Abstract
Phytoplankton growth rates are limited by the supply of iron (Fe) in approximately one third of the open ocean, with major implications for carbon dioxide sequestration and carbon (C) biogeochemistry. To date, understanding how alteration of Fe supply changes phytoplankton physiology has focused on traditional metrics such as growth rate, elemental composition, and biophysical measurements such as photosynthetic competence (Fv/Fm). Researchers have subsequently employed transcriptomics to probe relationships between changes in Fe supply and phytoplankton physiology. Recently, studies have investigated longer-term (i.e. following acclimation) responses of phytoplankton to various Fe conditions. In the present study, the coastal diatom, Thalassiosira pseudonana, was acclimated (10 generations) to either low or high Fe conditions, i.e. Fe-limiting and Fe-replete. Quantitative proteomics and a newly developed proteomic profiling technique that identifies low abundance proteins were employed to examine the full complement of expressed proteins and consequently the metabolic pathways utilized by the diatom under the two Fe conditions. A total of 1850 proteins were confidently identified, nearly tripling previous identifications made from differential expression in diatoms. Given sufficient time to acclimate to Fe limitation, T. pseudonana up-regulates proteins involved in pathways associated with intracellular protein recycling, thereby decreasing dependence on extracellular nitrogen (N), C and Fe. The relative increase in the abundance of photorespiration and pentose phosphate pathway proteins reveal novel metabolic shifts, which create substrates that could support other well-established physiological responses, such as heavily silicified frustules observed for Fe-limited diatoms. Here, we discovered that proteins and hence pathways observed to be down-regulated in short-term Fe starvation studies are constitutively expressed when T. pseudonana is acclimated (i.e., nitrate and nitrite transporters, Photosystem II and Photosystem I complexes). Acclimation of the diatom to the desired Fe conditions and the comprehensive proteomic approach provides a more robust interpretation of this dynamic proteome than previous studies.
Highlights
Many field studies have demonstrated that phytoplankton stocks across the world’s oceans are frequently limited by Fe supply [1,2,3,4]
Of the 1257 identifications from Fe- replete cells, 85% overlapped with the Fe-limited diatoms, revealing 188 and 593 proteins uniquely expressed under Fe-replete and Fe-limiting conditions, respectively (Figure 1)
This suggests that pure genomic analysis or transcriptomic tiling arrays may be limited in their ability to estimate cellular processes and that proteomics may provide an additional metric for determining metabolic strategies
Summary
Many field studies have demonstrated that phytoplankton stocks across the world’s oceans are frequently limited by Fe supply [1,2,3,4]. The widespread Fe limitation of phytoplankton in HNLC waters has major implications for the ocean C cycle and has led to modelling efforts to link the cycling and bioavailability of Fe to atmospheric draw-down of CO2 into the ocean [8], [9]. More fundamental research into the biochemical basis of long-term physiological acclimation used by diatoms to survive in low Fe environments provides researchers with more accurate information with which to better model global ocean biogeochemistry. Open ocean centric diatoms survive with extremely low cellular Fe requirements by parsimonious modifications to their photosynthetic architecture [17]
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