Distribution of Complex and Core Lipids within New Hyperthermophilic Members of the Archaea Domain

Trincone, Antonio; Nicolaus, Barbara; Palmieri, Gianna; Rosa, Mario De; Huber, Robert; Huber, Gertrud; Stetter, Karl O.; Gambacorta, Agata

doi:10.1016/s0723-2020(11)80130-x

Cited by 41 publications

(21 citation statements)

References 28 publications

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“…Sprott et al 12 detected ions corresponding to all types of components in total polar lipid extracts using fast atom bombardment mass spectrometry (FABMS) from several archaeal thermophiles, to show the presence of minor amount of diether lipids in Sulfolobus acidocaldarius adding to the ether lipids reported by Gulik et al 9 and Trincone et al 8 High‐performance liquid chromatographic (HPLC) analyses were carried out for tetraethers obtained by acid hydrolysis of complex lipids from Desulfurolobus ambivalence and Sulfolobus solfataricus 13. The results revealed that the cyclic components of tetraether fractions, in particular in the case of D. ambivalens , showed significant differences.…”

Section: Introductionmentioning

confidence: 99%

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Facile distinction of neutral and acidic tetraether lipids in archaea membrane by halogen atom adduct ions in electrospray ionization mass spectrometry

et al. 2002

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Calditocaldarchaeol (neutral tetraether lipid) from Sulfolobus acidocaldarius (acidothermophilic archaea) and intact total lipid from the thermoacidophilic archaea Sulfolobus sp. was examined by electrospray ionization time-of-flight mass spectrometry in the negative-ion mode using high resolution. When the sample was injected as a solution in a 3:1 mixture of methanol (MeOH) and chloroform (CHCl(3)) using an infusion system, the total ether lipid afforded molecular-related ions as [M - H](-) for acidic polar lipids containing a phosphoric or sulfuric group, and as [M + Cl](-) ion for neutral glycolipids. The attachment of chloride was confirmed by the observation of [M + Br](-) ion, instead of [M + Cl](-) ion, when a 3:1 mixture of MeOH and CHBr(3) was used in place of MeOH-CHCl(3) as the solvent. The composition of tetraether neutral glycolipids that are different from each other only in the number of five-membered rings in the isoprenoid chain was determined on the basis of the isotope-resolved mass spectrum of [M + Cl](-) ions. As for acidic tetraether lipids, molecular-related ions [M - H](-)) were not observed when the 3:1 MeOH-CHBr(3) mixture was used as the solvent. These results together afforded a facile method of distinguishing neutral from acidic tetraether lipids in intact total lipids of acidothermophilic archaea. This method was applied to determine the difference of the number of five-membered rings in isoprenyl chains of neutral tetraether glycolipids yielded by the Sulfolobus sp. grown at different temperatures. Discrimination of neutral tetraether glycolipids from acidic tetraether lipids in the total lipids obtained from Thermoplasma sp. was also achieved by this method.

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Section: Introductionmentioning

confidence: 99%

“…The complex ether lipids of Sulfolobus contain phospholipids, glycolipids, phosphoglycolipids and glycolipid sulfate 8. These polar groups contribute significantly to the physical polymorphism of the tetraethers 9.…”

Section: Introductionmentioning

confidence: 99%

Facile distinction of neutral and acidic tetraether lipids in archaea membrane by halogen atom adduct ions in electrospray ionization mass spectrometry

et al. 2002

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“…Depending on the growth temperature, certain thermophilic archaea are capable of controlling membrane fluidity by altering the number of cyclopentane rings from 0 to 8 in the caldarchaeol lipid chains (11). The macrocyclic archaeol lipid has so far been found only in M. jannaschii (6) and Methanococcus igneus (12).…”

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confidence: 99%

Molecular Mechanisms of Water and Solute Transport across Archaebacterial Lipid Membranes

