an organism that thrives in extremely hot environments—from 60 °C (140 °F) upwards. An optimal temperature for the existence of hyperthermophiles is often above 80 °C (176 °F). Hyperthermophiles are often within the domain Archaea, although some bacteria are also able to tolerate extreme temperatures. Some of these bacteria are able to live at temperatures greater than 100 °C, deep in the ocean where high pressures increase the boiling point of water. Many hyperthermophiles are also able to withstand other environmental extremes, such as high acidity or high radiation levels. Hyperthermophiles are a subset of extremophiles. Their existence may support the possibility of extraterrestrial life, showing that life can thrive in environmental extremes.

<span class="mw-page-title-main">Ether lipid</span>

In biochemistry, an ether lipid refers to any lipid in which the lipid "tail" group is attached to the glycerol backbone via an ether bond at any position. In contrast, conventional glycerophospholipids and triglycerides are triesters. Structural types include:

<i>Sulfolobus</i> Genus of archaea

Sulfolobus is a genus of microorganism in the family Sulfolobaceae. It belongs to the archaea domain.

TEX<sub>86</sub>

TEX86 is an organic paleothermometer based upon the membrane lipids of mesophilic marine Nitrososphaerota (formerly "Thaumarchaeota", "Marine Group 1 Crenarchaeota").

<span class="mw-page-title-main">Thermoacidophile</span> Microorganisms which live in water with high temperature and high acidity

A thermoacidophile is an extremophilic microorganism that is both thermophilic and acidophilic; i.e., it can grow under conditions of high temperature and low pH. The large majority of thermoacidophiles are archaea or bacteria, though occasional eukaryotic examples have been reported. Thermoacidophiles can be found in hot springs and solfataric environments, within deep sea vents, or in other environments of geothermal activity. They also occur in polluted environments, such as in acid mine drainage.

Phytane is the isoprenoid alkane formed when phytol, a chemical substituent of chlorophyll, loses its hydroxyl group. When phytol loses one carbon atom, it yields pristane. Other sources of phytane and pristane have also been proposed than phytol.

<span class="mw-page-title-main">Membrane lipid</span> Lipid molecules on cell membrane

Membrane lipids are a group of compounds which form the lipid bilayer of the cell membrane. The three major classes of membrane lipids are phospholipids, glycolipids, and cholesterol. Lipids are amphiphilic: they have one end that is soluble in water ('polar') and an ending that is soluble in fat ('nonpolar'). By forming a double layer with the polar ends pointing outwards and the nonpolar ends pointing inwards membrane lipids can form a 'lipid bilayer' which keeps the watery interior of the cell separate from the watery exterior. The arrangements of lipids and various proteins, acting as receptors and channel pores in the membrane, control the entry and exit of other molecules and ions as part of the cell's metabolism. In order to perform physiological functions, membrane proteins are facilitated to rotate and diffuse laterally in two dimensional expanse of lipid bilayer by the presence of a shell of lipids closely attached to protein surface, called annular lipid shell.

<i>Nitrosopumilus</i> Genus of archaea

Nitrosopumilus maritimus is an extremely common archaeon living in seawater. It is the first member of the Group 1a Nitrososphaerota to be isolated in pure culture. Gene sequences suggest that the Group 1a Nitrososphaerota are ubiquitous with the oligotrophic surface ocean and can be found in most non-coastal marine waters around the planet. It is one of the smallest living organisms at 0.2 micrometers in diameter. Cells in the species N. maritimus are shaped like peanuts and can be found both as individuals and in loose aggregates. They oxidize ammonia to nitrite and members of N. maritimus can oxidize ammonia at levels as low as 10 nanomolar, near the limit to sustain its life. Archaea in the species N. maritimus live in oxygen-depleted habitats. Oxygen needed for ammonia oxidation might be produced by novel pathway which generates oxygen and dinitrogen. N. maritimus is thus among organisms which are able to produce oxygen in dark.

