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  1. Abstract

    Hopanoid lipids, bacteriohopanols and bacteriohopanepolyols, are membrane components exclusive to bacteria. Together with their diagenetic derivatives, they are commonly used as biomarkers for specific bacterial groups or biogeochemical processes in the geologic record. However, the sources of hopanoids to marine and freshwater environments remain inadequately constrained. Recent marker gene studies suggest a widespread potential for hopanoid biosynthesis in marine bacterioplankton, including nitrifying (i.e., ammonia‐ and nitrite‐oxidizing) bacteria. To explore their hopanoid biosynthetic capacities, we studied the distribution of hopanoid biosynthetic genes in the genomes of cultivated and uncultivated ammonia‐oxidizing (AOB), nitrite‐oxidizing (NOB), and complete ammonia‐oxidizing (comammox) bacteria, finding that biosynthesis of diverse hopanoids is common among seven of the nine presently cultivated clades of nitrifying bacteria. Hopanoid biosynthesis genes are also conserved among the diverse lineages of bacterial nitrifiers detected in environmental metagenomes. We selected seven representative NOB isolated from marine, freshwater, and engineered environments for phenotypic characterization. All tested NOB produced diverse types of hopanoids, with some NOB producing primarily diploptene and others producing primarily bacteriohopanepolyols. Relative and absolute abundances of hopanoids were distinct among the cultures and dependent on growth conditions, such as oxygen and nitrite limitation. Several novel nitrogen‐containing bacteriohopanepolyols were tentatively identified, of which the so called BHP‐743.6 was present in all NOB. Distinct carbon isotopic signatures of biomass, hopanoids, and fatty acids in four tested NOB suggest operation of the reverse tricarboxylic acid cycle inNitrospiraspp. andNitrospina gracilisand of the Calvin–Benson–Bassham cycle for carbon fixation inNitrobacter vulgarisandNitrococcus mobilis. We suggest that the contribution of hopanoids by NOB to environmental samples could be estimated by their carbon isotopic compositions. The ubiquity of nitrifying bacteria in the ocean today and the antiquity of this metabolic process suggest the potential for significant contributions to the geologic record of hopanoids.

     
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  2. Summary

    Adaptation of lipid membrane composition is an important component of archaeal homeostatic response. Historically, the number of cyclopentyl and cyclohexyl rings in the glycerol dibiphytanyl glycerol tetraether (GDGT) Archaeal lipids has been linked to variation in environmental temperature. However, recent work with GDGT‐making archaea highlight the roles of other factors, such as pH or energy availability, in influencing the degree of GDGT cyclization. To better understand the role of multiple variables in a consistent experimental framework and organism, we cultivated the model CrenarchaeonSulfolobus acidocaldariusDSM639 at different combinations of temperature, pH, oxygen flux, or agitation speed. We quantified responses in growth rate, biomass yield, and core lipid compositions, specifically the degree of core GDGT cyclization. The degree of GDGT cyclization correlated with growth rate under most conditions. The results suggest the degree of cyclization in archaeal lipids records a universal response to energy availability at the cellular level, both in thermoacidophiles, and in other recent findings in the mesoneutrophilic Thaumarchaea. Although we isolated the effects of key individual parameters, there remains a need for multi‐factor experiments (e.g., pH + temperature + redox) in order to more robustly establish a framework to better understand homeostatic membrane responses.

     
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  3. 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.

