Variation in molecular species of polar lipids from <i>Thermoplasma acidophilum</i> depends on growth temperature

Uda, Ikuko; Sugai, Akihiko; Itoh, Yuko; Itoh, Toshihiro

doi:10.1007/s11745-001-0914-2

Cited by 174 publications

(130 citation statements)

References 18 publications

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“…Experiments using pure cultures show that thermophilic archaea increase the number of cyclopentane units in their membrane lipids in response to temperature or physical agitation (29,30). Pelagic archaeal lipids show a similar response: the relative distribution of GDGTs III, IV, V, and VI defines the TEX 86 index, which has a calibrated relationship to temperature (16).…”

Section: Discussionmentioning

confidence: 99%

Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon

Ingalls

Shah

Hansman

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

425

376

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An ammonia-oxidizing, carbon-fixing archaeon, Candidatus ''Nitrosopumilus maritimus,'' recently was isolated from a salt-water aquarium, definitively confirming that chemoautotrophy exists among the marine archaea. However, in other incubation studies, pelagic archaea also were capable of using organic carbon. It has remained unknown what fraction of the total marine archaeal community is autotrophic in situ. If archaea live primarily as autotrophs in the natural environment, a large ammonia-oxidizing population would play a significant role in marine nitrification. Here we use the natural distribution of radiocarbon in archaeal membrane lipids to quantify the bulk carbon metabolism of archaea at two depths in the subtropical North Pacific gyre. Our compound-specific radiocarbon data show that the archaea in surface waters incorporate modern carbon into their membrane lipids, and archaea at 670 m incorporate carbon that is slightly more isotopically enriched than inorganic carbon at the same depth. An isotopic mass balance model shows that the dominant metabolism at depth indeed is autotrophy (83%), whereas heterotrophic consumption of modern organic carbon accounts for the remainder of archaeal biomass. These results reflect the in situ production of the total community that produces tetraether lipids and are not subject to biases associated with incubation and͞or culture experiments. The data suggest either that the marine archaeal community includes both autotrophs and heterotrophs or is a single population with a uniformly mixotrophic metabolism. The metabolic and phylogenetic diversity of the marine archaea warrants further exploration; these organisms may play a major role in the marine cycles of nitrogen and carbon.biomarkers ͉ carbon isotopes ͉ microbial ecology ͉ nitrogen cycle ͉ oceanography N onthermophilic archaea represent up to 40% of the free-living prokaryotic community in the water column of the world's oceans (1-6), but until recently there has been limited information about the sources of carbon and energy that fuel these organisms (7-11). The characteristic membrane lipids of planktonic archaea include glycerol dialkyl glycerol tetraethers (GDGTs) (12). These compounds are ubiquitous in marine sediments and ocean water (12-15). The relative abundance of individual GDGTs recovered from sediments is used to reconstruct sea-surface temperatures (16)(17)(18). This distribution, known as TEX 86 , has been shown through experimental manipulation of surface-water mesocosm experiments to respond to changes in incubation temperature (18). In addition, the ␦ 13 C values of GDGTs display a remarkably constant offset from ␦ 13 C values of dissolved inorganic carbon (DIC) over a range of settings and geologic time (13,(19)(20)(21). The collective metabolic activities of the numerous archaea in the ocean are likely to play a significant role in the cycling of organic carbon (OC) and nutrients, and their membrane lipids show significant utility for paleoceanography. However, neither the metabolic requiremen...

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Section: Discussionmentioning

confidence: 99%

Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon

Ingalls

Shah

Hansman

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

425

376

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“…We have hypothesized that the formation of the cyclohexane ring is an adaption of the membrane lipids of hyperthermophilic archaea to relatively cold conditions in the open ocean (3,31). It is well known that the presence of cyclopentane rings in GDGTs has a pronounced effect on the thermal transition points of cell membranes composed of GDGTs (7,32). Consequently, hyperthermophilic archaea adjust the physical characteristics of their membranes to higher temperatures by increasing the number of cyclopentane rings.…”

