Carbon Oxidation State in Microbial Polar Lipids Suggests Adaptation to Hot Spring Temperature and Redox Gradients

Abstract

The influence of oxidation-reduction (redox) potential on the expression of biomolecules is a topic of ongoing exploration in geobiology. In this study, we investigate the novel possibility that structures and compositions of lipids produced by microbial communities are sensitive to environmental redox conditions. We extracted lipids from microbial biomass collected along the thermal and redox gradients of four alkaline hot springs in Yellowstone National Park (YNP) and investigated patterns in the average oxidation state of carbon (Z C ), a metric calculated from the chemical formulae of lipid structures. Carbon in intact polar lipids (IPLs) and their alkyl chains becomes more oxidized (higher Z C ) with increasing distance from each of the four hot spring sources. This coincides with decreased water temperature and increased concentrations of oxidized inorganic solutes, such as dissolved oxygen, sulfate, and nitrate. Carbon in IPLs is most reduced (lowest Z C ) in the hot, reduced conditions upstream, with abundance-weighted Z C values between −1.68 and −1.56. These values increase gradually downstream to around −1.36 to −1.33 in microbial communities living between 29.0 and 38.1 • C. This near-linear increase in Z C can be attributed to a shift from ether-linked to ester-linked alkyl chains, a decrease in average aliphatic carbons per chain (nC), an increase in average degree of unsaturation per chain (nUnsat), and increased cyclization in tetraether lipids. The Z C of lipid headgroups and backbones did not change significantly downstream. Expression of lipids with relatively reduced carbon under reduced conditions and oxidized lipids under oxidized conditions may indicate microbial adaptation across environmental gradients in temperature and electron donor/acceptor supply.

Multiple environmental parameters impact core lipid cyclization in Sulfolobus acidocaldarius

“…We further examine, for the first time, the impact of agitation on GDGT cyclization. Higher temperatures yielded higher average cyclization, which is consistent with most experimental studies of both Thaum- and Crenarchaeota (9–12, 24, 25), yet opposes recent environmental findings in alkaline hotsprings (26). When pH deviated from the optimum pH of ∼3 for DSM639, cyclization decreased.…”

Uncovering chemical signatures of salinity gradients through compositional analysis of protein sequences

“…1 m deep hypersaline, oxygenated water (approximately 200 mM O 2 ), but in the mat, oxygen rises during the daytime and is depleted within a few millimeters, giving way to anoxic, then sulfidic conditions (Ley et al, 2006 Using metagenomic data for these redox gradients (Kunin et al, 2008;Havig et al, 2011;Swingley et al, 2012;Reveillaud et al, 2016;Fortunato et al, 2018), Dick et al (2019) showed that the carbon oxidation states of DNA, messenger RNA, and proteins increase down the outflow channel of Bison Pool and between fluids from diffuse hydrothermal vents and relatively oxidizing seawater. Notably, intact polar lipids extracted from the microbial communities of Bison Pool and other alkaline hot springs also exhibit downstream increases in carbon oxidation state (Boyer et al, 2020), confirming that similar trends characterize multiple classes of biomolecules. The Z C of proteins increases more subtly toward the surface in the upper few millimeters of the Guerrero Negro microbial mat; it also increases at greater depths, perhaps due to heterotrophic degradation and/or horizontal gene transfer (Dick et al, 2019).…”

Butyrate Conversion by Sulfate-Reducing and Methanogenic Communities from Anoxic Sediments of Aarhus Bay, Denmark

“…The high abundance of SRB at the end of the slurry incubations and the positive correlation between PE IPLs and high-sulfate condition ( Figure S8) might indicate that the occurrence of PE can be linked to the presence of SRB in enrichment slurries. The presence of trimethylornithine (TMO) IPLs in three butyrate-amended slurries from the methane zone ( Figure S7, Table S4) was surprising since these lipids were originally identified in planctomycete isolates from ombrotrophic northern wetlands [49], and later observed in northern wetland peat [50], meso-oligotrophic lakes of Minnesota and Iowa [51], and Yellow Stone National Park hot spring microbial communities [52]. No planctomycete phylotypes were detected in any of the butyrate-amended methane zone-derived slurries, indicating that the observed TMOs were produced by other microbial groups or the relative abundance of planctomycete phylotypes was very low.…”