An official website of the United States government
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.
more »
« less
Mechanistic constraints on the trade-off between photosynthesis and respiration in response to warming
Phytoplankton are responsible for half of all oxygen production and drive the ocean carbon cycle. Metabolic theory predicts that increasing global temperatures will cause phytoplankton to become more heterotrophic and smaller. Here, we uncover the metabolic trade-offs between cellular space, energy, and stress management driving phytoplankton thermal acclimation and how these might be overcome through evolutionary adaptation. We show that the observed relationships between traits such as chlorophyll, lipid content, C:N, and size can be predicted on the basis of the metabolic demands of the cell, the thermal dependency of transporters, and changes in membrane lipids. We suggest that many of the observed relationships are not fixed physiological constraints but rather can be altered through adaptation. For example, the evolution of lipid metabolism can favor larger cells with higher lipid content to mitigate oxidative stress. These results have implications for rates of carbon sequestration and export in a warmer ocean.
more »
« less
- Award ID(s):
- 2044852
- PAR ID:
- 10498055
- Publisher / Repository:
- AAAS
- Date Published:
- Journal Name:
- Science Advances
- Volume:
- 9
- Issue:
- 35
- ISSN:
- 2375-2548
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Summary Emiliania huxleyiis a calcifying haptophyte, contributing to both the organic and inorganic marine carbon cycles. In marine ecosystems, light is a major driver of phytoplankton physiology and ultimately carbon flow through the ecosystem. Here, we analysed a Lagrangian time‐series of metatranscriptomes collected in the North Pacific Subtropical Gyre (NPSG) to examine howin situpopulations ofE.huxleyimodulate gene expression over day–night transitions. ManyE.huxleyicontigs had a diel expression pattern, with 61% of contigs clustering into modules with statistically significant diel periodicity. Contigs involved in processes that build up energy stores, like carbon fixation and lipid synthesis, peaked around dawn. In contrast, contigs involved in processes that released energy stores, like respiration and lipid degradation, peaked mid‐day and towards dusk. These patterns suggest an orchestrated cycle of building, then consuming energy stores inE.huxleyipopulations in the NPSG. Selected contigs related to the cell cycle also exhibited significant diel periodicity consistent with phased modulations of division observed in culture. Overall, these patterns of gene expression suggest a daily metabolic cascade that could contribute to both organic and inorganic carbon flow in this nutrient depleted ecosystem.more » « less
-
The CO2 content of Earth's atmosphere is rapidly increasing due to human consumption of fossil fuels. Models based on short-term culture experiments predict that major changes will occur in marine phytoplankton communities in the future ocean, but these models rarely consider how the evolutionary potential of phytoplankton or interactions within marine microbial communities may influence these changes. Here we experimentally evolved representatives of four phytoplankton functional types (silicifiers, calcifiers, coastal cyanobacteria, and oligotrophic cyanobacteria) in co-culture with a heterotrophic bacterium, Alteromonas, under either present-day or predicted future pCO2 conditions. The data and analysis code in this dataset show that the genomes of all four phytoplankton as well as Alteromonas evolved over the course of the experiment. Mutations in oxidative stress related genes (PTOX and thioredoxin reductase) were ubiquitous in evolved cultures of Prochlorococcus, suggesting adaptation in response to the well-studied deficiencies of this genus in terms of stress resistance in culture. With the exception of Prochlorococcus, most phytoplankton genomes appeared to experience mostly purifying selection, but Alteromonas genomes showed strong evidence of directional selection, particularly in co-culture with eukaryotic phytoplankton. Metabolic pathways were under intense selection for Alteromonas, and in particular adaptation to co-culture with eukaryotes appeared to select for a shift from growth on organic acids using an abbreviated TCA cycle to growth on more complex substrates using the complete TCA cycle. This work provides new insights on how phytoplankton will respond to anthropogenic change and on the evolutionary mechanisms governing the structure and function of marine microbial communities.more » « less
-
We describe considerations and strategies for developing a nuclear magnetic resonance (NMR) sample preparation method to extract low molecular weight metabolites from high‐salt spent media in a model coculture system of phytoplankton and marine bacteria. Phytoplankton perform half the carbon fixation and oxygen generation on Earth. A substantial fraction of fixed carbon becomes part of a metabolite pool of small molecules known as dissolved organic matter (DOM), which are taken up by marine bacteria proximate to phytoplankton. There is an urgent need to elucidate these metabolic exchanges due to widespread anthropogenic transformations on the chemical, phenotypic, and species composition of seawater. These changes are increasing water temperature and the amount of CO2absorbed by the ocean at energetic costs to marine microorganisms. Little is known about the metabolite‐mediated, structured interactions occurring between phytoplankton and associated marine bacteria, in part because of challenges in studying high‐salt solutions on various analytical platforms. NMR analysis is problematic due to the high‐salt content of both natural seawater and culture media for marine microbes. High‐salt concentration degrades the performance of the radio frequency coil, reduces the efficiency of some pulse sequences, limits signal‐to‐noise, and prolongs experimental time. The method described herein can reproducibly extract low molecular weight DOM from small‐volume, high‐salt cultures. It is a promising tool for elucidating metabolic flux between marine microorganisms and facilitates genetic screens of mutant microorganisms.more » « less
-
This dataset includes data from the nutrient amendment experiments. In these experiments, tracer additions (14C, 32Si) were used to quantify the level of Si, N, and Fe stress being experienced by the phytoplankton and to contextualize taxa-specific metatranscriptome responses for resolving gene expression profiles in the in situ communities. Seawater samples were collected on EXPORTS cruise DY131 during May 2021. This research focuses on the vertical export of the carbon associated with a major group of phytoplankton, the diatoms in the North Atlantic near the Porcupine Abyssal Plain. The major objective is to understand how diatom community composition and the prevailing nutrient conditions create taxonomic differences in metabolic state that combine to direct diatom taxa to different carbon export pathways. The focus is on diatoms, given their large contribution to global marine primary productivity and carbon export which translates into a significant contribution to the biogeochemical cycling of carbon (C), nitrogen (N), phosphorus (P), iron (Fe) and silicon (Si). It is hypothesized that the type and degree of diatom physiological stress are vital aspects of ecosystem state that drive export. To test this hypothesis, combined investigator expertise in phytoplankton physiology, genomics, and trace element chemistry is used to assess the rates of nutrient use and the genetic composition and response of diatom communities, with measurements of silicon and iron stress to evaluate stress as a predictor of the path of diatom carbon export. The EXPORTS field campaign in the North Atlantic sampled a retentive eddy over nearly a month. At the beginning of the cruise, nitrate was abundant while silicic acid was nearly undetectable. Such low dissolved Si concentrations significantly limit diatom silicification resulting in diatoms with reduced mineral ballast and low Si:C and Si:N ratios that would reduce sinking rates and competition for Si can alter diatom taxonomic composition. Both factors can the path cells follow through the food web ultimately altering diatom carbon export. Within each ecosystem state examined in the EXPORTS program, nutrient biogeochemistry, diatom and phytoplankton community structure, and global diatom gene expression patterns (metatranscriptomics) are characterized in the ocean. Nutrient amendment experiments with tracer addition (14C, 32Si) are used to quantify the level of Si, N, and Fe stress being experienced by the phytoplankton and to contextualize taxa-specific metatranscriptome responses for resolving gene expression profiles in the in situ communities.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1126/sciadv.adh8043