<span class="mw-page-title-main">Caldarchaeol</span> Chemical compound

Caldarchaeol is a membrane-spanning lipid of the glycerol dialkyl glycerol tetraether class. It is found in hyperthermophilic archaea. Membranes made up of caldarchaeol are more stable since the hydrophobic chains are linked together, allowing the microorganisms to withstand high temperatures. It is also known as dibiphytanyldiglycerol tetraether. Two glycerol units are linked together by two strains which consist of two phytanes linked together to form a linear chain of 32 carbon atoms.

Fuselloviridae is a family of viruses. Sulfolobus species, specifically shibatae, solfataricus, and islandicus, serve as natural hosts. There are two genera and nine species in the family. The Fuselloviridae are ubiquitous in high-temperature (≥70 °C), acidic hot springs around the world.

<span class="mw-page-title-main">Archaea</span> Domain of single-celled organisms

Archaea is a domain of single-celled organisms. These microorganisms lack cell nuclei and are therefore prokaryotes. Archaea were initially classified as bacteria, receiving the name archaebacteria, but this term has fallen out of use.

Archaeol is composed of two phytanyl chains linked to the sn-2 and sn-3 positions of glycerol. As its phosphate ester, it is a common component of the membranes of archaea.

<span class="mw-page-title-main">Nitrososphaerota</span> Phylum of archaea

The Nitrososphaerota are a phylum of the Archaea proposed in 2008 after the genome of Cenarchaeum symbiosum was sequenced and found to differ significantly from other members of the hyperthermophilic phylum Thermoproteota. Three described species in addition to C. symbiosum are Nitrosopumilus maritimus, Nitrososphaera viennensis, and Nitrososphaera gargensis. The phylum was proposed in 2008 based on phylogenetic data, such as the sequences of these organisms' ribosomal RNA genes, and the presence of a form of type I topoisomerase that was previously thought to be unique to the eukaryotes. This assignment was confirmed by further analysis published in 2010 that examined the genomes of the ammonia-oxidizing archaea Nitrosopumilus maritimus and Nitrososphaera gargensis, concluding that these species form a distinct lineage that includes Cenarchaeum symbiosum. The lipid crenarchaeol has been found only in Nitrososphaerota, making it a potential biomarker for the phylum. Most organisms of this lineage thus far identified are chemolithoautotrophic ammonia-oxidizers and may play important roles in biogeochemical cycles, such as the nitrogen cycle and the carbon cycle. Metagenomic sequencing indicates that they constitute ~1% of the sea surface metagenome across many sites.

Nitrososphaera is a mesophilic genus of ammonia-oxidizing Crenarchaeota. The first Nitrososphaera organism was discovered in garden soils at the University of Vienna leading to the categorization of a new genus, family, order and class of Archaea. This genus is contains three distinct species: N. viennensis, Ca. N. gargensis, and Ca N. evergladensis. Nitrososphaera are chemolithoautotrophs and have important biogeochemical roles as nitrifying organisms.

Nitrososphaera gargensis is a non-pathogenic, small coccus measuring 0.9 ± 0.3 μm in diameter. N. gargensis is observed in small abnormal cocci groupings and uses its archaella to move via chemotaxis. Being an Archaeon, Nitrososphaera gargensis has a cell membrane composed of crenarchaeol, its isomer, and a distinct glycerol dialkyl glycerol tetraether (GDGT), which is significant in identifying ammonia-oxidizing archaea (AOA). The organism plays a role in influencing ocean communities and food production.

Jessica E. Tierney (born 1982) is an American paleoclimatologist who has worked with geochemical proxies such as marine sediments, mud, and TEX86, to study past climate in East Africa. Her papers have been cited more than 2,500 times; her most cited work is Northern Hemisphere Controls on Tropical Southeast African Climate During the Past 60,000 Years. Tierney is currently an associate professor of geosciences and the Thomas R. Brown Distinguished Chair in Integrative Science at the University of Arizona and faculty affiliate in the University of Arizona School of Geography, Development and Environment Tierney is the first climatologist to win NSF's Alan T Waterman Award (2022) since its inception in 1975.

Paula Veronica Welander is a microbiologist and professor at Stanford University who is known for her research using lipid biomarkers to investigate how life evolved on Earth.

