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

Grayson M Boyer,Roger E Summons,Everett L Shock,Jade Woods,Florence Schubotz

doi:10.3389/fmicb.2020.00229

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 (ZC), a metric calculated from the chemical formulae of lipid structures. Carbon in intact polar lipids (IPLs) and their alkyl chains becomes more oxidized (higher ZC) 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 ZC) in the hot, reduced conditions upstream, with abundance-weighted ZC 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 ZC 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 ZC 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.

Highlights

There is ongoing interest in how geochemistry influences lipid compositions expressed in living communities of microorganisms
Upstream samples collected closest to the source pools of each spring ranged from circumneutral to alkaline, with temperatures close to the boiling point of water (82.2– 91.0◦C) given their altitude in Yellowstone National Park (YNP) (∼2,200 m above sea level at Bison Pool and Mound Spring, 2,250 m at Octopus Spring, and 2,300 m at Empress Pool)
A study by Meyer-Dombard et al (2011) found the bulk of the bacterial community in the pink streamers of Bison Pool belonged to Aquificales and Thermatogales, while most archaea were mainly comprised of Crenarchaeota and Desulfurococcales

Summary

Introduction

There is ongoing interest in how geochemistry influences lipid compositions expressed in living communities of microorganisms. Interpreting lipid biomarkers can be challenging because they are often not specific to any single type of organism or set of geochemical conditions (Rashby et al, 2007; Pitcher et al, 2009; French et al, 2015). For this reason, it is useful to investigate how bulk lipid compositions change across a variety of natural systems and look for patterns that are universally applicable. Changes in lipid structures and compositions along these gradients likely reflect adaptation to the collective set of environmental conditions experienced by the microorganisms present

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