Abstract
Isoprenoidal glycerol dialkyl glycerol tetraethers (iGDGTs) are core membrane lipids of many archaea that enhance the integrity of cytoplasmic membranes in extreme environments. We examined the iGDGT profiles and corresponding aqueous geochemistry in 40 hot spring sediment and microbial mat samples from the U.S. Great Basin with temperatures ranging from 31 to 95°C and pH ranging from 6.8 to 10.7. The absolute abundance of iGDGTs correlated negatively with pH and positively with temperature. High lipid concentrations, distinct lipid profiles, and a strong relationship between polar and core lipids in hot spring samples suggested in situ production of most iGDGTs rather than contamination from local soils. Two-way cluster analysis and non-metric multidimensional scaling (NMS) of polar iGDGTs indicated that the relative abundance of individual lipids was most strongly related to temperature (r2 = 0.546), with moderate correlations with pH (r2 = 0.359), nitrite (r2 = 0.286), oxygen (r2 = 0.259), and nitrate (r2 = 0.215). Relative abundance profiles of individual polar iGDGTs indicated potential temperature optima for iGDGT-0 (≤70°C), iGDGT-3 (≥55°C), and iGDGT-4 (≥60°C). These relationships likely reflect both physiological adaptations and community-level population shifts in response to temperature differences, such as a shift from cooler samples with more abundant methanogens to higher-temperature samples with more abundant Crenarchaeota. Crenarchaeol was widely distributed across the temperature gradient, which is consistent with other reports of abundant crenarchaeol in Great Basin hot springs and suggests a wide distribution for thermophilic ammonia-oxidizing archaea (AOA).
Highlights
The cellular membranes of many archaea have a monolayer architecture comprised of membrane-spanning lipids composed of isoprenoidal chains joined by four ether bonds to two glycerol backbones, known as isoprenoidal GDGTs
Forty hot spring sediment and microbial mat samples were collected from eight different U.S Great Basin locations, with temperatures ranging from 31 to 95◦C and pH values from 6.8 to 10.7 (Table 1)
The absolute abundance of both polar and core isoprenoidal GDGTs (iGDGTs) was negatively correlated with pH; core iGDGT abundance was positively correlated with temperature (Figure 2)
Summary
The cellular membranes of many archaea have a monolayer architecture comprised of membrane-spanning lipids composed of isoprenoidal chains joined by four ether bonds to two glycerol backbones, known as isoprenoidal GDGTs (iGDGTs; Figure S1) (van de Vossenberg et al, 1998; Schouten et al, 2000). Archaea that produce iGDGTs include thermophilic and hyperthermophilic Thermoprotei (Crenarchaeota), Thaumarchaeota, and at least eight orders of Euryarchaeota including methanogens, thermoacidophiles, and other thermophilic Euryarchaeota (reviewed in Schouten et al, 2013; Pearson and Ingalls, 2013). Some iGDGTs are synthesized by non-extremophilic archaea, crenarchaeol-producing Thaumarchaeota (Sinninghe Damsté et al, 2002; Könneke et al, 2005), the importance of membrane-spanning lipids to life at high temperature and low pH has been supported by a large body of research. Several pure culture studies, including Crenarchaeota, Euryarchaeota, and Thaumarchaeota, have shown that archaea increase the number of alkyl group cyclopentane rings, ranging from 0 to 8 per iGDGT, in response to growth temperature increase or pH decrease (Gliozzi et al, 1983; reviewed in De Rosa et al, 1980; Chong, 2010). Molecular modeling studies have shown that increased cyclization stabilizes membranes by tightening membrane packing in the hydrophobic core and by strengthening hydrogen bonding at the membrane surface [reviewed in Chong (2010)]
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