Glycerol dialkyl glycerol tetraether lipids (GDGTs) are a class of membrane lipids synthesized by archaea and some bacteria, making them useful biomarkers for these organisms in the geological record. Their presence, structure, and relative abundances in natural materials can be useful as proxies for temperature, terrestrial organic matter input, and soil pH for past periods in Earth history. Some structural forms of GDGT form the basis for the TEX86 paleothermometer. Isoprenoid GDGTs, now known to be synthesized by many archaeal classes, were first discovered in extremophilic archaea cultures. Branched GDGTs, likely synthesized by acidobacteriota, were first discovered in a natural Dutch peat sample in 2000.

Biphytane (or bisphytane) is a C40 isoprenoid produced from glycerol dialkyl glycerol tetraether (GDGT) degradation. As a common lipid membrane component, biphytane is widely used as a biomarker for archaea. In particular, given its association with sites of active anaerobic oxidation of methane (AOM), it is considered a biomarker of methanotrophic archaea. It has been found in both marine and terrestrial environments.

References

  1. ↑ Caforio, Antonella; Driessen, Arnold J.M. (2017). "Archaeal phospholipids: Structural properties and biosynthesis" (PDF). Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids. 1862 (11): 1325–1339. doi:10.1016/j.bbalip.2016.12.006. PMID   28007654.
  2. 1 2 3 Pitcher A, Rychlik N, Hopmans EC, Spieck E, Rijpstra WI, Ossebaar J, Schouten S, Wagner M, Damsté JS (April 2010). "Crenarchaeol dominates the membrane lipids of Candidatus Nitrososphaera gargensis, a thermophilic group I.1b Archaeon". The ISME Journal. 4 (4): 542–52. doi: 10.1038/ismej.2009.138 . PMID   20033067.
  3. ↑ Hoefs M, Schouten S, De Leeuw JW, King LL, Wakeham SG, Damste J (August 1997). "Ether lipids of planktonic archaea in the marine water column". Applied and Environmental Microbiology. 63 (8): 3090–5. doi:10.1128/AEM.63.8.3090-3095.1997. PMC   1389224 . PMID   16535669.
  4. ↑ Schouten S, Hopmans EC, Pancost RD, Damste JS (December 2000). "Widespread occurrence of structurally diverse tetraether membrane lipids: evidence for the ubiquitous presence of low-temperature relatives of hyperthermophiles". Proceedings of the National Academy of Sciences of the United States of America. 97 (26): 14421–6. doi:10.1073/pnas.97.26.14421. PMC   18934 . PMID   11121044.
  5. ↑ DeLong EF, King LL, Massana R, Cittone H, Murray A, Schleper C, Wakeham SG (March 1998). "Dibiphytanyl ether lipids in nonthermophilic crenarchaeotes". Applied and Environmental Microbiology. 64 (3): 1133–8. doi:10.1128/AEM.64.3.1133-1138.1998. PMC   106379 . PMID   9501451.
  6. 1 2 3 4 Damsté JS, Schouten S, Hopmans EC, van Duin AC, Geenevasen JA (October 2002). "Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota". Journal of Lipid Research. 43 (10): 1641–51. doi: 10.1194/jlr.M200148-JLR200 . PMID   12364548.
  7. ↑ Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (March 2008). "Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota". Nature Reviews. Microbiology. 6 (3): 245–52. doi:10.1038/nrmicro1852. PMID   18274537. S2CID   8030169.
  8. ↑ Schouten S, Hopmans EC, Baas M, Boumann H, Standfest S, Könneke M, Stahl DA, Sinninghe Damsté JS (April 2008). "Intact membrane lipids of "Candidatus Nitrosopumilus maritimus," a cultivated representative of the cosmopolitan mesophilic group I Crenarchaeota". Applied and Environmental Microbiology. 74 (8): 2433–40. doi:10.1128/AEM.01709-07. PMC   2293165 . PMID   18296531.
