SignificanceReliable prediction of future climate conditions requires a thorough understanding of climate variability throughout Earth’s history. Microbial molecular fossils, such as bacterial membrane-spanning tetraether lipids [branched glycerol dialkyl glycerol tetraethers (brGDGTs)], have proven to be particularly useful for the assessment of past climatic conditions, because they occur ubiquitously in the environment and show compositional changes related to temperature. However, the identity and ecology of brGDGT-producing bacteria is largely unknown, and a mechanistic basis for brGDGT-based paleoclimate reconstruction is still lacking. Here, we present insights into the ecological parameters that affect brGDGT synthesis in lakes, demonstrating that eutrophic lakes with oxygen-deprived bottom waters are the preferred sites for brGDGT-based reconstructions of continental climate.
Significance StatementMicrobial lipid membranes protect and isolate a cell from its environment and play a crucial role in cellular bioenergetics by regulating the flow of nutrients and metabolites to reaction centers within. We demonstrate that membrane lipids change as a function of energy flux using a well-studied archaeon that thrives in acidic hot springs and observe an increase in membrane packing as energy becomes more limited. These observations are consistent with chemostat experiments utilizing a low temperature, neutral pH, marine archaeon. This strategy to regulate membrane homeostasis is common across GDGT-producing lineages, demonstrating that diverse taxa adjust membrane composition in response to chronic energy stress.
The continental settings of Central Asia witnessed increased desertification during the Cenozoic as a result of mountain uplift and the Paratethys retreat. The interaction of these tectonic-scale processes with orbitally forced climate change and their influence on Asia's atmospheric moisture distribution are poorly constrained. A Miocene succession of continental mudflat deposits, exposed in the Aktau Mountains (Ili Basin, south-east Kazakhstan), has great potential as a terrestrial palaeoclimate archive. About 90 m of the 1700 m thick succession comprise alluvial mudflat deposits and appear as cyclic alternation of coarse sheet floods, mudflat fines and semi-arid hydromorphic soils. In this study, bulk-sediment mineralogy and geochemistry, magnetic susceptibility, sediment colour and palynology are used to reconstruct environmental conditions by determining changes and forcing mechanisms in the intensity of sediment discharge, weathering and pedogenesis. The results presented here indicate four major periods of arid soil formation and one palustrine interval characterized by higher evaporation rates under highly alkaline/saline conditions. A positive correlation between weathering indices and the Mg/Al ratio suggest that these horizons correspond to maximum rates of evapotranspiration and aridity. The formation of mudflat fines is, instead, interpreted as representing higher detrital sediment production by more intense alluvial fan activity during times of higher precipitation. Time series analysis of weathering indices, colour and magnetic susceptibility data yields cycle-to-frequency ratios with the potential to represent Milankovitch cyclicity with short and long eccentricity as dominant periodicities. Periods of pronounced aridity, paced by long eccentricity forcing, reflect changes in moisture availability. On longer tectonic timescales, the persistent appearance of gypsum indicates a shift towards more arid conditions. This trend in climate is considered to result from the closure of the eastern gateway of the Mediterranean to the Indian Ocean that restricted circulation and enhanced salinity within the Eastern Paratethys.
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Significance Statement 13Microbial lipid membranes protect and isolate a cell from its environment while regulating 14 the flow of energy and nutrients to metabolic reaction centers within. We demonstrate that 15 membrane lipids change as a function of energy flux using a well-studied archaeon that 16 thrives in acidic hot springs and observe an increase in membrane packing as energy 17 becomes more limited. These observations are consistent with chemostat experiments 18 utilizing a low temperature, neutral pH, marine archaeon. This strategy appears to regulate 19 membrane homeostasis is common across GDGT-producing lineages, demonstrating that 20 diverse taxa adjust membrane composition in response to chronic energy stress. 21 Summary 22 23 Microorganisms regulate the composition of their membranes in response to environmental 24 cues. Many archaea maintain the fluidity and permeability of their membranes by adjusting 25 the number of cyclic moieties within the cores of their glycerol dibiphytanyl glycerol 26 tetraether (GDGT) lipids. Cyclized GDGTs increase membrane packing and stability, which 27 has been shown to help cells survive shifts in temperature and pH. However, the extent of 28 this cyclization also varies with growth phase and electron acceptor or donor limitation. 29 These observations indicate a relationship between energy metabolism and membrane 30 composition. Here we show that the average degree of GDGT cyclization increases with 31 Zhou et al. 2019 20190817 2 doubling time in continuous cultures of the thermoacidophile Sulfolobus acidocaldarius 32 (DSM 639). This is consistent with the behavior of a mesoneutrophile, Nitrosopumilus 33 maritimus SCM1. Together, these results demonstrate that archaeal GDGT distributions can 34 shift in response to electron donor flux and energy availability, independent of pH or 35 temperature. Paleoenvironmental reconstructions based on GDGTs thus capture the energy 36 available to microbes, which encompasses fluctuations in temperature and pH, as well as 37 electron donor and acceptor availability. The ability of Archaea to adjust membrane 38 composition and packing may be an important strategy that enables survival during episodes 39 of energy stress. 40 41
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 Crenarchaeon Sulfolobus acidocaldarius DSM639 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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