Archaeal Lipid Hydrogen Isotope Signatures of the Metabolically Flexible Archaeoglobus fulgidus During Autotrophy and Heterotrophy (original) (raw)
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Archaeal lipid hydrogen isotopes in a marine thaumarchaeon
2022
The stable hydrogen isotope composition of persistent biomolecules is used as a paleoenvironmental proxy. While much previous work has focused on plant leaf wax-derived n-alkanes, the potential of bacterial and archaeal lipid biomarkers as carriers of H isotope signatures remains underexplored. Here we investigated H isotope distributions in the membrane lipids of the ammonia-oxidizing chemoautotroph Nitrosopumilus maritimus strain SCM1. Hydrogen isotope ratios were measured on the biphytane chains of tetraether membrane lipids extracted from steady-state continuous cultures cultivated at slow, medium, and fast growth rates. In contrast to recent work on bacterial fatty acids, where the direction and magnitude of isotopic fractionation varies widely (ca. 600 energy metabolism, archaeal biphytane data in the present work are relatively invariant. The weighted average 2H/1H fractionation values relative to growth water (2εL/W) only ranged from 272 to 260 a threefold difference in doubling times (30.8 hr to 92.5 hr), yielding an average growth-rate effect of 0.2 depleted than all heterotrophic archaeal and bacterial lipid H isotope measurements in the literature, and on par with those from other autotrophic archaea,
Lipids of marine Archaea: Patterns and provenance in the water-column and sediments
Geochimica et Cosmochimica Acta, 2007
We measured archaeal lipid distributions from globally distributed samples of freshwater, marine, and hypersaline suspended particulate matter. Cluster analysis of relative lipid distributions identified four distinct groups, including: (1) marine epipelagic (<100 m) waters, (2) marine mesopelagic (200-1500 m) and upwelling waters, (3) freshwater/estuarine waters, and (4) hypersaline waters. A pronounced difference in lipid composition patterns is the near absence of ring-containing glycerol dialkyl glycerol tetraethers (GDGTs) at high salinity. Different archaeal communities populate marine (mesophilic Crenarchaeota and Euryarchaeota), and hypersaline environments (halophilic Euryarchaeota) and community shifts can regulate differences in lipid patterns between marine and hypersaline waters. We propose that community changes within meosphilic marine Archaea also regulate the lipid patterns distinguishing epipelagic and mesopelagic/upwelling zones. Changes in the relative amounts of crenarchaeol and caldarchaeol and low relative abundances of ringed structures in surface waters differentiate lipids from the epipelagic and mesopelagic/upwelling waters. Patterns of lipids in mesopelagic (and upwelling) waters are similar to those expected of the ammonia-oxidizing Group I Crenarchaeota, with predominance of crenarchaeol and abundant cyclic GDGTs; non-metric multidimensional analysis (NMDS) shows this pattern is associated with high nitrate concentrations. In contrast, limited culture evidence indicates marine Group II Euryarchaeota may be capable of producing mainly caldarchaeol and some, but not all, of the ringed GDGTs and we suggest that these organisms, along with the Crenarchaeota, contribute to lipids in epipelagic marine waters. Calculated TEX 86 temperatures in mesopelagic samples (reported here and in published data sets) are always much warmer than measured in situ temperatures. We propose lipids used in the temperature proxy derive from both Euryarchaeaota and Crenarchaeota, and observed values of TEX 86 are subject to changes in their ecology as influenced by nutrient fluctuations or other perturbations. Applications of published core-top TEX 86-SST correlations require that (1) the surface waters are always composed of similar communities with the same temperature response and (2) that deeper water GDGT production is not transported to the sediments. Our lipid distribution patterns demonstrate both surface-water archaeal community differences (which accompany greater nutrient influxes, shoaling of mesopelagic Crenarchaeota during upwelling periods, and possibly due to an influx of terrestrial Archaea), and changes in organic matter transport through the water column can affect the distribution of lipids recorded in sediments. We therefore suggest that reported temperature shifts in ancient applications indicate TEX 86 lipids recorded not only temperature changes, but also changes in archaeal ecology, nutrient concentrations, and possibly oceanographic conditions.
