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The three-isotope system of oxygen (16O, 17O, 18O) is a powerful tool to study environmental oxidation chemistry and cycling of oxygen-bearing species (e.g., sulfates, nitrates, carbonates, etc.). Despite its evident utility, little work has focused onextending the triple oxygen isotope (Δ’17O) tool to oxygen contained in organic matter (OM). This is largely due to methodological challenges with isolating OM-bound oxygen and preparing it for isotopic analysis. Herein, we report on a newly developed method for high-precision Δ’17O measurements of OM (Δ’17O precision of 0.020‰) and apply this technique to investigate partial photochemical oxidation of Suwannee River natural OM in air-equilibrated aquatic samples. Through this, we reveal that the oxygen isotope evolution of the Suwannee OM supports a model whereby OM partial photo-oxidation proceeds via one or more reactive oxygen intermediates. Our measurements further highlight the potential of triple oxygen isotope analyses on OM-bound oxygen to fingerprint OM oxidation pathways, redox chemistry, and source and synthesis reactions. 

The geochemical characterization of phytoplankton-derived organic compounds found in marine sediments has been widely used to reconstruct atmospheric pCO2 thoughout the Cenozoic. This is possible owing to a well-established relationship between the carbon isotope ratios of phytoplankton biomass and CO2 concentration in the ambient seawater. An ideal molecular target for such proxy reconstructions would be degradation resistant on geologic timescales and unambiguously associated with known, experimentally tractable, organisms, so that species-specific models can be developed, calibrated, and applied to appropriate material. However, existing organic matter targets do not quite meet these criteria, primarily owing to ambiguity in the source species of recalcitrant compounds in deep time. Here we explore the potential of a novel organic carbon target for isotopic analysis: acidic polysaccharides extracted from the calcite plates (coccoliths) that are produced by all calcifying haptophytes. Carbohydrates are usually rapidly remineralized in sediments, but coccolith-associated polysaccharides (CAPs) are mechanically protected from diagenesis within the coccolith calcite lattice. Coccoliths can be taxonomically separated by size and identified, often to species level, prior to CAP extraction, providing a species-specific record. Coccolith morphology and composition are important additional sources of information, which are then unambiguously associated with the extracted CAPs. We find that carbon isotope ratios of CAPs changed in response to the environmental changes associated with a glacial cycle, which we attribute to temperature-driven changes in average growth rate. Once the underlying biosynthetic processes and the associated isotope effects are better understood, this archive of pristine organic matter has the potential to provide insight into phytoplankton growth rates and atmospheric pCO2 far beyond the Cenozoic, to when the first coccolithophores inhabited the surface ocean over 200 million years ago. 

ABSTRACT The degree of cyclization, or ring index (RI), in archaeal glycerol dibiphytanyl glycerol tetraether (GDGT) lipids was long thought to reflect homeoviscous adaptation to temperature. However, more recent experiments show that other factors (e.g., pH, growth phase, and energy flux) can also affect membrane composition. The main objective of this study was to investigate the effect of carbon and energy metabolism on membrane cyclization. To do so, we cultivatedAcidianussp. DS80, a metabolically flexible and thermoacidophilic archaeon, on different electron donor, acceptor, and carbon source combinations (S⁰/Fe³⁺/CO₂, H₂/Fe³⁺/CO₂, H₂/S⁰/CO₂, or H₂/S⁰/glucose). We show that differences in energy and carbon metabolism can result in over a full unit of change in RI in the thermoacidophileAcidianussp. DS80. The patterns in RI correlated with the normalized electron transfer rate between the electron donor and acceptor and did not always align with thermodynamic predictions of energy yield. In light of this, we discuss other factors that may affect the kinetics of cellular energy metabolism: electron transfer chain (ETC) efficiency, location of ETC reaction components (cytoplasmicvs.extracellular), and the physical state of electron donors and acceptors (gasvs.solid). Furthermore, the assimilation of a more reduced form of carbon during heterotrophy appears to decrease the demand for reducing equivalents during lipid biosynthesis, resulting in lower RI. Together, these results point to the fundamental role of the cellular energy state in dictating GDGT cyclization, with those cells experiencing greater energy limitation synthesizing more cyclized GDGTs. IMPORTANCESome archaea make unique membrane-spanning lipids with different numbers of five- or six-membered rings in the core structure, which modulate membrane fluidity and permeability. Changes in membrane core lipid composition reflect the fundamental adaptation strategies of archaea in response to stress, but multiple environmental and physiological factors may affect the needs for membrane fluidity and permeability. In this study, we tested howAcidianussp. DS80 changed its core lipid composition when grown with different electron donor/acceptor pairs. We show that changes in energy and carbon metabolisms significantly affected the relative abundance of rings in the core lipids of DS80. These observations highlight the need to better constrain metabolic parameters, in addition to environmental factors, which may influence changes in membrane physiology in Archaea. Such consideration would be particularly important for studying archaeal lipids from habitats that experience frequent environmental fluctuations and/or where metabolically diverse archaea thrive. 

Archaea adjust the number of cyclopentane rings in their glycerol dibiphytanyl glycerol tetraether (GDGT) membrane lipids as a homeostatic response to environmental stressors such as temperature, pH, and energy availability shifts. However, archaeal expression patterns that correspond with changes in GDGT composition are less understood. Here we characterize the acid and cold stress responses of the thermoacidophilic crenarchaeonSaccharolobus islandicusREY15A using growth rates, core GDGT lipid profiles, transcriptomics and proteomics. We show that both stressors result in impaired growth, lower average GDGT cyclization, and differences in gene and protein expression. Transcription data revealed differential expression of the GDGT ring synthasegrsBin response to both acid stress and cold stress. Although the GDGT ring synthase encoded bygrsBforms highly cyclized GDGTs with ≥5 ring moieties,S. islandicus grsBupregulation under acidic pH conditions did not correspond with increased abundances of highly cyclized GDGTs. Our observations highlight the inability to predict GDGT changes from transcription data alone. Broader analysis of transcriptomic data revealed thatS. islandicusdifferentially expresses many of the same transcripts in response to both acid and cold stress. These included upregulation of several biosynthetic pathways and downregulation of oxidative phosphorylation and motility. Transcript responses specific to either of the two stressors tested here included upregulation of genes related to proton pumping and molecular turnover in acid stress conditions and upregulation of transposases in cold stress conditions. Overall, our study provides a comprehensive understanding of the GDGT modifications and differential expression characteristic of the acid stress and cold stress responses inS. islandicus. 

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 (TEX 86 ) to the ratio of GDGTs with two and three cyclopentane rings (GDGT-2/GDGT-3). Thermal-dependent biosynthesis should increase TEX 86 and 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 TEX 86 . 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.