The Macromolecular Basis of Phytoplankton C:N:P Under Nitrogen Starvation

Abstract

Biogeochemical cycles in the ocean are strongly affected by the elemental stoichiometry (C:N:P) of phytoplankton, which largely reflects their macromolecular content. A greater understanding of how this macromolecular content varies among phytoplankton taxa and with resource limitation may strengthen physiological and biogeochemical modeling efforts. We determined the macromolecular basis (protein, carbohydrate, lipid, nucleic acids, pigments) of C:N:P in diatoms and prasinophytes, two globally important phytoplankton taxa, in response to N starvation. Despite their differing cell sizes and evolutionary histories, the relative decline in protein during N starvation was similar in all four species studied and largely determined variations in N content. The accumulation of carbohydrate and lipid dominated the increase in C content and C:N in all species during N starvation, but these processes differed greatly between diatoms and prasinophytes. Diatoms displayed far greater accumulation of carbohydrate with N starvation, possibly due to their greater cell size and storage capacity, resulting in larger increases in C content and C:N. In contrast, the prasinophytes had smaller increases in C and C:N that were largely driven by lipid accumulation. Variation in C:P and N:P was species-specific and mainly determined by residual P pools, which likely represent intracellular storage of inorganic P and accounted for the majority of cellular P in all species throughout N starvation. Our findings indicate that carbohydrate and lipid accumulation may play a key role in determining the environmental and taxonomic variability in phytoplankton C:N. This quantitative assessment of macromolecular and elemental content spanning several marine phytoplankton species can be used to develop physiological models for ecological and biogeochemical applications.

A Mechanistic Model of Macromolecular Allocation, Elemental Stoichiometry, and Growth Rate in Phytoplankton

“…Laboratory studies have shown that almost all the cellular carbon in phytoplankton is accounted for by the major macromolecular pools: proteins (C Pro ), chlorophyll and other pigments (C Chl ), nucleic acids (C Nuc ), carbohydrates (C Carb ), and lipids (C Lip ) (Anderson, 1995;Liefer et al, 2019). The carbon quota of a phytoplankton cell, C Cell (mol C cell −1 ) is thus defined as the sum of these components along with carbon associated with nitrogen storage molecules, C Nsto :…”

“…Cellular nitrogen (N Cell ) is mostly associated with protein (N Pro ) (Anderson, 1995;Liefer et al, 2019), along with contributions from RNA (N RNA ), DNA (N DNA ), chlorophyll (N Chl ), and nitrogen storage (N Sto ):…”

“…The elemental stoichiometry of a cell depends on the relative abundances of the macromolecules from which it is composed and they, in turn, are linked to environment and physiological state (Sterner and Elser, 2002). The C:N:P stoichiometry of phytoplankton can be largely accounted for by the sum of contributions from a handful of major macromolecular components: protein, pigment, carbohydrate, lipid, DNA, RNA, and storage molecules (Liefer et al, 2019) each of which has a distinct elemental stoichiometry (see Table 1). For example, proteins are relatively rich in nitrogen so increasing the cellular allocation to protein typically raises cellular N:C (Sterner and Elser, 2002;Klausmeier et al, 2004).…”

“…For example, proteins are relatively rich in nitrogen so increasing the cellular allocation to protein typically raises cellular N:C (Sterner and Elser, 2002;Klausmeier et al, 2004). The broad-brush response of the macromolecular allocation of phytoplankton to changes in environmental factors is common across broad taxonomic groupings; for example in laboratory studies of nitrogen starvation in four marine species (Liefer et al, 2019) and with changing temperature and growth rate amongst a wide variety of freshwater phytoplankton (Fanesi et al, 2017(Fanesi et al, , 2019.…”

Representative diatom and coccolithophore species exhibit divergent responses throughout simulated upwelling cycles

“…With a maximum C:N of 20.2 ± 2.1 for C. decipiens and 29.96 ± 8.4 for E. huxleyi under the iron-replete condition, it can be inferred that a large proportion of the high carbon relative to nitrogen can be attributed to cells suffering from N and/or light limitation. Similarly under Nlimitation, several Thalassiosira species were shown to have C:N ratios over 20 which can be attributed to an accumula-tion of carbohydrates (36). Previous laboratory experiments that mimicked sinking cells with the diatom Pseudo-nitzschia australis grown in excess N relative to Si did not show as dramatic of an increase in C:N suggesting that Si limitation, as can often occur in conjunction with Fe-limited diatoms in the California coastal upwelling region, may influence these elemental stoichiometries (37,38).…”