Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton

Although the principal source of marine organic matter is phytoplankton, experimental data on carbon and nitrogen mass balance during their growth cycle are lacking. Phytoplankton from diverse taxonomic groups (Synechococcus bacillaris, Phaeocystis sp., Emiliania huxleyi, Skeletonema costatum) were grown in synthetic seawater media, and changes in particulate and dissolved carbon, nitrogen, and carbohydrates were followed for 14 d. There was a close molar balance between dissolved inorganic carbon (DIC) uptake and total organic carbon (TOC) production in all phytoplankton except Emiliania, which synthesizes carbonate-containing coccoliths. Rates of dissolved organic carbon (DOC) production during phytoplankton growth ranged from 5 to 13 FM DOC d-l (O.Ol0.06 pmol DOC pM cell C-l d-l) and constituted a substantial (10-3256) fraction of TOC production. The carbohydrate content of both the particulate and dissolved pools increased over the growth cycle and constituted 1845% and 26-80% of TOC, respectively. The dissolved carbohydrate pool was predominantly composed of polysaccharides (70-94%). Despite some species-specific variability, phytoplankton cellular (particulate) and extracellular (dissolved) organic matter C: N ratios did not deviate far from Redfield values. However, phytoplankton synthesized compositionally distinct pools of high molecular weight dissolved organic matter (> 1,000 Da, average C : N ratio -21) and low molecular weight dissolved organic matter (< 1,000 Da, average C : N ratio -6.0). Most of the organic matter in the sea originates from phytoplankton production. Phytoplankton influence seawater composition by the uptake of inorganic carbon and nutrients for synthesis of cellular organic materials (Eppley and Peterson 1979) and exudation and loss of dissolved organic matter (Mague et al. 1980). The occurrence of phytoplankton blooms at sea have been observed to cause physicochemical changes in the seawater milieu through redistribution of inorganic macronutrients (McAllister et al. 1961) and synthesis and release of organic compounds (Jenkinson and Biddanda 1995). According to Redfield et al. (1963, p. 26), “the influence of organisms on the composition of seawater is profound, with elements being withdrawn from seawater by the growth of phytoplankton in the proportions required to synthesize protoplasm of specific composition and being returned to it as excretions and decomposition products of an equally specific nature.” The major portion of DOM released by phytoplankton in the sea consists of small molecules (low-molecular-weight dissolved organic matter [LMW DOM], < 1,000 Da; Jensen 1983; Lancelot 1984). Past studies demonstrate that 20-30% of oceanic DOM is high molecular weight (HMW, Carlson et al. 1985; Benner et al. 1992) and that this pool is carbohydrate rich (25-50%) relative to bulk DOM (Benner et al. Acknowledgments This work was supported by NSF grant OCE 9413843. We are thankful to Marisa Garza for helping with preliminary culture studies, Andy Biersmith for assistance with ultrafiltration, and Brenda Black for particulate organic carbon and nitrogen analyses. Ellery Ingall provided laboratory facilities for carrying out inorganic nitrogen analyses. The manuscript was improved by discussions with Andy Biersmith, Steve Opsahl, Annelie Skoog, and Sue Ziegler. This is contribution 891 of the University of Texas Marine Science Institute. 1992). During a diatom bloom in the northern Gulf of Mexico, Amon and Benner (1994) observed that -30% of DOM was of HMW and suggest that the HMW and LMW pools of DOM c,ycle in the ocean on quite different time scales. Kepkay et al. (1993), studying dissolved organic carbon (DOC) accumulation over the spring bloom in the Bedford Basin, have argued the necessity for establishing a direct link between the production of colloidal (HMW) DOM and phytoplankton as its source. Measurable accumulations of DOM have been observed to take place toward the end of phytoplankton blooms in the ocean (Barlow 1980; Carlson et al. 1994). Such seasonal accumulations of DOM are comparable to or exceed that of particulate organic matter (POM; Williams 1995). Because these accumulations of organic matter are clearly linked to seasonal phytoplankton growth events, there is interest in the composition of both the cellular and extracellular release products of’ phytoplankton. Parsons et al. (1961) carried out a detailed study of the chemical composition of 11 species of phytoplankton cells in culture during their exponential growth phase and found that cellular carbohydrate content ranged between 6 and 37% and the C : N ratios varied between 4.4 and 9.0. The release of DOM by phytoplankton is positively related to the photosynthetic rate (Anderson and Zeutschel 1970; Zoltnik and Dubinsky 1989). Some 5-30% of marine primary production is directly released as DOM by phytoplankton (Mague et al. 1980; Lancelot and Billen 1985; Bain’es and Pace 1991). The little that is known about the composition of dissolved materials produced by phytoplankton (see Hellebust 1974; Lancelot 1984) indicates it consists of all types of biochemical products including carbohydrates (mono, oligo, and polysaccharides), nitrogenous compounds (amino acids, proteins, and polypeptides), lipids (fatty acids), and organic acids (glycollate, tricarboxylic acids, hydroxamate, vitamins). Carbohydrates in the form of exopolymers are released in