Mathai¹,

Sprott²,

Zeidel³

2001

Journal of Biological Chemistry

144

133

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Archaebacteria thrive in environments characterized by anaeobiosis, saturated salt, and both high and low extremes of temperature and pH. The bulk of their membrane lipids are polar, characterized by the archaeal structural features typified by ether linkage of the glycerol backbone to isoprenoid chains of constant length, often fully saturated, and with sn-2,3 stereochemistry opposite that of glycerolipids of Bacteria and Eukarya. Also unique to these bacteria are macrocyclic archaeol and membrane spanning caldarchaeol lipids that are found in some extreme thermophiles and methanogens. To define the barrier function of archaebacterial membranes and to examine the effects of these unique structural features on permeabilities, we investigated the water, solute (urea and glycerol), proton, and ammonia permeability of liposomes formed by these lipids. Both the macrocyclic archaeol and caldarchaeol lipids reduced the water, ammonia, urea, and glycerol permeability of liposomes significantly (6 -120-fold) compared with diphytanylphosphatidylcholine liposomes. The presence of the ether bond and phytanyl chains did not significantly affect these permeabilities. However, the apparent proton permeability was reduced 3-fold by the presence of an ether bond. The presence of macrocyclic archaeol and caldarchaeol structures further reduced apparent proton permeabilities by 10 -17-fold. These results indicate that the limiting mobility of the midplane hydrocarbon region of the membranes formed by macrocyclic archaeol and caldarchaeol lipids play a significant role in reducing the permeability properties of the lipid membrane. In addition, it appears that substituting ether for ester bonds presents an additional barrier to proton flux.Many archaebacteria thrive in hostile environments, such as hot springs, salt lakes, and acidic or alkaline domains (1, 2). For instance, Methanococcus jannaschii grows optimally at 85°C, pH 6 (3, 4), Thermoplasma acidophilum at 55°C, pH 2.0 (5), and Halobacterium salinarum in near-saturated salt brines (2). The major role of the cell membrane is to provide a selective barrier between the external environment and the inside of the cell. Given the extreme environmental conditions in which these bacteria thrive, it is not surprising that their plasma membranes are composed of lipids that differ markedly in structure and physicochemical properties from the glycerolipids of eubacterial, animal, and plant cell membranes. In these unique bacteria, the membrane lipids are characterized by the presence of ether linkages instead of ester linkages, and they contain regularly branched phytanyl and biphytanyl chains instead of fatty acyl chains (6). The presence of ether rather than ester bonds is thought to contribute to greater chemical stability at extreme pH. Moreover the glycerol ethers contain an sn-2,3 stereochemistry that is opposite that of the naturally occurring sn-1,2 stereochemistry of glycerophospholipids of the other domains (7). The basic lipid core structures of these unique organisms are su...

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“…This temperature is also consistent with the temperature limit observed for methanogenesis using enrichment culture at Yellowstone National Park, which was 72°C (Zeikus et al, 1980). Polar iGDGT-0 at higher temperatures, albeit at low relative abundance, could derive from a large number of microorganisms, but may possibly be connected with the presence of Archaeoglobus , which is known to produce iGDGT-0 as the only iGDGT (Trincone et al, 1992). Several studies have documented Archaeoglobus in Great Basin hot springs at temperatures up to 85°C (Costa et al, 2009; Dodsworth et al, 2011b; Cole et al, 2013; Peacock et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

The distribution and abundance of archaeal tetraether lipids in U.S. Great Basin hot springs

et al. 2013

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Isoprenoidal glycerol dialkyl glycerol tetraethers (iGDGTs) are core membrane lipids of many archaea that enhance the integrity of cytoplasmic membranes in extreme environments. We examined the iGDGT profiles and corresponding aqueous geochemistry in 40 hot spring sediment and microbial mat samples from the U.S. Great Basin with temperatures ranging from 31 to 95°C and pH ranging from 6.8 to 10.7. The absolute abundance of iGDGTs correlated negatively with pH and positively with temperature. High lipid concentrations, distinct lipid profiles, and a strong relationship between polar and core lipids in hot spring samples suggested in situ production of most iGDGTs rather than contamination from local soils. Two-way cluster analysis and non-metric multidimensional scaling (NMS) of polar iGDGTs indicated that the relative abundance of individual lipids was most strongly related to temperature (r2 = 0.546), with moderate correlations with pH (r2 = 0.359), nitrite (r2 = 0.286), oxygen (r2 = 0.259), and nitrate (r2 = 0.215). Relative abundance profiles of individual polar iGDGTs indicated potential temperature optima for iGDGT-0 (≤70°C), iGDGT-3 (≥55°C), and iGDGT-4 (≥60°C). These relationships likely reflect both physiological adaptations and community-level population shifts in response to temperature differences, such as a shift from cooler samples with more abundant methanogens to higher-temperature samples with more abundant Crenarchaeota. Crenarchaeol was widely distributed across the temperature gradient, which is consistent with other reports of abundant crenarchaeol in Great Basin hot springs and suggests a wide distribution for thermophilic ammonia-oxidizing archaea (AOA).

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Distribution of Complex and Core Lipids within New Hyperthermophilic Members of the Archaea Domain

Cited by 41 publications

References 28 publications

Facile distinction of neutral and acidic tetraether lipids in archaea membrane by halogen atom adduct ions in electrospray ionization mass spectrometry

Facile distinction of neutral and acidic tetraether lipids in archaea membrane by halogen atom adduct ions in electrospray ionization mass spectrometry

Molecular Mechanisms of Water and Solute Transport across Archaebacterial Lipid Membranes

The distribution and abundance of archaeal tetraether lipids in U.S. Great Basin hot springs

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