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The generation of hydrogen and reduced carbon compounds during serpentinization provides sustained energy for microorganisms on Earth, and possibly on other extraterrestrial bodies (e.g., Mars, icy satellites). However, the geochemical conditions that arise from water-rock reaction also challenge the known limits of microbial physiology, such as hyperalkaline pH, limited electron acceptors and inorganic carbon. Because cell membranes act as a primary barrier between a cell and its environment, lipids are a vital component in microbial acclimation to challenging physicochemical conditions. To probe the diversity of cell membrane lipids produced in serpentinizing settings and identify membrane adaptations to this environment, we conducted the first comprehensive intact polar lipid (IPL) biomarker survey of microbial communities inhabiting the subsurface at a terrestrial site of serpentinization. We used an expansive, custom environmental lipid database that expands the application of targeted and untargeted lipodomics in the study of microbial and biogeochemical processes. IPLs extracted from serpentinite-hosted fluid communities were comprised of >90% isoprenoidal and non-isoprenoidal diether glycolipids likely produced by archaeal methanogens and sulfate-reducing bacteria. Phospholipids only constituted ~1% of the intact polar lipidome. In addition to abundant diether glycolipids, betaine and trimethylated-ornithine aminolipids and glycosphingolipids were also detected, indicating pervasive membrane modifications in response to phosphate limitation. The carbon oxidation state of IPL backbones was positively correlated with the reduction potential of fluids, which may signify an energy conservation strategy for lipid synthesis. Together, these data suggest microorganisms inhabiting serpentinites possess a unique combination of membrane adaptations that allow for their survival in polyextreme environments. The persistence of IPLs in fluids beyond the presence of their source organisms, as indicated by 16S rRNA genes and transcripts, is promising for the detection of extinct life in serpentinizing settings through lipid biomarker signatures. These data contribute new insights into the complexity of lipid structures generated in actively serpentinizing environments and provide valuable context to aid in the reconstruction of past microbial activity from fossil lipid records of terrestrial serpentinites and the search for biosignatures elsewhere in our solar system.
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Lipid remodeling in phytoplankton exposed to multi-environmental drivers in a mesocosm experiment
Abstract. Lipid remodeling, the modification of cell membrane chemistry via structural rearrangements within the lipid pool of an organism, is a common physiological response amongst all domains of life to alleviate environmental stress and maintain cellular homeostasis. Whereas culture experiments and environmental studies of phytoplankton have demonstrated the plasticity of lipids in response to specific abiotic stressors, few analyses have explored the impacts of multi-environmental stressors at the community-level scale. Here, we study changes in the pool of intact polar lipids (IPLs) of a phytoplanktonic community exposed to multi-environmental stressors during a ∼ 2-month-long mesocosm experiment deployed in the eastern tropical South Pacific off the coast of Callao, Peru. We investigate lipid remodeling of IPLs in response to changing nutrient stoichiometries, temperature, pH, and light availability in surface and subsurface water masses with contrasting redox potentials, using multiple linear regressions, classification and regression trees, and random forest analyses. We observe proportional increases in certain glycolipids (namely mono- and diglycosyldiacylglycerol – MGDG and DGDG, respectively) associated with higher temperatures and oxic conditions, consistent with previous observations of their utility to compensate for thermal stress and their degradation under oxygen stress. N-bearing (i.e., betaine lipids and phosphatidylethanolamine – BLs and PE) and non-N-bearing (i.e., MGDG; phosphatidylglycerol, PG; and sulfoquinovosyldiacylglycerol, SQDG) IPLs are anti-correlated and have strong positive correlations with nitrogen-replete and nitrogen-depleted conditions, respectively, which suggests a substitution mechanism for N-bearing IPLs under nitrogen limitation. Reduced CO2(aq) availability and increased pH levels are associated with greater proportions of DGDG and SQDG IPLs, possibly in response to the lower concentration of CO2(aq) and the overall lower availability of inorganic carbon for fixation. A higher production of MGDG in surface waters corresponds well with its established photoprotective and antioxidant mechanisms in thylakoid membranes. The observed statistical relationships between IPL distributions, physicochemical parameters, and the composition of the phytoplankton community suggest evidence of lipid remodeling in response to environmental stressors. These physiological responses may allow phytoplankton to reallocate resources from structural or extrachloroplastic membrane lipids (i.e., phospholipids and betaine lipids) under high-growth conditions to thylakoid and/or plastid membrane lipids (i.e., glycolipids and certain phosphatidylglycerols) under growth-limiting conditions. Further investigation of the exact mechanisms controlling the observed trends in lipid distributions is necessary to better understand how membrane reorganization under multi-environmental stressors can affect the pools of cellular C, N, P, and S, as well as their fluxes to higher trophic levels in marine environments subjected to increasing environmental pressure. Our results suggest that future studies addressing the biogeochemical consequences of climate change in the eastern tropical South Pacific Ocean must take into consideration the impacts of lipid remodeling in phytoplankton.
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- Award ID(s):
- 2047057
- PAR ID:
- 10591239
- Publisher / Repository:
- Copernicus Publications
- Date Published:
- Journal Name:
- Biogeosciences
- Volume:
- 21
- Issue:
- 17
- ISSN:
- 1726-4189
- Page Range / eLocation ID:
- 3927 to 3958
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.5194/bg-21-3927-2024
