The effect of cell size on cellular Zn and Cd and Zn‐Cd‐CO₂ colimitation of growth rate in marine diatoms

Abstract

Cadmium (Cd) can serve as nutrient in marine diatoms by partially replacing zinc (Zn) in Zn‐limited cells. A major basis for this is the replacement of Cd for Zn in a Cd‐containing carbonic anhydrase (CDCA) needed for cellular acquisition of CO2. As a result of these interactions, cells can become colimited by Zn, Cd, and CO2. Large cell size should restrict the cellular uptake of Zn, Cd, and CO2 due to decreasing surface to volume ratios and limitation of diffusive flux of these nutrients to the cell surface. Large cells are thus more likely to become Zn‐Cd‐CO2 colimited than smaller ones. These predictions were confirmed in experiments with three marine diatoms: Thalassiosira pseudonana, Thalassiosira weissflogii, and Ditylum brightwellii, ranging in cell volume from 50 to 6000 fL. Cellular Zn : C ratios decreased by 10‐fold between the largest and smallest species, and consequently, the largest diatom was more readily growth‐limited than smaller ones by low external concentrations of bioavailable dissolved inorganic Zn (Zn′). Decreasing cellular Zn : C ratios were accompanied by large increases in cellular Cd uptake rates and Cd : C ratios. However, at the lowest Zn′ concentrations, Cd uptake plateaued, with the larger cells having lower cellular concentrations of both Zn and Cd. Cellular replacement of Zn by Cd was accompanied by increases in cellular CDCA expression. The largest diatom had higher combined carbonic anhydrase activities for a given Zn‐, Cd‐limited growth rate, supporting the hypothesis that these cells could be colimited by Zn, Cd, and CO2 at low external CO2 concentrations.

The Role of Extracellular Carbonic Anhydrase in Biogeochemical Cycling: Recent Advances and Climate Change Responses

“…A recent field study by Morel, et al [ 48 ] in the eastern tropical South Pacific revealed that the substitution of Cd and Co for Zn occurred when dissolved Zn levels were extremely low and not necessarily with the lowest pCO 2 conditions. This further suggests that diatoms in the marine environment may be co-limited by Zn-Cd-Co and CO 2 [ 49 ]. To date, the cellular quotas of Zn attached to CA in marine phytoplankton remain an open question.…”

“…Some species are likely to utilize Cd, Co or even newly found Mn as a cofactor, and such estimations are likely to be very uncertain within natural assemblages. Trace metal quotas in marine phytoplankton also depend on cell size [ 49 , 51 ]. A holistic approach is needed to resolve the coupling of marine trace metal chemistry to total CA expression and activity in natural phytoplankton assemblages.…”

“…A shift towards larger cells—as observed for diatoms—could increase the vertical flux of POC and the efficiency of the carbon pump to the deep ocean by forming rapidly sinking aggregates [ 79 ]. Moreover, larger diatoms had higher total CA activity for a given Zn- or Cd-limited growth rate, and thus, the cell could be co-limited by Zn, Cd, and CO 2 at low external CO 2 concentrations [ 49 ]. This is because larger cells have lower cellular Zn due to their lower cell surface to volume ratio, and a greater restriction of a diffusive flux of biologically available dissolved Zn to their surface due to a thicker diffusive boundary layer around their cells [ 80 ].…”

The response of diazotrophs to nutrient amendment in the South China Sea and western North Pacific

“…Briefly, 4-9 L of surface waters was filtered onto acid-cleaned 0.22 µm polycarbonate membrane filters. For PFe intra samples, in order to remove metal bound to the cell surface, cells were exposed twice to an oxalate-EDTA solution for 5 min and rinsed nine times with Chelex-cleaned 0.56 mol L −1 NaCl solution (Li et al, 2020). PFe total and PFe intra concentrations were then determined by inductively coupled plasma mass spectrometry (ICP-MS 7700x, Agilent).…”

The response of diazotrophs to nutrient amendment in the South China Sea and western North Pacific

“…Briefly, 4-9 L of surface waters were filtered onto acid-cleaned 0.22-μm polycarbonate membrane filters. For PFeintra samples, in order to remove metal-bound to the cell surface, cells were exposed twice to an oxalate-EDTA solution for 5 minutes and rinsed nine times with Chelex-cleaned 0.56 mol L -1 NaCl solution (Li et al, 2020).…”