  9. ↑ de la Torre JR, Walker CB, Ingalls AE, Könneke M, Stahl DA (March 2008). "Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol". Environmental Microbiology. 10 (3): 810–8. doi: 10.1111/j.1462-2920.2007.01506.x . PMID   18205821.
  10. 1 2 3 Schouten, Stefan; Hopmans, Ellen C.; Sinninghe Damsté, Jaap S. (2013-01-01). "The organic geochemistry of glycerol dialkyl glycerol tetraether lipids: A review". Organic Geochemistry. 54: 19–61. doi:10.1016/j.orggeochem.2012.09.006. ISSN   0146-6380.
  11. ↑ Langworthy TA, Holzer G, Zeikus JG, Tornabene TG (1983-01-01). "Iso- and Anteiso-Branched Glycerol Diethers of the Thermophilic Anaerobe Thermodesulfotobacterium commune". Systematic and Applied Microbiology. 4 (1): 1–17. doi:10.1016/S0723-2020(83)80029-0. PMID   23196295.
  12. ↑ Schouten, Stefan; Hopmans, Ellen C.; Schefuß, Enno; Sinninghe Damsté, Jaap S. (2002). "Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures?". Earth and Planetary Science Letters. 204 (1–2): 265–274. Bibcode:2002E&PSL.204..265S. doi:10.1016/S0012-821X(02)00979-2.
  13. 1 2 Jenkyns, H. C.; Schouten-Huibers, L.; Schouten, S.; Sinninghe Damsté, J. S. (2012-02-02). "Warm Middle Jurassic–Early Cretaceous high-latitude sea-surface temperatures from the Southern Ocean". Climate of the Past. 8 (1): 215–226. Bibcode:2012CliPa...8..215J. doi: 10.5194/cp-8-215-2012 . ISSN   1814-9332.
  14. ↑ Schouten, Stefan; Hopmans, Ellen C.; Schefuß, Enno; Sinninghe Damsté, Jaap S. (2002-11-30). "Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures?". Earth and Planetary Science Letters. 204 (1): 265–274. Bibcode:2002E&PSL.204..265S. doi:10.1016/S0012-821X(02)00979-2. ISSN   0012-821X.
  15. ↑ Mollenhauer, Gesine; Eglinton, Timothy I.; Hopmans, Ellen C.; Sinninghe Damsté, Jaap S. (2008-08-01). "A radiocarbon-based assessment of the preservation characteristics of crenarchaeol and alkenones from continental margin sediments" (PDF). Organic Geochemistry. Advances in Organic Geochemistry 2007. 39 (8): 1039–1045. doi:10.1016/j.orggeochem.2008.02.006. hdl: 1912/2459 . ISSN   0146-6380.
  16. ↑ Kim, Jung-Hyun; van der Meer, Jaap; Schouten, Stefan; Helmke, Peer; Willmott, Veronica; Sangiorgi, Francesca; Koç, Nalân; Hopmans, Ellen C.; Damsté, Jaap S. Sinninghe (2010-08-15). "New indices and calibrations derived from the distribution of crenarchaeal isoprenoid tetraether lipids: Implications for past sea surface temperature reconstructions". Geochimica et Cosmochimica Acta. 74 (16): 4639–4654. Bibcode:2010GeCoA..74.4639K. doi:10.1016/j.gca.2010.05.027. ISSN   0016-7037.
  17. ↑ Shah, Sunita R.; Mollenhauer, Gesine; Ohkouchi, Naohiko; Eglinton, Timothy I.; Pearson, Ann (2008). "Origins of archaeal tetraether lipids in sediments: Insights from radiocarbon analysis". Geochimica et Cosmochimica Acta. 72 (18): 4577–4594. Bibcode:2008GeCoA..72.4577S. doi:10.1016/j.gca.2008.06.021. hdl: 1912/2486 .
  18. 1 2 3 Schouten S, Huguet C, Hopmans EC, Kienhuis MV, Damsté JS (April 2007). "Analytical methodology for TEX86 paleothermometry by high-performance liquid chromatography/atmospheric pressure chemical ionization-mass spectrometry". Analytical Chemistry. 79 (7): 2940–4. doi:10.1021/ac062339v. PMID   17311408.
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