Large centric diatoms allocate more cellular nitrogen to photosynthesis to counter slower RUBISCO turnover rates

Abstract

Diatoms contribute ∼40% of primary production in the modern ocean and encompass the largest cell size range of any phytoplankton group. Diatom cell size influences their nutrient uptake, photosynthetic light capture, carbon export efficiency, and growth responses to increasing pCO 2 . We therefore examined nitrogen resource allocations to the key protein complexes mediating photosynthesis across six marine centric diatoms, spanning 5 orders of magnitude in cell volume, under past, current and predicted future pCO 2 levels, in balanced growth under nitrogen repletion. Membrane bound photosynthetic protein concentrations declined with cell volume in parallel with cellular concentrations of total protein, total nitrogen and chlorophyll. Larger diatom species, however, allocated a greater fraction (by 3.5-fold) of their total cellular nitrogen to the soluble Ribulose-1,5-bisphosphate Carboxylase Oxygenase (RUBISCO) carbon fixation complex than did smaller species. Carbon assimilation per unit of RUBISCO large subunit (C RbcL −1 s −1 ) decreased with cell volume, from ∼8 to ∼2 C RbcL −1 s −1 from the smallest to the largest cells. Whilst a higher allocation of cellular nitrogen to RUBISCO in larger cells increases the burden upon their nitrogen metabolism, the higher RUBISCO allocation buffers their lower achieved RUBISCO turnover rate to enable larger diatoms to maintain carbon assimilation rates per total protein comparable to small diatoms. Individual species responded to increased pCO 2 , but cell size effects outweigh pCO 2 responses across the diatom species size range examined. In large diatoms a higher nitrogen cost for RUBISCO exacerbates the higher nitrogen requirements associated with light absorption, so the metabolic cost to maintain photosynthesis is a cell size-dependent trait. Citation: Wu Y, Jeans J, Suggett DJ, Finkel ZV and Campbell DA (2014) Large centric diatoms allocate more cellular nitrogen to photosynthesis to counter slower RUBISCO turnover rates. Front. Mar. Sci. 1:68.

Interactive effects of nitrogen and light on growth rates and RUBISCO content of small and large centric diatoms

“…The prevalence of larger phytoplankton cells in eutrophic and brackish coastal waters can be explained by enhanced resistance to predation (Ward et al 2012), greater nutrient storage capacity (Grover 2011) and potentially lower metabolic costs to withstand and exploit fluctuating light because of lower susceptibility to photoinactivation of PSII (Key et al 2010). We found that under near-saturating growth light and media with high-nitrogen larger diatoms invested more cellular nitrogen to RUBISCO than did smaller ones, to counter a lower achieved RUBISCO turnover rate (Wu et al 2014b), a finding that parallels increased allocations to RUBISCO in cold water diatoms where RUBISCO performance is kinetically limited (Losh et al 2013; Young et al 2015). To explain our finding of slower achieved RUBISCO turnover in larger diatoms (Wu et al 2014b), we hypothesized that in higher-nitrogen (HN) media large cells have luxury accumulation of RUBISCO protein that in turn lowers their achieved performance per unit RUBISCO.…”

“…We found that under near-saturating growth light and media with high-nitrogen larger diatoms invested more cellular nitrogen to RUBISCO than did smaller ones, to counter a lower achieved RUBISCO turnover rate (Wu et al 2014b), a finding that parallels increased allocations to RUBISCO in cold water diatoms where RUBISCO performance is kinetically limited (Losh et al 2013; Young et al 2015). To explain our finding of slower achieved RUBISCO turnover in larger diatoms (Wu et al 2014b), we hypothesized that in higher-nitrogen (HN) media large cells have luxury accumulation of RUBISCO protein that in turn lowers their achieved performance per unit RUBISCO. To test this hypothesis, we grew two representative diatom strains with a ~4 orders of magnitude difference in cell biovolume, small Thalassiosira pseudonana (~40 µm 3 ) and large T. punctigera (~300,000 µm 3 ) in turbidostats across a range of growth light, in lower-nitrogen (LN) media to attempt to limit cellular luxury accumulation of RUBISCO protein, compared with cells grown in a typical laboratory HN media.…”

“…Nitrogen is critical for marine phytoplankton to build abundant cellular materials including proteins and nucleic acids to support their growth and cell division (Finkel et al 2010; Wu et al 2014b; Li et al 2015). One of these nitrogen-rich materials the ribulose-1,5-bisphosphate carboxylase oxygenase (RUBISCO) protein is particularly important, because this bifunctional enzyme catalyzes the initial step of photosynthetic carbon reduction by combining CO 2 with ribulose-1,5-bisphosphate (RuBP) (Mizohata et al 2002), fixing inorganic carbon to organic matter (Kroth 2015).…”

“…Furthermore, pigment packaging in large phytoplankton can lead to a decline in light absorption per unit of pigment–protein complex (Finkel 2001; Key et al 2010; Clark et al 2013), and thus, a decrease in captured photons per unit of metabolic nitrogen invested into pigment–protein complexes (Raven 1984; Wu et al 2014b) and carbon assimilation per RUBSICO molecule (Wu et al 2014b), again conferring advantages to smaller phytoplankton. The prevalence of larger phytoplankton cells in eutrophic and brackish coastal waters can be explained by enhanced resistance to predation (Ward et al 2012), greater nutrient storage capacity (Grover 2011) and potentially lower metabolic costs to withstand and exploit fluctuating light because of lower susceptibility to photoinactivation of PSII (Key et al 2010).…”

Autotrophic Stoichiometry Emerging from Optimality and Variable Co-limitation

“…In the set of culture species compiled here major taxonomic groups are underrepresented. For example, diatoms usually have higher P:C than other groups (Quigg et al, 2003) or larger diatom species invest a much greater fraction of their N pool into Rubisco than smaller species (Wu et al, 2014). To describe these trends, also model coefficients in Table S2 may be more group specificor should vary at time-scales larger than the few weeks considered…”