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Elemental and macromolecular composition of the marine Chloropicophyceae, a major group of oceanic photosynthetic picoeukaryotes
Corresponding Author
Vinitha Ebenezer
Department of Oceanography, Dalhousie University, Halifax, Nova Scotia, Canada
Correspondence: [email protected]
Search for more papers by this authorYingyu Hu
Department of Oceanography, Dalhousie University, Halifax, Nova Scotia, Canada
Search for more papers by this authorOlga Carnicer
Department of Mathematics and Statistics, Dalhousie University, Halifax, Nova Scotia, Canada
Search for more papers by this authorAndrew J. Irwin
Department of Earth, Atmospheric and Planetary Science, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA
Search for more papers by this authorZoe V. Finkel
Department of Oceanography, Dalhousie University, Halifax, Nova Scotia, Canada
Search for more papers by this authorCorresponding Author
Vinitha Ebenezer
Department of Oceanography, Dalhousie University, Halifax, Nova Scotia, Canada
Correspondence: [email protected]
Search for more papers by this authorYingyu Hu
Department of Oceanography, Dalhousie University, Halifax, Nova Scotia, Canada
Search for more papers by this authorOlga Carnicer
Department of Mathematics and Statistics, Dalhousie University, Halifax, Nova Scotia, Canada
Search for more papers by this authorAndrew J. Irwin
Department of Earth, Atmospheric and Planetary Science, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA
Search for more papers by this authorZoe V. Finkel
Department of Oceanography, Dalhousie University, Halifax, Nova Scotia, Canada
Search for more papers by this authorAuthor Contribution Statement: V.E., Y.Y.H., A.I., and Z.F. contributed to the conceptualization and experimental design of the work. V.E. and O.C. contributed to sample collection. V.E. and Y.Y.H. performed all biochemical analyses. V.E. wrote the first manuscript draft. A.I. contributed to data analysis. Z.F., A.I., M.J.F., Y.Y.H., and O.C. contributed to the writing and revisions. All authors read and approved the submitted version.
Editor-in-Chief: K. David Hambright
Abstract
Chloropicophyceae (Prasinophyte Clade VII) are small nonmotile coccoid cells with cell diameters ranging from 1 to 3 μm. Molecular surveys indicate they are relatively high in abundance in moderately oligotrophic oceanic waters and may substantively contribute to biogeochemical cycling in the sea. Here, we quantify the elemental and macromolecular composition of three subtropical Chloropicophyceae strains: Chloropicon mariensis, Chloropicon maureeniae, and Chloropicon roscoffensis under nutrient-sufficient exponential growth and nitrate starvation. Under nutrient-sufficient conditions the Chloropicophyceae are high in C : N and quite low in C : P and N : P relative to the canonical Redfield ratio, reflecting their relatively high nucleic acid composition compared to many other phytoplankton taxa. Nitrate starvation causes increases in C : N and C : P and decreases in N : P, primarily due to increases in carbohydrate and lipid and decreases in protein and RNA. There is genetic evidence that unlike most other green algae, Chloropicophyceae are diploid. The high nucleic acid content in the Chloropicon is consistent with the hypothesis that the nucleus, as a nonscalable component, takes up a larger and substantial proportion of cell mass in diploid picoeukaryotes. The elemental and macromolecular composition of these Chloropicophyceae, and relatively homeostatic response to N-starvation compared to diatoms, provides some insight into their success in the moderately oligotrophic ocean.
Conflict of interest
None declared.
Supporting Information
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lno12013-sup-0001-supinfo.pdfPDF document, 464.4 KB | Fig. S1 Experimental set-up. Cultures were maintained in triplicate bottles in nutrient-replete media (filled symbols) and kept in exponential growth using semi-continuous batch technique (4 d before the initiation of the N-starvation treatment shown) and then transferred into nitrogen (N)-free media (open circles) and sampled 0, 7, 9, 12, and 15 d after the initiation of the N-starvation treatment. The figure shows the growth curve of Chloropicon mariensis under N-replete and N-starvation conditions in triplicate bottles. Error bars represent 1 SD. Fig. S2. Experimental conditions: (a) Growth rate estimated from the change in cell density over the nitrogen starvation treatment (μ, d−1), (b) bacterial density (cells mL−1), (c) pH, (d) dissolved inorganic phosphorus ([DIP], μM), and (e) dissolved inorganic nitrogen concentration ([DIN], μM) over the course of the treatment. Sample size, error bars and symbols as described in Fig. 1. Fig. S3. Percent retention of (a) Chloropicon cells, (b) chlorophyll a, and (c) bacteria, on various filter types. The horizontal axis indicates the pore size of polycarbonate filters (1.2–0.22 μm) or GF/F filters used. Fig. S4. Mass ratio of intracellular phosphorus (IP) to total particulate phosphorus (TPP). Error bars and symbols as described in Fig. 1. Fig. S5. Macromolecular content (pg macromolecule cell−1) as a function of N-starvation. (a–c) protein (black circles), carbohydrate (grey circles), lipid (open grey triangles). (d–f) RNA (blue open circles), DNA (pink triangles). (g–i) Chlorophyll a (green squares), polyP (dark yellow open inverted triangles), lipid-P (orange diamonds). Sample size, error bars, and symbols as described in Fig. 1. Table S1. Statistical analyses of C : N : P for Chloropicon mariensis, Chloropicon maureeniae, and Chloropicon roscoffensis under resource-replete exponential growth (Day 0) and after 12 d in N-free media (N-Starved). The mean and 95% confidence interval for elemental ratios were computed on the log scale and transformed back for display in the table. Ratios that can be distinguished between species (ANOVA, pairwise t-test, corrected p < 0.05) are indicated with different letters (A, B) in the AOV column. Table S2. Cell volume, C : N, C : P, N : P under resource sufficient conditions in Chloropicon (this study) and other marine phytoplankton documented in (1) Liefer et al. (2019) and (2) Garcia et al. (2018) (± SD, N = 3) Table S3. Macromolecular content (in pg cell−1) of the Chloropicophyceae under N-replete conditions (Day 0) and after 12 d of N-starvation, (± SD, N = 3). Table S4. The percentage of total cellular C, N, and intracellular P accounted for by the macromolecules measured under N-replete conditions (Day 0) and after 12 d of N-starvation (± SD, N = 3). |
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