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Diatoms serve as the major link between the marine carbon (C) and silicon (Si) biogeochemical cycles through their contributions to primary productivity and requirement for Si during cell wall formation. Although several culture-based studies have investigated the molecular response of diatoms to Si and nitrogen (N) starvation and replenishment, diatom silicon metabolism has been understudied in natural populations. A series of deckboard Si-amendment incubations were conducted using surface water collected in the California Upwelling Zone near Monterey Bay. Steep concentration gradients in macronutrients in the surface ocean coupled with substantial N and Si utilization led to communities with distinctly different macronutrient states: replete (‘healthy’), low N (‘N-stressed’), and low N and Si (‘N- and Si-stressed’). Biogeochemical measurements of Si uptake combined with metatranscriptomic analysis of communities incubated with and without added Si were used to explore the underlying molecular response of diatom communities to different macronutrient availability. Metatranscriptomic analysis revealed that N-stressed communities exhibited dynamic shifts in N and C transcriptional patterns suggestive of compromised metabolism. Expression patterns in communities experiencing both N and Si stress imply that the presence of Si stress may partially ameliorate N stress and dampen the impact on organic matter metabolism. This response builds upon previous observations that the regulation of C and N metabolism is decoupled from Si limitation status, where Si stress allows the cell to optimize the metabolic machinery necessary to respond to episodic pulses of nutrients. Several well-characterized Si-metabolism associated genes were found to be poor molecular markers of Si physiological status; however, several uncharacterized Si-responsive genes were revealed to be potential indicators of Si stress or silica production.

 

The contribution of diatoms to the production and export of organic carbon is highly modified in high-nutrient low-chlorophyll (HNLC) regions due to the decoupling of upper-ocean silicon and carbon cycling caused by low iron. The Si cycle and the role of diatoms in the biological carbon pump was examined at Ocean Station Papa (OSP) in the HNLC region of the northeastern subarctic Pacific during the NASA EX port Processes in the Ocean from RemoTe Sensing (EXPORTS) field study. Sampling occurred during the annual minimum in surface silicic acid concentration, [Si(OH)4 ]. Biogenic silica (bSi) concentrations were low being in the tens of nanomolar range despite high [Si(OH) 4 ], ~15 μM. On average the > 5.0 μm particle size fraction dominated Si dynamics accounting for 65% of bSi stocks and 81% of Si uptake compared to the small fraction (0.6 - 5.0 μm). Limitation of Si uptake was detected in the small, but not the large, size fraction. Small diatoms were co-limited with growth rate restricted by Fe and Si uptake restricted by [Si(OH) 4 ], whereas larger diatoms were only growth limited by Fe. About a third of silica production was exported out of the upper 100 m. The contribution of diatoms to carbon export (9 - 13%) was about twice their contribution to primary productivity (3 - 7%). The combination of low silica production, low diatom primary productivity and high bSi export efficiency at OSP was more similar to the dynamics in the subtropical gyres than to other HNLC regions. 

Diatoms are major contributors to marine primary productivity and carbon export due to their rapid growth in high-nutrient environments and their heavy silica ballast. Their contributions are highly modified in high-nutrient low-chlorophyll regions due to the decoupling of upper-ocean silicon and carbon cycling caused by low iron (Fe). The Si cycle and the role of diatoms in the biological carbon pump was examined at Ocean Station Papa (OSP) in the HNLC region of the northeastern subarctic Pacific during the NASA EXport Processes in the Ocean from RemoTe Sensing (EXPORTS) field study. Sampling occurred during the annual minimum in surface silicic acid (Si(OH)4) concentration. Biogenic silica (bSi) concentrations were low, being in the tens of nanomolar range, despite high Si(OH)4 concentrations of about 15 μM. On average, the >5.0-µm particle size fraction dominated Si dynamics, accounting for 65% of bSi stocks and 81% of Si uptake compared to the small fraction (0.6–5.0 μm). Limitation of Si uptake was detected in the small, but not the large, size fraction. Growth rate in small diatoms was limited by Fe, while their Si uptake was restricted by Si(OH)4 concentration, whereas larger diatoms were only growth-limited by Fe. About a third of bSi production was exported out of the upper 100 m. The contribution of diatoms to carbon export (9–13%) was about twice their contribution to primary productivity (3–7%). The combination of low bSi production, low diatom primary productivity and high bSi export efficiency at OSP was more similar to the dynamics in the subtropical gyres than to other high-nutrient low-chlorophyll regions. 

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.

 

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-nitzschiawere favored by iron removal and displayed unique ferritin expression consistent with a long-term storage function. Meanwhile,ChaetocerosandThalassiosiragene expression aligned with vacuolar storage mechanisms.Pseudo-nitzschiaalso 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.