Response of the marine diatom Thalassiosira weissflogii to iron stress1

The coastal diatom Thalassiosira weissfogii responds to iron limitation with decreasing growth rate, decreasing quotas of cellular iron, and increasing rates of maximum short term uptake. Growth response to steady iron limitation can be modeled according to the equations of Droop and Monod. The cellular iron quota varies from about 2 to 25 x 1O-5 mol iron per liter-cell with increasing iron; the half-saturation constant for growth, K,, is 1.1 x 10m21 M (free ferric ion). In contrast, the half-saturation constant for iron uptake, K,, is about 3 x lo-l9 M; the maximum iron uptake rate (p,,,) is increased several-fold under iron limitation, resulting in a potential short term uptake rate that is a few hundred times the steady state rate. At a fixed concentration of free manganese ion, the cellular manganese quota is increased several-fold in iron-limited cultures compared to ironsufficient cultures. Iron is a component of many algal proteins responsible in particular for the biosynthesis of chlorophyll and electron transport reactions of respiration and photosynthesis. In oxygenated seawater the low solubility of ferric hydroxide has been hypothesized to limit the biological availability of iron and algal growth (Menzel and Ryther 1960). Indeed, there is recent evidence of iron limitation of marine photosynthetic organisms (Entsch et al. 1983; Subba Rao and Yeats 1984). Phytoplankters in the sea adjust their nutrient uptake rates according to variations in nutrient availability. In studies of algal growth under limitation by nitrogen, phosphorus, and silicon, it has been observed that algae regulate their short term nutrient uptake rate by varying rates of maximum uptake (p,,,) as much as 30-fold, but not half-saturation constants (K,) (Goldman and McCarthy 1978; Nalewajko and Lean 1980; Tilman and Kilham 1976; McCarthy 198 1). Sunda and Huntsman (1985) found that a similar response of short term uptake rate to nutrient stress controls cellular man1 This work was supported in part by grants from NOAA (NA79AA) and NSF (OCE 83-17532), and by a NATO fellowship to G.I.H. 2 Current address: Health Sciences and Technology, 20A104, Massachusetts Institute of Technology, Cambridge 02 139. 3 Reprint requests: 48-425, Ralph M. Parsons Laboratory, Massachusetts Institute of Technology, Cambridge 02 139. ganese quotas and transport in a Chlamydomonas species under manganese limitation. In addition to regulating short term uptake rates, organisms may respond to iron limitation by substituting another metal at a protein-active site or by replacing one ironcontaining protein with another. For example, in bacteria, superoxide dismutase may contain either iron or manganese depending on their concentrations (Meier et al. 1982). In cyanobacteria the synthesis of flavodoxin, a noniron-containing electron carrier, is favored over ferredoxin, a Fe-S protein, in response to iron stress (Entsch et al. 1983). We examine here the ability of a marine diatom, Thalassiosira weissjlogii, to regulate its short term iron uptake rate. We compare growth rates, cellular iron quotas, and short term iron uptake of cells maintained in iron-sufficient and iron-deficient semicontinuous batch cultures. In addition, we report on the effect of iron limitation on cellular manganese quotas at constant concentrations of free manganese ion. The limitation of algal growth by iron has been studied in continuous cultures of Dunaliella tertiolecta (Davies 1970), Pavlova lutherii (Droop 1973), Isochrysis galbana, and Phaeodactylum tricornutum (Glover 1977). These studies provide no information on short term uptake rates and the reported cellular iron quotas may be too high due to adsorption of saturated hydrous fer-