Archaeal Lipid Hydrogen Isotope Signatures of the Metabolically Flexible Archaeoglobus fulgidus During Autotrophy and Heterotrophy (original) (raw)
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,
Annual Review of Earth and Planetary Sciences, 2012
Hydrogen-isotopic abundances of lipid biomarkers are emerging as important proxies in the study of ancient environments and ecosystems. A decade ago, pioneering studies made use of new analytical methods and demonstrated that the hydrogen-isotopic composition of individual lipids from aquatic and terrestrial organisms can be related to the composition of their growth (i.e., environmental) water. Subsequently, compound-specific deuterium/hydrogen (D/H) ratios of sedimentary biomarkers have been increasingly used as paleohydrological proxies over a range of geological timescales. Isotopic fractionation observed between hydrogen in environmental water and hydrogen in lipids, however, is sensitive to biochemical, physiological, and environmental influences on the composition of hydrogen available for biosynthesis in cells. Here we review the factors and processes that are known to influence the hydrogen-isotopic compositions of lipids-especially n-alkanes-from photosynthesizing organisms, and we provide a framework for interpreting their D/H ratios from ancient sediments and identify future research opportunities. 222 Sachse et al. Annu. Rev. Earth Planet. Sci. 2012.40:221-249. Downloaded from www.annualreviews.org by Texas A&M University -College Station on 05/03/12. For personal use only. www.annualreviews.org • Molecular Paleohydrology 223 Annu. Rev. Earth Planet. Sci. 2012.40:221-249. Downloaded from www.annualreviews.org by Texas A&M University -College Station on 05/03/12. For personal use only. 224 Sachse et al. Annu. Rev. Earth Planet. Sci. 2012.40:221-249. Downloaded from www.annualreviews.org by Texas A&M University -College Station on 05/03/12. For personal use only. www.annualreviews.org • Molecular Paleohydrology 225 Annu. Rev. Earth Planet. Sci. 2012.40:221-249. Downloaded from www.annualreviews.org by Texas A&M University -College Station on 05/03/12. For personal use only.
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.
Hydrogen-isotopic variability in lipids from Santa Barbara Basin sediments
Geochimica Et Cosmochimica Acta, 2009
We conducted an extensive survey of hydrogen-isotopic compositions (D/H ratios) of diverse sedimentary lipids from the Santa Barbara Basin (SBB), offshore southern California. The main goal of this survey was to assess the diversity of D/H ratios in lipids from marine sediments, in order to provide a more detailed understanding of relevant biological and geochemical factors impacting lipid isotopic variability. A total of 1182 individual dD values are reported from two stations in SBB, one located in the suboxic basin depocenter and the other on the fully oxic flank of the basin. Sediments collected from the basin depocenter span a depth of $2.5 m and reach the methanogenic zone. Lipids that were analyzed include n-alkanes, n-alkanols and alkenols, short-and long-chain fatty acids, linear isoprenoids, steroids, and hopanoids, and exhibit several systematic patterns. First, there are no significant differences in dD values between the two sampling locations, nor with increasing depth for most lipids, indicating that degradation does not influence sedimentary lipid dD values. Second, relatively large differences in dD values among differing molecular structures are observed in all samples. n-Alkyl lipids of probable marine origin have typical dD values between À150 and À200&, those from terrestrial leaf waxes and aquatic plants range from À80 to À170&, while petroleum n-alkanes are typically À90 to À150&. Third, lipids inferred to derive from bacteria (branched fatty acids and hopanols) living at the sediment surface or in the water column tend to be D-enriched relative to similar algal products by 30& or more. At the same time, several other lipids have dD values that decrease strongly with depth, presumably as a result of in situ production by anaerobic bacteria. This dichotomy in isotopic compositions of bacterial lipids is inconsistent with a nearly constant D/H fractionation during lipid biosynthesis, and likely reflects significant variations associated with metabolism.
Archaeal lipids trace ecology and evolution of marine ammonia-oxidizing archaea
Proceedings of the National Academy of Sciences of the United States of America, 2022
Archaeal membrane lipids are widely used for paleotemperature reconstructions, yet these molecular fossils also bear rich information about ecology and evolution of marine ammonia-oxidizing archaea (AOA). Here we identified thermal and nonthermal behaviors of archaeal glycerol dialkyl glycerol tetraethers (GDGTs) by comparing the GDGT-based temperature index (TEX86) to the ratio of GDGTs with two and three cyclopentane rings (GDGT-2/GDGT-3). Thermal-dependent biosynthesis should increase TEX86and decrease GDGT-2/GDGT-3 when the ambient temperature increases. This presumed temperature-dependent (PTD) trend is observed in GDGTs derived from cultures of thermophilic and mesophilic AOA. The distribution of GDGTs in suspended particulate matter (SPM) and sediments collected from above the pycnocline—shallow water samples—also follows the PTD trend. These similar GDGT distributions between AOA cultures and shallow water environmental samples reflect shallow ecotypes of marine AOA. While there are currently no cultures of deep AOA clades, GDGTs derived from deep water SPM and marine sediment samples exhibit nonthermal behavior deviating from the PTD trend. The presence of deep AOA increases the GDGT-2/GDGT-3 ratio and distorts the temperature-controlled correlation between GDGT-2/GDGT-3 and TEX86. We then used Gaussian mixture models to statistically characterize these diagnostic patterns of modern AOA ecology from paleo-GDGT records to infer the evolution of marine AOA from the Mid-Mesozoic to the present. Long-term GDGT-2/GDGT-3 trends suggest a suppression of today’s deep water marine AOA during the Mesozoic–early Cenozoic greenhouse climates. Our analysis provides invaluable insights into the evolutionary timeline and the expansion of AOA niches associated with major oceanographic and climate changes.
