Nutrient limitation of picophytoplankton photosynthesis and growth in the tropical North Atlantic

Abstract

Identification of the proximal nutrient limiting primary production is a necessary first step toward evaluating the physiological state of phytoplankton communities and the biogeochemical constraints on the current oceanic carbon cycle. We conducted 48-h nutrient addition bioassay experiments to evaluate nitrogen, phosphorus, and iron limitation of primary productivity, net chlorophyll synthesis, and net increase in cell numbers of the dominant picophytoplankton from the tropical North Atlantic. Our results indicate that N was the proximal limiting factor for primary production during the autumn of 2002, followed by P and then Fe. Net chlorophyll synthesis was significantly stimulated by addition of N alone and further stimulated by addition of P. Analysis of picophytoplankton populations by analytical flow cytometry revealed a more complex response. Cellular red fluorescence, an index of cell chlorophyll content, increased in Prochlorococcus, Synechococcus, and picoeukaryotes in response to addition of NH 4 NO 3 but was not affected by single or combined additions of P and Fe. In contrast, cell abundance in these picophytoplankton populations increased only after combined N and P (63% of comparisons) or N and Fe (21% of comparisons) additions. Thus, our experiments revealed that chlorophyll synthesis and primary production were limited by the availability of nitrogen alone, while net increase in cell abundance was colimited by N and P or N and Fe in the majority of these picophytoplankton populations.

Analogous nutrient limitations in unicellular diazotrophs and Prochlorococcus in the South Pacific Ocean

“…The data suggest that Prochlorococcus and diazotrophs were limited by the same nutrients and that the net growth of Prochlorococcus was not primarily N limited, inspite the fact that overall N limitation was seen at the total phytoplankton biomass level. The results appear to differ from those from the North Atlantic (Bell et al, 2002;Moore et al, 2008), but the types of nutrient response measures used (pigment content vs cell abundance) may not be comparable, as per cell Chl a content potentially increases relatively more than cell abundance in response to N (Davey et al, 2008).…”

“…While some uncultivated Prochlorococcus are thought to acquire nitrate (Martiny et al, 2009), none of the cultivated strains have this capability. In the Sargasso Sea, Prochlorococcus pigment content responded positively to NH 4 NO 3 additions, although nitrate alone or iron had no effect (Davey et al, 2008;Moore et al, 2008). In contrast, in our experiments, the HL Prochlorococcus abundances remained stable or were reduced under N (nitrate þ ammonium) additions, and responded positively to iron and organic carbon additions.…”

“…Nitrogen is thought to be the most significant limiting nutrient in oligotrophic oceans with low nutrient and low chlorophyll, suggested by results from nutrient bioassays conducted in the North Atlantic (Graziano et al, 1996;Mills et al, 2004;Davey et al, 2008) and Pacific Oceans. The presence and activity of microorganisms fixing atmospheric N 2 in oligotrophic oceans indicates scarcity of bioavailable N and relative sufficiency of other essential nutrients that allows growth of these microorganisms.…”

Genome-wide analysis of diel gene expression in the unicellular N2-fixing cyanobacterium Crocosphaera watsonii WH 8501

“…Nearly all phosphate acquisition and metabolism genes were differentially expressed in C. watsonii during the diel cycle ( Figures 5b and c); the exception was phoH gene encoding phosphate starvation inducible protein (Supplementary Table S2). DNA replication may cause the increased demand for inorganic phosphate in a cell (Klausmeier et al, 2004;Davey et al, 2008) explaining maximum transcript abundance for phosphate acquisition and phosphatase genes during late light-early dark period (Figure 5b), similar to the expression of pstCAB and phoA genes in Prochlorococcus (Zinser et al, 2009). In contrast, only one phosphate transport gene, pstS, was cycling in Cyanothece, although it had similar to C. watsonii maximum expression at L11 .…”

Influence of CO<sub>2</sub> and nitrogen limitation on the coccolith volume of <I>Emiliania huxleyi</I> (Haptophyta)

“…Studies on E. huxleyi under nutrient limited conditions and elevated pCO 2 are rare (Sciandra et al, 2003;Leonardos and Geider, 2005;Borchard et al, 2011), whereas light, macroand micronutrient supply in the upper ocean are the main factors limiting phytoplankton growth (Davey et al, 2008;Moore et al, 2008;Marinov et al, 2010). Emiliania huxleyi is a poor competitor for nitrate compared to diatoms (Riegmann et al, 1992) but has an extraordinarily high affinity for orthophosphate and is able to utilise organic phosphates (Riegmann et al, 2000), displaying a high competitive ability in phosphate limited areas of the ocean.…”