Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability

In vast expanses of the oceans, growth of large phytoplankton such as diatoms is limited by iron availability. Diatoms respond almost immediately to the delivery of iron and rapidly comprise the majority of phytoplankton biomass. The molecular bases underlying the subsistence of diatoms in iron-poor waters and the plankton community dynamics that follow iron-resupply remain largely unknown. Here we use comparative metatranscriptomics to identify changes in gene expression associated with iron-stimulated growth of diatoms and other eukaryotic plankton groups. A microcosm iron-enrichment experiment using mixed-layer waters from the NE Pacific Ocean resulted in increased proportions of diatom transcripts with a subsequent reduction in proportions of transcripts from most other taxa within 98 hours after iron addition. Hundreds of diatom genes were differentially expressed in the iron-enriched community when compared to iron-limited community; transcripts of diatom genes required for synthesis of photosynthesis and chlorophyll components, nitrate assimilation and the urea cycle, and synthesis of hydrocarbon storage compounds were significantly over-represented. Transcripts of genes encoding rhodopsins in eukaryotic phytoplankton were significantly under-represented following iron enrichment, suggesting rhodopsins help cells cope with low-iron conditions. Oceanic diatoms appear to display a distinctive transcriptional response to iron enrichment that allow chemical reduction of available nitrogen and carbon sources along with a continued dependence on iron-free photosynthetic proteins rather than substituting for iron-containing functional equivalents present within their gene repertoire. This ability of diatoms to divert their newly acquired iron towards nitrate assimilation may underlie why diatoms consistently dominate iron enrichments in HNLC regions.