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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. Free, publicly-accessible full text available July 1, 2024
  5. This paper characterizes the acid and cold stress responses of the thermoacidophilic crenarchaeon Saccharolobus islandicus REY15A, showing that each stress results in impaired growth rates, altered GDGT-lipid profiles, and differences in transcriptomes and proteomes. 
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    Free, publicly-accessible full text available July 1, 2024
  6. 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. 
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