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

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Carbon Oxidation State in Microbial Polar Lipids Suggests Adaptation to Hot Spring Temperature and Redox Gradients Carbon oxidation state in microbial polar lipids suggests adaptation to hot spring temperature and redox gradients The MIT Faculty has made this article openly available. Please share how this access benefits you. Your story matters. Citation Boyer, Grayson M., Florence Schubotz, Roger E. Summons, Jade Woods, and Everett L. Shock, "Carbon oxidation state in microbial polar lipids suggests adaptation to hot spring temperature and redox gradients." Frontiers in microbiology 11 (2020): no. 229 doi 10.3389/fmicb.2020.00229 ©2020 Author(s) As Published 10.3389/fmicb.2020.00229 Publisher Frontiers Media SA Version Final published version Citable link https://hdl.handle.net/1721.1/124728 Terms of Use Creative Commons Attribution 4.0 International license Detailed Terms https://creativecommons.org/licenses/by/4.0/ ORIGINAL RESEARCH published: 20 February 2020 doi: 10.3389/fmicb.2020.00229 Carbon Oxidation State in Microbial Polar Lipids Suggests Adaptation to Hot Spring Temperature and Redox Gradients Grayson M. Boyer 1*, Florence Schubotz 2, Roger E. Summons 3, Jade Woods 4 and Everett L. Shock 1,5 1 School of Earth and Space Exploration, Arizona State University, Tempe, AZ, United States, 2 MARUM and Department of Geosciences, University of Bremen, Bremen, Germany, 3 Department of Earth, Atmospheric and Planetary Science, Massachusetts Institute of Technology, Cambridge, MA, United States, 4 Department of Chemistry, University of Nebraska-Lincoln, Lincoln, NE, United States, 5 School of Molecular Sciences, Arizona State University, Tempe, AZ, United States 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 Edited by: Akihiko Yamagishi, state of carbon (ZC), a metric calculated from the chemical formulae of lipid structures. Tokyo University of Pharmacy and Life Carbon in intact polar lipids (IPLs) and their alkyl chains becomes more oxidized (higher Sciences, Japan ZC) with increasing distance from each of the four hot spring sources. This coincides Reviewed by: with decreased water temperature and increased concentrations of oxidized inorganic Jeremy Dodsworth, The California State University, solutes, such as dissolved oxygen, sulfate, and nitrate. Carbon in IPLs is most reduced United States (lowest ZC) in the hot, reduced conditions upstream, with abundance-weighted ZC Zackary J. Jay, Montana State University, values between −1.68 and −1.56. These values increase gradually downstream to United States around −1.36 to −1.33 in microbial communities living between 29.0 and 38.1◦C. This *Correspondence: near-linear increase in ZC can be attributed to a shift from ether-linked to ester-linked alkyl Grayson M. Boyer chains, a decrease in average aliphatic carbons per chain (nC), an increase in average [email protected] degree of unsaturation per chain (nUnsat), and increased cyclization in tetraether lipids. Specialty section: The ZC of lipid headgroups and backbones did not change significantly downstream. This article was submitted to Expression of lipids with relatively reduced carbon under reduced conditions and oxidized Extreme Microbiology, a section of the journal lipids under oxidized conditions may indicate microbial adaptation across environmental Frontiers in Microbiology gradients in temperature and electron donor/acceptor supply. Received: 05 May 2019 Accepted: 31 January 2020 Keywords: geobiochemistry, intact polar lipid, redox gradient, hydrothermal system, microbial community, carbon Published: 20 February 2020 oxidation state Citation: Boyer GM, Schubotz F, Summons RE, 1. INTRODUCTION Woods J and Shock EL (2020) Carbon Oxidation State in Microbial Polar Lipids Suggests Adaptation to There is ongoing interest in how geochemistry influences lipid compositions expressed in living Hot Spring Temperature and Redox communities of microorganisms. Lipids can provide valuable information about the environmental Gradients. Front. Microbiol. 