Decoupling silicon metabolism from carbon and nitrogen assimilation poises diatoms to exploit episodic nutrient pulses in a coastal upwelling system

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.