A role for manganese in superoxide dismutases and growth of iron-deficient diatoms

We have discovered that coastal and oceanic diatoms require more manganese (Mn) to grow in iron (Fe) -deficient than in Fe-sufficient seawater. At low inorganic concentrations, like those of the open sea, Fe and Mn can thus colimit Thalassiosira pseudonana and T. oceanica so that maximum rates of cell division are achieved only when both resources are added simultaneously to cultures. Colimited diatoms amended with either Fe or Mn alone show unique physiological responses, which implies that the observed interaction between Fe and Mn is not caused by a substitution of one metal for the other. Iron deficiency increases the Mn quota of T. pseudonana by three times compared with controls and enhances the production of reactive oxygen species by 1.7 times in T. weissflogii. Both diatoms respond to this oxidative stress by increasing the activities of the antioxidant enzyme superoxide dismutase (SOD). The Mn content of the SODs increases by 1.8 to 2.8 times when Fe is limiting, which suggests that the SODs contain Mn and may account for part of the observed increase in the Mn quota. Such an increased biochemical requirement may elevate the Mn content of low Fe diatoms, and possibly other phytoplankton, resulting in high Mn : Fe ratios in surficial particulate matter in Fe-limited regions of the sea. Iron greatly influences the ecology and physiology of phytoplankton in some open-ocean regions and upwelling regimes (Coale et al. 1996; Hutchins et al. 1998). Subnanomolar concentrations of dissolved Fe are typical of surface waters and limiting to phytoplankton growth (Price and Morel 1998). Phytoplankton exist in these environments because they are able to reduce their Fe requirements (Sunda and Huntsman 1995) and to acquire what little Fe exists with high-affinity Fe transport systems (Maldonado and Price 1999). Intense demand for limiting Fe nonetheless leads to characteristic changes in phytoplankton physiology and biochemistry. A large body of literature has examined the strategies of Fe acquisition by plankton. Under limiting conditions, phytoplankton up-regulate Fe transport capacity (Morel 1987), produce siderophores (Wilhelm and Trick 1994), reduce Fe(III) chelates (Maldonado and Price 2001), and even ingest insoluble, particulate forms of Fe (Maranger et al. 1998; Nodwell and Price 2000). These strategies represent adaptations to maintain high cellular Fe quotas (QFe) and facilitate normal functioning of cellular metabolism, which is highly dependent on Fe (Raven 1990). When the Fe supply is insufficient to meet cellular demand, the Fe : C ratio drops (Sunda and Huntsman 1995; Maldonado and Price 1996), electron transport chains—such as those involved in photosynthesis—are compromised (Greene et al. 1991), and the growth rate slows. The replacement of Fe-containing enzymes and proteins with their Fe-free equivalents is one way to use Fe sparingly and to maintain biochemical function. Some organisms have 1 Corresponding author ([email protected]).