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 pCO2. 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 pCO2 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 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 pCO2, but cell size effects outweigh pCO2 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.
Highlights
Nitrogen is essential to life as a major constituent of proteins, nucleic acids, and other macromolecules
Total protein concentration per unit biovolume decreased with increasing cell volume, from ∼ 0.37 × 10−6 μg protein μm−3 for the smallest species, T. pseudonana, to ∼ 8 × 10−9 μg protein μm−3 for the largest species, C. wailesii, (Figure 1A)
As expected (Mullin et al, 1966; Finkel, 2001; Marañón et al, 2007, 2013) the cellular concentrations of total protein, chlorophyll and the membrane bound photosynthetic complexes Photosystem II, Photosystem I and Cytochrome b6f all declined with increasing cell volume, with similar negative scaling exponents
Summary
Nitrogen is essential to life as a major constituent of proteins, nucleic acids, and other macromolecules. Larger phytoplankton cells incur significant optical packaging effects (Falkowski, 1981; Morel and Bricaud, 1981; Kirk, 1994; Finkel, 2001), which lower the photons absorbed per unit of pigment-protein complex. These changes in optical performance decrease the return of captured photons per unit of metabolic nitrogen invested into pigment protein complexes (Raven, 1984). Some fraction of the reductant is retained in assimilated organic material (Kroon and Thoms, 2006; Kromkamp et al, 2008; Suggett et al, 2009; Halsey et al, 2010, 2013)
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