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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. 

Bacterial hopanoid lipids are ubiquitous in the geologic record and serve as biomarkers for reconstructing Earth’s climatic and biogeochemical evolution. Specifically, the abundance of 2-methylhopanoids deposited during Mesozoic ocean anoxic events (OAEs) and other intervals has been interpreted to reflect proliferation of nitrogen-fixing marine cyanobacteria. However, there currently is no conclusive evidence for 2-methylhopanoid production by extant marine cyanobacteria. As an alternative explanation, here we report 2-methylhopanoid production by bacteria of the genusNitrobacter, cosmopolitan nitrite oxidizers that inhabit nutrient-rich freshwater, brackish, and marine environments. The model organismNitrobacter vulgarisproduced only trace amounts of 2-methylhopanoids when grown in minimal medium or with added methionine, the presumed biosynthetic methyl donor. Supplementation of cultures with cobalamin (vitamin B₁₂) increased nitrite oxidation rates and stimulated a 33-fold increase of 2-methylhopanoid abundance, indicating that the biosynthetic reaction mechanism is cobalamin dependent. BecauseNitrobacterspp. cannot synthesize cobalamin, we postulate that they acquire it from organisms inhabiting a shared ecological niche—for example, ammonia-oxidizing archaea. We propose that during nutrient-rich conditions, cobalamin-based mutualism intensifies upper water column nitrification, thus promoting 2-methylhopanoid deposition. In contrast, anoxia underlying oligotrophic surface ocean conditions in restricted basins would prompt shoaling of anaerobic ammonium oxidation, leading to low observed 2-methylhopanoid abundances. The first scenario is consistent with hypotheses of enhanced nutrient loading during OAEs, while the second is consistent with the sedimentary record of Pliocene–Pleistocene Mediterranean sapropel events. We thus hypothesize that nitrogen cycling in the Pliocene–Pleistocene Mediterranean resembled modern, highly stratified basins, whereas no modern analog exists for OAEs. 

Abstract A negative carbon isotope excursion recorded in terrestrial and marine archives reflects massive carbon emissions into the exogenic carbon reservoir during the Paleocene-Eocene Thermal Maximum. Yet, discrepancies in carbon isotope excursion estimates from different sample types lead to substantial uncertainties in the source, scale, and timing of carbon emissions. Here we show that membrane lipids of marine planktonic archaea reliably record both the carbon isotope excursion and surface ocean warming during the Paleocene-Eocene Thermal Maximum. Novel records of the isotopic composition of crenarchaeol constrain the global carbon isotope excursion magnitude to −4.0 ± 0.4‰, consistent with emission of >3000 Pg C from methane hydrate dissociation or >4400 Pg C for scenarios involving emissions from geothermal heating or oxidation of sedimentary organic matter. A pre-onset excursion in the isotopic composition of crenarchaeol and ocean temperature highlights the susceptibility of the late Paleocene carbon cycle to perturbations and suggests that climate instability preceded the Paleocene-Eocene Thermal Maximum.