Effect of growth temperature on ether lipid biochemistry in Archaeoglobus fulgidus
Extremophiles, 2008
The archaea are distinguished by their unique isoprenoid ether lipids, which typically consist of the sn-2,3-diphytanylglycerol diether or sn-2,3-dibiphytanyldiglycerol tetraether core modified with a variety of polar headgroups. However, many hyperthermophilic archaea also synthesize tetraether lipids with up to four pentacyclic rings per 40-carbon chain, presumably to improve membrane thermal stability at temperatures up to∼110 °C. This study aimed to correlate the ratio of tetraether to diether core lipid, as well as the presence of pentacyclic groups in tetraether lipids, with growth temperature for the hyperthermophilic archaeon, Archaeoglobus fulgidus. Analysis of the membrane core lipids of A. fulgidus using APCI–MS analysis revealed that the tetraether-to-diether lipid ratio increases from 0.3 ± 0.1 for cultures grown at 70°C to 0.9 ± 0.1 for cultures grown at 89°C. Thin-layer chromatography (TLC) followed by APCI–MS analysis provided evidence for no more than one pentacycle in the hydrocarbon chains of tetraether lipid from cultures grown at 70°C and up to 2 pentacycles in the tetraether lipid from cultures grown at higher temperatures. Analysis of the polar lipid extract using TLC and negative-ion ESI–MS suggested the presence of diether and tetraether phospholipids with inositol, glycosyl, and ethanolamine headgroup chemistry.
Geochimica et Cosmochimica Acta, 2014
The characteristic glycerol dibiphytanyl glycerol tetraether membrane lipids (GDGTs) of marine ammonia-oxidizing archaea (AOA) are widely used as biomarkers for studying their occurrence and distribution in marine environments and for reconstructing past sea surface temperatures using the TEX 86 index. Despite an increasing use of GDGT biomarkers in microbial ecology and paleoceanography, the physiological and environmental factors influencing lipid composition in AOA, in particular the cyclization of GDGTs, remain unconstrained. We investigated the effect of metabolic state on the composition of intact polar and core lipids and the resulting TEX 86 paleothermometer in pure cultures of the marine AOA Nitrosopumilus maritimus as a function of growth phase. The cellular lipid content ranged from 0.9 to 1.9 fg cell À1 and increased during growth but was lower in the stationary phases, indicating changes in average cell size in response to metabolic status. The relative abundances of monoglycosidic GDGTs increased from 27% in early growth phase to 60% in late stationary phase, while monohydroxylated GDGTs increased only slightly. The proportions of characteristic hexose-phosphohexose GDGTs were up to 7-fold higher during growth than in stationary phase, suggesting that they are valuable biomarkers for the metabolically active fraction of AOA assemblages in the environment. Methoxy archaeol was identified as novel, genuine archaeal lipid of yet unknown function; it is one of the most abundant single compounds in the lipidome of N. maritimus. TEX 86 values of individual intact GDGTs and total GDGTs differed substantially, were generally lower during early and late growth phases than in stationary phase, and did not reflect growth temperature. Consequently, our results strongly suggest that biosynthesis is at least partially responsible for the systematic offsets in TEX 86 values between different intact polar GDGT classes observed previously in environmental samples. Nevertheless, differences in degradation rates of intact polar GDGTs may influence the TEX 86 index because the intact polar lipid precursors differ for individual core GDGTs and moreover their relative abundances change with growth stage, which may result in distinct release rates of core GDGTs from their polar precursors. Overall, our findings stress the need to accurately describe the factors influencing GDGT cyclization in thaumarchaea and thus paleotemperature reconstructions.