Chemical Geology, 2014
The δD of fatty acids is emerging as an important marine biogeochemical proxy, but the microbiological and environmental factors controlling the variations of δD of the lipids are not fully constrained. We report here the first measurement of D/H ratios of fatty acids in a piezophilic bacterium and show that hydrostatic pressure and the lipid biosynthetic pathway probably exerts dominant control over the δD of fatty acids. Piezophilic bacterium Moritella japonica DSK1 was grown at a pressure of 30 MPa with glucose as substrate. Fatty acids in DSK1 showed vastly varied δD, ranging from +44.4 to −171‰. Short-chain fatty acids (SCFA), which are synthesized by the fatty acid synthase (FAS) pathway, had positive δD (average +3‰), whereas long-chain polyunsaturated fatty acid (LC-PUFA) synthesized via the polyketide pathway exhibited much depleted δD (−171‰). Our results suggest that the lipid biosynthetic pathways can exert first-order control on the hydrogen isotope signature of bacterial membrane lipids under elevated pressure. Our findings have important implications in marine biogeochemistry. D-depleted fatty acids in marine sediments and in the water column may be derived from piezophilic bacterial reworking and resynthesis of organic matter at high pressure condition. Thus, caution must be exercised in the interpretation of hydrogen isotope signatures of lipids in, e.g., deducing sources of organic matter and tracing microbial biogeochemical processes in the deep ocean and the deep biosphere.
Biogeosciences Discussions, 2017
The hydrogen isotope composition (δ<sup>2</sup>H) of biomarkers produced by algae is strongly influenced by the δ<sup>2</sup>H values of the water in which they grew. δ<sup>2</sup>H values of algal biomarkers preserved in lake sediments are thus a useful tool for reconstructing past changes in lake water δ2H values, which can be used to infer hydroclimate variability. However, studies from laboratory cultures of marine algae have shown that a number of factors can influence the magnitude of hydrogen isotope fractionation between algal lipids and their source water, including temperature and growth rates. Quantifying the natural extent of these changes in freshwater lacustrine settings and identifying their causes is essential for robust application of δ<sup>2</sup>H values of algal lipids as paleohydroclimate proxies, yet the influence of these factors remains poorly constrained.<br><br> This work targets the effect of temp...
Origins of archaeal tetraether lipids in sediments: Insights from radiocarbon analysis
Geochimica et Cosmochimica Acta, 2008
Understanding the supply and preservation of glycerol dibiphytanyl glycerol tetraethers 2 (GDGTs) in marine sediments helps inform their use in paleoceanography. Compound-specific 3 radiocarbon measurements of sedimentary alkenones from multiple environments have been 4 used to gain insight into processes that affect paleo-temperature reconstructions. Similar 5 analyses are warranted to investigate how analogous processes affecting GDGTs impact TEX 86 6 paleotemperatures. Here we present radiocarbon measurements on individual GDGTs from 7 Bermuda Rise and Santa Monica Basin sediments and discuss the results in the context of 8 previous studies of co-depositional alkenones and foraminifera. The 14 C contents of GDGTs and 9 planktonic foraminifera in Bermuda Rise are very similar, suggesting a local source; and TEX 86 -10 derived temperatures agree more closely with foraminiferal temperatures than do 11 temperatures. In contrast, GDGTs in Santa Monica Basin are depleted in 14 C relative to both 12 alkenones and foraminifera, and TEX 86 temperatures agree poorly with known surface water 13 values. We propose three possible factors that could explain these results: (i) GDGTs may be 14 labile relative to alkenones during advective transport through oxic waters; (ii) archaeal 15 production deep in the water column may contribute 14 C-depleted GDGTs to sediments; and (iii) 16 some GDGTs also may derive from sedimentary archaeal communities. Each of these three 17 processes is likely to occur with varying relative importance depending on geographic location. 18 The latter two may help to explain why TEX 86 temperature reconstructions from Santa Monica 19 Basin do not appear to reflect actual sea surface temperatures. Terrigenous GDGTs are unlikely 20 to be major contributors to Bermuda Rise or Santa Monica Basin sediments, based on values of 21 the BIT index. The results also indicate that the crenarchaeol regioisomer is governed by 22 processes different from other GDGTs. Individual measurements of the crenarchaeol regioisomer 23 are significantly depleted in 14 C relative to co-occurring GDGTs, indicating an alternative origin 24 for this compound that presently remains unknown. Re-examination of the contribution of 25 crenarchaeol regioisomer to the TEX 86 index shows that it is a significant influence on the 26 sensitivity of temperature reconstructions.