Section: Discussionmentioning

confidence: 99%

Crenarchaeol

Damsté

Schouten

Hopmans

et al. 2002

Journal of Lipid Research

579

106

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The basic structure and stereochemistry of the characteristic glycerol dibiphytanyl glycerol tetraether (GDGT) membrane lipid of cosmopolitan pelagic crenarchaeota has been identified by high field two-dimensional (2D)-NMR techniques. It contains one cyclohexane and four cyclopentane rings formed by internal cyclisation of the biphytanyl chains. Its structure is similar to that of GDGTs biosynthesized by (hyper)thermophilic crenarchaeota apart from the cyclohexane ring. These findings are consistent with the close phylogenetic relationship of (hyper)thermophilic and pelagic crenarchaeota based 16S rRNA. The latter group inherited the biosynthetic capabilities for a membrane composed of cyclopentane ring-containing GDGTs from the (hyper)thermophilic crenarchaeota. However, to cope with the much lower temperature of the ocean, a small but key step in their evolution was the adjustment of the membrane fluidity by making a kink in one of the bicyclic biphytanyl chains by the formation of a cyclohexane ring.This prevents the dense packing characteristic for the cyclopentane ring-containing GDGTs membrane lipids used by hyperthermophilic crenarchaeota to adjust their membrane fluidity to high temperatures. -Sinninghe Damsté, J. S., S. Schouten, E. C. Hopmans, A. C. T. van Duin, and J. A. J. Geenevasen. Crenarchaeol: The characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota.

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“…These lipids may contribute to the organisms' adaptation to extremely low pHs and high temperatures. The number of cyclopentane rings in the caldarchaeol moiety in a thermophilic archaeon varies with growth temperature (11,30,31). The variation is considered to be an adaptation to different temperatures by adjusting membrane fluidity (15).…”

mentioning

confidence: 99%

Effects of pH and Temperature on the Composition of Polar Lipids in Thermoplasma acidophilum HO-62

et al. 2008

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Thermoplasma acidophilum HO-62 was grown at different pHs and temperatures, and its polar lipid compositions were determined. Although the number of cyclopentane rings in the caldarchaeol moiety increased when T. acidophilum was cultured at high temperature, the number decreased at low pHs. Glycolipids, phosphoglycolipids, and phospholipids were analyzed by high-performance liquid chromatography with an evaporative light-scattering detector. The amount of caldarchaeol with more than two sugar units on one side increased under low-pH and high-temperature conditions. The amounts of glycolipids increased and those of phosphoglycolipids decreased under these conditions. The proton permeability of the liposomes obtained from the phosphoglycolipids that contained two or more sugar units was lower than that of the liposomes obtained from the phosphoglycolipids that contained one sugar unit. From these results, we propose the hypothesis that T. acidophilum adapts to low pHs and high temperatures by extending sugar chains on their cell surfaces, as well as by varying the number of cyclopentane rings.Archaea have unique plasma membranes made of isoprenoid glycerol ether (14,19). The isoprenoid chains of archaeal membrane lipids consist of the hydrocarbons C 20 , C 25 , and C 40 . The C 20 and/or C 25 chain is linked to glycerol to form 2,3-di-O-alkyl-sn-glycerol diether (archaeol and its variants [10,20]), and the C 40 (biphytanyl) chains are connected to two glycerols to form dibiphytanyl diglyceryl tetraether (caldarchaeol [10,19,22]), as shown in Fig. 1. Other analogues (e.g., macrocyclic archaeol and glycerol-trialkyl-glycerol tetraether) have also been reported (7, 12). Various archaeal lipid structures have been summarized by Koga and Morii (21). The basic structure of an ether lipid in a hydrocarbon chain consisting of branched C 5 units attached to glycerol by an ether linkage is conserved in archaea. Because of the unique structural features of archaeal lipids, the properties of the membrane consisting of these lipids have been compared with those of the widely distributed ester-type lipids consisting of fatty acids and glycerol (2, 6, 23).The function of glycolipids is generally considered to be the stabilization of the membrane against environmental stresses such as osmotic stress and temperature alterations, through hydrogen bonding via glycosyl head groups (8). Because the amount of glycolipids increases under elevated growth temperature conditions in the thermophilic eubacterium Thermus aquaticus (25) and the algae Cyanidium caldarium (1), sugar residues were thought to be important for growth under hightemperature conditions. The structural features of polar head groups of archaea have also been discussed in relation to chemotaxonomic purposes (for a review, see reference 14).Thermoplasma acidophilum is a facultative anaerobic, thermophilic, and acidophilic archaeon which grows optimally at pHs ranging from 1 to 2 and 55 to 59°C. This microorganism does not have a cell wall outside its cell membrane. Previo...

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Variation in molecular species of polar lipids from Thermoplasma acidophilum depends on growth temperature

Abstract: Five types of molecular species of C40 isoprenoid chains, having different numbers of cyclopentane rings, were detected in the ether core lipid of Thermoplasma acidophilum. The average cyclization number of the hydrocarbon chains in the lipids increased with increasing growth temperatures.

Cited by 174 publications

References 18 publications

Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon

Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon

Crenarchaeol

Effects of pH and Temperature on the Composition of Polar Lipids in Thermoplasma acidophilum HO-62

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