Dataset Information

Evidence for contrasting roles of dimethylsulfoniopropionate production in Emiliania huxleyi and Thalassiosira oceanica.

ABSTRACT: Dimethylsulfoniopropionate (DMSP) is a globally abundant marine metabolite and a significant source of organic carbon and sulfur for marine microbial ecosystems with the potential to influence climate regulation. However, the physiological function of DMSP has remained enigmatic for >30 yr. Recent insight suggests that there are different physiological roles for DMSP based on the cellular DMSP concentrations in producers. Differential production of DMSP was tested with multiple physiological experiments that altered nitrate availability, salinity and temperature to create stressed growth and target different metabolic conditions in Emiliania huxleyi, a high DMSP producer and Thalassiosira oceanica, a low DMSP producer. Emiliania huxleyi intracellular DMSP did not respond to metabolically imbalanced conditions, while Thalassiosira oceanica intracellular DMSP was significantly correlated to stressed growth rate across all conditions tested and exhibited a plastic response on a timescale of hours in nonsteady-state. The previous assumption that proposed DMSP mechanism(s) can be universally applied to all producers is shown to be unlikely. Rather, two distinct ecological roles for DMSP likely exist that differ by producer type, where: (1) the primary role of DMSP in high producers is a constitutive compatible solute; and (2) DMSP production in low producers is a finely tuned stress response.

SUBMITTER: McParland EL

PROVIDER: S-EPMC7154784 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Evidence for contrasting roles of dimethylsulfoniopropionate production in Emiliania huxleyi and Thalassiosira oceanica.

McParland Erin L EL Wright Anna A Art Kristin K He Meagan M Levine Naomi M NM

The New phytologist 20200127 2

Dimethylsulfoniopropionate (DMSP) is a globally abundant marine metabolite and a significant source of organic carbon and sulfur for marine microbial ecosystems with the potential to influence climate regulation. However, the physiological function of DMSP has remained enigmatic for >30 yr. Recent insight suggests that there are different physiological roles for DMSP based on the cellular DMSP concentrations in producers. Differential production of DMSP was tested with multiple physiological exp ...[more]

PMID: 31850524

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Project description:The hydrogen isotope (2H/1H) ratio of lipids from phytoplankton is a powerful new tool for reconstructing hydroclimate variations in the geologic past from marine and lacustrine sediments. Water 2H/1H changes are reflected in lipid 2H/1H changes with R2 > 0.99, and salinity variations have been shown to cause about a 1‰ change in lipid ?2H values per unit (ppt) change in salinity. Less understood are the effects of growth rate, nutrient limitation and light on 2H/1H fractionation in phytoplankton. Here we present the first published study of growth rate effects on 2H/1H fractionation in the lipids of coccolithophorids grown in continuous cultures. Emiliania huxleyi was cultivated in steady state at four growth rates and the ?2H value of individual alkenones (C37:2, C37:3, C38:2, C38:3), fatty acids (C14:0, C16:0, C18:0), and 24-methyl cholest-5,22-dien-3?-ol (brassicasterol) were measured. 2H/1H fractionation increased in all lipids as growth rate increased by 24‰ to 79‰ (div d-1)-1. We attribute this response to a proportional increase in the fraction of NADPH from Photosystem I (PS1) of photosynthesis relative to NADPH from the cytosolic oxidative pentose phosphate (OPP) pathway in the synthesis of lipids as growth rate increases. A 3-endmember model is presented in which lipid hydrogen comes from NADPH produced in PS1, NADPH produced by OPP, and intracellular water. With published values or best estimates of the fractionation factors for these sources (?PS1 = 0.4, ?OPP = 0.75, and ?H2O = 0) and half of the hydrogen in a lipid derived from water the model indicates ?lipid = 0.79. This value is within the range measured for alkenones (?alkenone = 0.77 to 0.81) and fatty acids (?FA = 0.75 to 0.82) in the chemostat cultures, but is greater than the range for brassicasterol (?brassicasterol = 0.68 to 0.72). The latter is attributed to a greater proportion of hydrogen from NADPH relative to water in isoprenoid lipids. The model successfully explains the increase in 2H/1H fractionation in the sterol 24-methyl-cholesta-5,24(28)-dien-3?-ol from marine centric diatom T. pseudonana chemostat cultures as growth rate increases. Insensitivity of ?FA in those same cultures may be attributable to a larger fraction of hydrogen in fatty acids sourced from intracellular water at the expense of NADPH as growth rate increases. The high sensitivity of ? to growth rate in E. huxleyi lipids and a T. pseudonana sterol implies that any change in growth rate larger than ~0.15 div d-1 can cause a change in ?2Hlipid that is larger than the analytical error of the measurement (~5‰), and needs to be considered when interpreting ?2Hlipid variations in sediments.

Dataset Information

Evidence for contrasting roles of dimethylsulfoniopropionate production in Emiliania huxleyi and Thalassiosira oceanica.

Publications

Evidence for contrasting roles of dimethylsulfoniopropionate production in Emiliania huxleyi and Thalassiosira oceanica.

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