Geobiology, 2006
The capability of Time of Flight-Secondary Ion Mass Spectrometry (ToF-SIMS) of analysing molecular archaeal biomarkers in geobiological samples was tested and demonstrated. Using a bismuth cluster primary ion source, isopranyl glycerol di-and tetraether core lipids were detected in small amounts of total organic extracts from methanotrophic microbial mats, simultaneously and without further chemical treatment and chromatographic separation. ToF-SIMS was also employed to track the distribution of fossilized ether lipids in a massive carbonate (aragonite) microbialite that precipitated as a result of the microbial anaerobic oxidation of methane. An unambiguous signal was obtained when analysing a freshly broken rock surface (base of a microdrill core). Though some limitation occurred due to µ m-topographical effects (sample roughness), it was possible to display the abundance of high molecular weight (C 86 ) of tetraethers exposed in particular regions of the rock surface. 'Molecular mapping' revealed that a part of these molecules was encased within the rock fabric in a cluster-like distribution that might trace the arrangement of the calcifying microbial colonies in the once active mat system. The results reveal promising perspectives of ToF-SIMS for (i) the quasi-nondestructive analysis of lipids in extremely small geobiological samples at low concentrations; (ii) resolving the spatial distribution of these compounds on a µ m 2 -to cm 2 -scale; and (iii) the more exact assignment of lipid biomarkers to their biological source. Fig. 4 Molecular imaging at the base of the seep carbonate drill core (area of view: 500 × 500 µm 2 ). The intensity shows the lateral variation of the selected signals derived (A) from carbonate (CaO + + CaOH + ) and (B) from the sodium adduct ions [M + Na] + of archaeal glycerol dialkyl glycerol tetraethers (GDGT) in the 1316-1322 Da mass range. The right image (C) shows an overlay of the two ion images. The white line approximately delimits the 'area of levelness' plain enough to produce consistent mapping results. The mapping of the GDGT suggests a partly cluster-like distribution of the archaeal biomarkers in the rock fabric (bottom of area of interest). 82 V. THIEL et al.
Archaeal lipids in Mediterranean cold seeps: molecular proxies for anaerobic methane oxidation
Geochimica et Cosmochimica Acta, 2001
We investigated the distributions and ␦ 13 C values of biomarkers for Archaea associated with anaerobic methane oxidation in disparate settings throughout two Eastern Mediterranean mud dome fields. All major classes of archaeal lipids are present in the studied sediments, including isoprenoid glycerol diethers, isoprenoid glycerol dialkyl glycerol tetraethers, and irregular isoprenoid hydrocarbons. Of the compounds present, many, including a novel glycerol tetraether and sn-3-hydroxyarchaeol, have not been previously reported for settings in which methane oxidation is presumed to occur. Archaeal lipids are depleted in 13 C, indicating that the Archaea from which they derive are either directly or indirectly involved with methane consumption. The most widespread archaeal lipids are archaeol, PMI, and glycerol tetraethers, and these compounds are present at all active sites. However, archaeal lipid abundances and distributions are highly variable; ratios of crocetane, PMI, and hydroxyarchaeol relative to archaeol vary from 0 to 6.5, from 0 to 2, and from 0 to 1, respectively. These results suggest that archaeal communities differ amongst the sites examined. In addition, carbon isotopic variability amongst archaeal biomarkers in a given mud breccia can be as large as 24 ‰, suggesting that even at single sites multiple archaeal species perform or are supported by anaerobic methane oxidation.
1999
Hydrogen isotope ratios (D/H) of lipid biomarkers extracted from aquatic sediments were measured to determine whether they can be used as a proxy for D/H of environmental water. Values of ␦D were determined by using a recently developed isotope-ratio-monitoring gas chromatograph-mass spectrometer system (irmGCMS) and were confirmed by conventional hydrogen isotopic measurements (i.e., combustion followed by reduction) on individual compounds isolated by preparative capillary gas chromatography. Diverse lipids (alkanes, n-alkanols, sterols, and pentacyclic triterpenols) were analyzed to examine hydrogenisotopic controls on lipids of varying origin and biosynthetic pathway. For algal sterols (24-methylcholest-3-ol, 24-ethylcholest-5,22-dien-3-ol, and 4,23,24-trimethylcholesterol, or dinosterol), the fractionation between sedimentary lipids and environmental water was Ϫ201 Ϯ 10‰ and was similar in both marine and freshwater sites. In a sediment from a small lake in a forested catchment, triterpenols from terrestrial sources were enriched in D by 30‰ relative to algal sterols. Apparent fractionation factors for n-alkyl lipids were smaller than those of triterpenols and were more variable, probably reflecting multiple sources for these compounds. We conclude that hydrogen-isotopic analyses of algal sterols provide a viable means of reconstructing D/H of environmental waters. Results are less ambiguous than reconstructions based on analyses of kerogen or other operationally defined organic matter fractions.
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.