Accumulation and enhanced cycling of polyphosphate by Sargasso Sea plankton in response to low phosphorus

Abstract

Phytoplankton alter their biochemical composition according to nutrient availability, such that their bulk elemental composition varies across oceanic provinces. However, the links between plankton biochemical composition and variation in biogeochemical cycling of nutrients remain largely unknown. In a survey of phytoplankton phosphorus stress in the western North Atlantic, we found that phytoplankton in the phosphorus-depleted subtropical Sargasso Sea were enriched in the biochemical polyphosphate (polyP) compared with nutrient-rich temperate waters, contradicting the canonical oceanographic view of polyP as a luxury phosphorus storage molecule. The enrichment in polyP coincided with enhanced alkaline phosphatase activity and substitution of sulfolipids for phospholipids, which are both indicators of phosphorus stress. Further, polyP appeared to be liberated preferentially over bulk phosphorus from sinking particles in the Sargasso Sea, thereby retaining phosphorus in shallow waters. Thus, polyP cycling may form a feedback loop that attenuates the export of phosphorus when it becomes scarce, contributes bioavailable P for primary production, and supports the export of carbon and nitrogen via sinking particles. nutrient limitation | phosphorus cycling | marine phytoplankton | lipids P hosphorus (P) is an essential element for all living organisms.However, P can be extremely scarce in open-ocean surface waters such as in the subtropical western North Atlantic (the Sargasso Sea), where soluble reactive P (SRP) concentrations are routinely <10 nmol·L −1 and turnover rates are on the order of hours (1). Despite this scarcity, primary production by phytoplankton in the Sargasso Sea does not appear to be limited primarily by P (2, 3), reflecting the intensity of P recycling by the microbial community (4, 5) and the exquisite adaptations of marine phytoplankton to low P conditions, which remain to be fully characterized.Phytoplankton respond to low P by producing enzymes such as alkaline phosphatase to hydrolyze extracellular dissolved organic P molecules (4, 6, 7), increasing the affinity and rate of P uptake (8, 9) and reducing their inventory of P-containing biochemicals (1, 10). In contrast, when P is abundant, phytoplankton take up excess P and store it as a luxury reserve that is generally thought to be composed of polyphosphate (polyP) (10-12). This modulation of P-containing biochemicals results in basin-scale relationships between P availability and biomass carbon-to-phosphorus (C:P) ratios (13). Presently, the only class of molecules known to consistently contribute to these gradients in cellular P are lipids because P stress in phytoplankton triggers substitution of non-P-membrane lipids for phospholipids, such as the sulfolipid sulfoquinovosyldiacylglycerol (SQDG) for the phospholipid phosphatidylglycerol (PG) (1, 14). However, lipid substitution alone probably cannot account for the full range of C:P observed in the ocean, and yet an understanding of other biochemical drivers of the C:P gradient remains el...

Interactions between growth-dependent changes in cell size, nutrient supply and cellular elemental stoichiometry of marine Synechococcus

“…For example, the growth rate hypothesis (Sterner and Elser, 2002) predicts that ribosomes are needed in high concentrations when cells are growing fast, and the high P-content (~9%) in ribosomal RNA can cause changes in C:P and N:P with growth . Variability in other cell components, such as proteins (Rhee, 1978;Lourenço et al, 1998), pigments, phospholipids (Van Mooy et al, 2006) and polyphosphates (Rao et al, 2009;Martin et al, 2014), which are rich in specific elements like N or P, also contribute to variation in cellular elemental stoichiometry and may also co-vary with growth (Rhee 1973). Thus, variable nutrient supply ratios (for example, N:P) are known to influence cellular biochemical content, which can affect growth and elemental stoichiometry of organisms (Rhee, 1978;Goldman et al, 1979;Geider and La Roche, 2002;Klausmeier et al, 2008).…”

SAR11 lipid renovation in response to phosphate starvation

“…Microbes inhabiting these low P i environments have evolved numerous strategies to maintain growth and enhance their competitiveness for trace amounts of P i . These mechanisms are commonly induced by P i starvation and include one or more of the following: (i) expression of high affinity P i transporters (6); (ii) reduction of cellular P i quotas (7, 8); (iii) utilization of alternate phosphorus sources (9, 10); and (iv) polyphosphate storage and breakdown (11,12). Such strategies facilitate survival in the face of P i insufficiency.…”

Phosphorus sequestration in the form of polyphosphate by microbial symbionts in marine sponges

“…At our sampling site, the concentration of P in the water column ranged from 0.1 to 0.5 μM, with a high nitrogen-to-P ratio, an indication of possible P limitation (13). It was recently reported in the oligotrophic Sargasso Sea that accumulation of polyP in phytoplankton enhanced the recycling of P in the local environment (14), and polyP metabolism can be important in the ocean (15). Considering the prevalence of sponges in the coral reef and the very low P concentration in the surrounding seawater, the amount of P sequestered within sponges is likely to be a significant proportion of the total P in the ecosystem.…”