Diminished carbon and nitrate assimilation drive changes in diatom elemental stoichiometry independent of silicification in an iron-limited assemblage.

In the California Current Ecosystem, upwelled water low in dissolved iron (Fe) can limit phytoplankton growth, altering the elemental stoichiometry of the particulate matter and dissolved macronutrients. Iron-limited diatoms can increase biogenic silica (bSi) content >2-fold relative to that of particulate organic carbon (C) and nitrogen (N), which has implications for carbon export efficiency given the ballasted nature of the silica-based diatom cell wall. Understanding the molecular and physiological drivers of this altered cellular stoichiometry would foster a predictive understanding of how low Fe affects diatom carbon export. In an artificial upwelling experiment, water from 96 m depth was incubated shipboard and left untreated or amended with dissolved Fe or the Fe-binding siderophore desferrioxamine-B (+DFB) to induce Fe-limitation. After 120 h, diatoms dominated the communities in all treatments and displayed hallmark signatures of Fe-limitation in the +DFB treatment, including elevated particulate Si:C and Si:N ratios. Single-cell, taxon-resolved measurements revealed no increase in bSi content during Fe-limitation despite higher transcript abundance of silicon transporters and silicanin-1. Based on these findings we posit that the observed increase in bSi relative to C and N was primarily due to reductions in C fixation and N assimilation, driven by lower transcript expression of key Fe-dependent genes.

Different iron storage strategies among bloom-forming diatoms.

Diatoms are prominent eukaryotic phytoplankton despite being limited by the micronutrient iron in vast expanses of the ocean. As iron inputs are often sporadic, diatoms have evolved mechanisms such as the ability to store iron that enable them to bloom when iron is resupplied and then persist when low iron levels are reinstated. Two iron storage mechanisms have been previously described: the protein ferritin and vacuolar storage. To investigate the ecological role of these mechanisms among diatoms, iron addition and removal incubations were conducted using natural phytoplankton communities from varying iron environments. We show that among the predominant diatoms, Pseudo-nitzschia were favored by iron removal and displayed unique ferritin expression consistent with a long-term storage function. Meanwhile, Chaetoceros and Thalassiosira gene expression aligned with vacuolar storage mechanisms. Pseudo-nitzschia also showed exceptionally high iron storage under steady-state high and low iron conditions, as well as following iron resupply to iron-limited cells. We propose that bloom-forming diatoms use different iron storage mechanisms and that ferritin utilization may provide an advantage in areas of prolonged iron limitation with pulsed iron inputs. As iron distributions and availability change, this speculated ferritin-linked advantage may result in shifts in diatom community composition that can alter marine ecosystems and biogeochemical cycles.

Divergent gene expression among phytoplankton taxa in response to upwelling.

Frequent blooms of phytoplankton occur in coastal upwelling zones creating hotspots of biological productivity in the ocean. As cold, nutrient-rich water is brought up to sunlit layers from depth, phytoplankton are also transported upwards to seed surface blooms that are often dominated by diatoms. The physiological response of phytoplankton to this process, commonly referred to as shift-up, is characterized by increases in nitrate assimilation and rapid growth rates. To examine the molecular underpinnings behind this phenomenon, metatranscriptomics was applied to a simulated upwelling experiment using natural phytoplankton communities from the California Upwelling Zone. An increase in diatom growth following 5 days of incubation was attributed to the genera Chaetoceros and Pseudo-nitzschia. Here, we show that certain bloom-forming diatoms exhibit a distinct transcriptional response that coordinates shift-up where diatoms exhibited the greatest transcriptional change following upwelling; however, comparison of co-expressed genes exposed overrepresentation of distinct sets within each of the dominant phytoplankton groups. The analysis revealed that diatoms frontload genes involved in nitrogen assimilation likely in order to outcompete other groups for available nitrogen during upwelling events. We speculate that the evolutionary success of diatoms may be due, in part, to this proactive response to frequently encountered changes in their environment.

Taxon-specific contributions to silica production in natural diatom assemblages.

The metabolic activity and growth of phytoplankton taxa drives their ecological function and contribution to biogeochemical processes. We present the first quantitative, taxon-resolved silica production rates, growth rates, and silica content estimates for co-occurring diatoms along two cross-shelf transects off the California coast using the fluorescent tracer PDMPO (2-(4-pyridyl)-5-((4-(2-dimethylaminoethylaminocarbamoyl)methoxy)phenyl)oxazole), and confocal microscopy. Taxon contribution to total diatom community silica production was predominantly a function of the surface area of new frustule that each taxon created as opposed to cell abundance or frustule thickness. The influential role of surface area made large diatoms disproportionately important to community silica production over short time scales (<1 d). In some cases, large taxa that comprised only ~15% of numerical cell abundance accounted for over 50% of total community silica production. Over longer time scales relevant to bloom dynamics, the importance of surface area declines and growth rate becomes the dominant influence on contribution to production. The relative importance of surface area and growth rate in relation to silica production was modeled as the time needed for a smaller, faster-growing taxon to create more surface area than a larger, slower-growing taxon. Differences in growth rate between the taxa effected the model outcome more than differences in surface area. Shifts in relative silica production among taxa are time restricted by finite resources that limit the duration of a bloom. These patterns offer clues as to how taxa respond to their environment and the consequences for both species succession and the potential diatom contribution to elemental cycling.