     
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  4. Abstract

    The TEX86proxy, based on the distribution of isoprenoid glycerol dialkyl glycerol tetraethers (iGDGTs) from planktonic Thaumarchaeota, is widely used to reconstruct sea surface temperature (SST). Recent observations of species‐specific and regionally dependent TEX86‐SST relationships in cultures and the modern ocean raise the question of whether nonthermal factors may have impacted TEX86paleorecords. Here we evaluate the effects of ecological changes on TEX86using one Pliocene and two Pleistocene sapropels from the Mediterranean Sea. We find that TEX86‐derived SSTs deviate from‐derived SSTs before, during, and after each sapropel event.‐derived SSTs vary by less than 6 °C, while TEX86‐derived SSTs vary by up to 15 °C within a single record. Compound‐specific carbon isotope compositions indicate minimal confounding influence on TEX86from exogenous sources. Some of the variation can be accounted for by changes in nitrogen cycling intensity affecting thaumarchaeal iGDGT biosynthesis, as demonstrated by an inverse relationship between TEX86and δ15NTN. TEX86‐derived SSTs also consistently show warm anomalies in the Pleistocene, while the Pliocene samples exhibit both warmer and cooler relative offsets. These anomalies result from systematic differences between Plio‐Pleistocene iGDGT distributions and both modern Mediterranean and modern, globally distributed core top samples. Through characteristic GDGT distributions, we suggest the existence of three distinct endemic populations of Thaumarchaeota in the Pliocene, Pleistocene, and modern Mediterranean Sea, respectively. Importantly, these communities prevailed during both sapropel and oligotrophic conditions. Our results demonstrate that ecological and community‐specific effects must be considered when applying the TEX86proxy to paleorecords.

     
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  5. Abstract

    Key features of late Neogene climate remain uncertain due to conflicting records derived from different sea surface temperature (SST) proxies. To understand scenarios in which proxy‐derived temperature estimates can be used interchangeably or are instead measuring different aspects of the same system, it is necessary to explore both the consistencies and differences between specific paleothermometers. Here, we report orbital‐scale climate records from ODP Site 846 in the eastern equatorial Pacific (EEP) for the interval from ~5–6 Ma using alkenone and archaeal lipid paleothermometers. Results from both proxies are similar in their secular trends and magnitude of long‐term temperature change, and spectral analysis demonstrates that the records are coherent and in‐phase in both the obliquity and precession bands. However, we find that the temperatures reconstructed by TEX86are consistently offset toward colder values by ~2 °C relative to Uk′37‐derived temperatures in global calibrations, or by ~0.8 °C in Bayesian‐based calibrations. All combinations of calibrations also yield approximately twice the amplitude of orbital‐scale variation in TEX86relative to Uk′37‐derived temperature fluctuations. Both temperature proxies are negatively correlated with sedimentary alkenone concentrations, which we use as an indicator of increased export productivity. Removing this productivity contribution from TEX86results in an adjusted TEX86record with temperature sensitivity identical to Uk′37. In future applications, this signal may be decoupled using additional sedimentary indicators of paleoproductivity, which likely will be most important for upwelling zone environments. There remain other nonexplained factors that contribute to differences between TEX86and Uk′37that warrant additional investigation.

     
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  6. Summary

    Microorganisms regulate the composition of their membranes in response to environmental cues. Many Archaea maintain the fluidity and permeability of their membranes by adjusting the number of cyclic moieties within the cores of their glycerol dibiphytanyl glycerol tetraether (GDGT) lipids. Cyclized GDGTs increase membrane packing and stability, which has been shown to help cells survive shifts in temperature and pH. However, the extent of this cyclization also varies with growth phase and electron acceptor or donor limitation. These observations indicate a relationship between energy metabolism and membrane composition. Here we show that the average degree of GDGT cyclization increases with doubling time in continuous cultures of the thermoacidophileSulfolobus acidocaldarius(DSM 639). This is consistent with the behavior of a mesoneutrophile,Nitrosopumilus maritimusSCM1. Together, these results demonstrate that archaeal GDGT distributions can shift in response to electron donor flux and energy availability, independent of pH or temperature. Paleoenvironmental reconstructions based on GDGTs thus capture the energy available to microbes, which encompasses fluctuations in temperature and pH, as well as electron donor and acceptor availability. The ability of Archaea to adjust membrane composition and packing may be an important strategy that enables survival during episodes of energy stress.

     
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  7. Free, publicly-accessible full text available July 1, 2024