11:229. conditions experienced by the microbes that produced them (Summons and Walter, 1990; Pearson doi: 10.3389/fmicb.2020.00229 and Ingalls, 2013; Schouten et al., 2013). Structural diversity, longevity, and potential traceability Frontiers in Microbiology | www.frontiersin.org 1 February 2020 | Volume 11 | Article 229 Boyer et al. Carbon Oxidation State in Polar Lipids have led to the extensive use of lipids in biogeoscience as we calculated the ZC of lipid headgroups, backbones, and alkyl biomarkers (Summons et al., 1999; Brocks and Pearson, 2005; chains to better understand how these components influence Schouten et al., 2007a). However, interpreting lipid biomarkers changes in the ZC of IPLs. These ZC values could then be can be challenging because they are often not specific to any correlated with the temperature, chemical composition, and single type of organism or set of geochemical conditions (Rashby redox state of the surrounding environment. We hypothesized et al., 2007; Pitcher et al., 2009; French et al., 2015). For this that lipids sampled closest to the hot, reduced source of each reason, it is useful to investigate how bulk lipid compositions spring would have the most reduced carbon on average, while change across a variety of natural systems and then look for the cool, oxidized conditions downstream would be characterized patterns that are universally applicable. by lipids with more oxidized carbon. This general pattern aligns Hot spring outflow channels provide particularly accessible with observations of amino acid compositions inferred from locations for studying changes in lipid composition across strong metagenomes along the outflow channel of Bison Pool (Dick and temperature and chemical gradients. For instance, microbial Shock, 2011, 2013), and the strong correlations found between communities in the submerged sediments and biofilms of the ZC of metagenomes and metatranscriptomes across natural boiling springs tend to express lipid compositions substantially redox gradients in a variety of microbial mats, terrestrial and different from those in a hot spring photosynthetic microbial marine hydrothermal systems, and hypersaline lakes (Dick et al., mat downstream (Zeng et al., 1992; Schubotz et al., 2013). It 2019). If compositions of microbial lipids display similar trends is conceivable that temperature is not the only environmental across a variety of natural systems, patterns in ZC preserved in stress governing distributions of lipid structural adaptations lipid biomarkers could potentially present a tantalizing target for along a hot spring outflow channel. As is often the case inferring paleoredox. in hydrothermal systems, temperature gradients coincide with gradients in water chemistry, such as pH, salinity, solute 2. METHODS concentrations, and redox potential. Changes in lipid structures and compositions along these gradients likely reflect adaptation 2.1. Water Chemistry to the collective set of environmental conditions experienced by Temperature, conductivity, and pH were measured in the field the microorganisms present. as close to sampling locations as possible and before sample Our goal was to identify patterns in the properties of microbial collection. Temperature and conductivity were measured with lipids that might be influenced by redox geochemistry. We a YSI model 30 meter. Sample pH was measured with a decided to explore the average oxidation state of carbon (ZC) WTW brand 3300i or 3110 model pH meter with WTW in lipids. In general, lower values of ZC in a molecule represent probe calibrated daily with pH 4, 7, and 10 buffer solutions at more reduced carbon (e.g., −4 in CH4) while higher values ambient temperature. Concentrations of dissolved oxygen and indicate more oxidized carbon (e.g., +4 in CO2). ZC was total sulfide were obtained from unfiltered water samples in the chosen as a metric primarily because thermodynamic or kinetic field using a Hach 2400 or 2800 portable spectrophotometer relationships with redox potential have been implicated in a with Hach reagents and protocols. Water samples collected variety of natural processes. Examples include the predicted for laboratory analyses were filtered in the field with SuporTM energetic favorability of amino acids biosynthesis in submarine (Pall Corporation) 0.2 µm polyethersulfone (PES) syringe filters hydrothermal vents (Amend and Shock, 1998), preservation and into 30 mL HDPE Nalgene bottles and stored at −20◦C. degradation of organic matter in sediments and soils (Likens, Concentrations of total ammonium, nitrate, nitrite, and sulfate 2010; LaRowe and Van Cappellen, 2011; Boye et al., 2017), were obtained by ion chromatography on two Dionex DX-600 oxidation rates of atmospheric organic aerosols (Kroll et al., 2011, systems; one for the analysis of cations and the other for anions. 2015), and evolutionary convergence on proteomes inferred from Suppressor columns on both systems were regenerated with metagenomes of microbial communities in natural systems (Dick deionized water to improve the signal-to-noise ratio. The anion and Shock, 2011, 2013; Dick, 2014; Dick et al., 2019; Fones analysis system was equipped with a potassium hydroxide eluent
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