Zinc–cobalt colimitation of Phaeocystis antarctica

We present evidence demonstrating the capability of Phaeocystis antarctica colonies to substitute cobalt (Co) and zinc (Zn) as micronutrients, in which Co limitation is alleviated by additions of Zn and vice versa. Maximal growth rates and biomass were determined by fluorescence and the values obtained under replete Zn and no added Co conditions were significantly higher than under replete Co and no added Zn conditions, suggesting a preference for Zn over Co. The observation of Zn-Co substitution in this high-latitude member of the Prymnesiophyceae class, coupled with similar previous observations in the coccolithophore Emiliana huxleyi and several centric diatoms, suggests that Zn-Co substitution could be a widespread global phenomenon in eukaryotic phytoplankton. The Zn-Co biochemical substitution seen in Phaeocystis might be the result of evolutionary pressure for maintaining growth rates in high export environments in which rapid depletion of Zn, Co, and carbon occur simultaneously in the upper water column. The influence of trace element nutrition on phytoplankton has been studied in a variety of representative species, but relatively little work has been done on phytoplankton from high-latitude environments. Phaeocystis sp. is a cosmopolitan marine phytoplankter found in low-temperature marine environments throughout the oceans. Species of Phaeocystis are known to be key components of the phytoplankton community in many environments (Schoemann et al. 2005). For example, the strain Phaeocystis antarctica is a major component of the phytoplankton community structure in the Ross Sea of Antarctica, exerting its biogeochemical influence through both carbon export and dimethyl sulfide production (DiTullio et al. 2000 and references therein). During the annual bloom, P. antarctica often forms large spherical colonies with cells distributed outside of a mucilaginous center (Scott and Marchant 2005). The phytoplankton productivity of the Ross Sea is known to be subject to seasonal iron limitation (Sedwick et al. 2000), whereas the influence of zinc (Zn) and manganese (Mn) has not been observed to have any noticeable effect on chlorophyll a (Chl a) concentrations in bottle incubations (Sedwick et al. 2000; Cochlan et al. 2002). The influences of other micronutrients such as cobalt (Co), cadmium (Cd), and vitamin B12 have not been studied in this environment until recently (Bertrand et al. 2007). Yet, analyses of field concentrations of metals have found that elements such as iron, Co, Cd, and Zn can all be drawn down to low concentrations in the Ross Sea surface waters (Fitzwater et al. 2000; Bertrand et al. 2007). The nutritional importance of elements such as Co, Cd, and Zn to marine phytoplankton has been the subject of numerous studies in recent years (Morel et al. 1994; Saito et al. 2003, and references therein). In several species of centric marine diatoms (Thalassiosira weissflogii, Thalassiosira oceanica, and Thalassiosira pseudonana), a physiological Zn requirement can be replaced by either Co or Cd (Price and Morel 1990; Sunda and Huntsman 1995). Moreover, this requirement is connected to the carbon acquisition system on the basis of physiological evidence demonstrating colimitation by carbon when under Zn limitation (Morel et al. 1994), as well as molecular evidence demonstrating the presence of Zn and Cd in the active site of two carbonic anhydrase enzymes purified and sequenced from these phytoplankton (Roberts et al. 1997; Lane et al. 2005). In contrast to these studies, the diatom Chaetoceros calcitrans appears to lack the Zn-Co substitution capability (Timmermans et al. 2001), although the molecular basis for this is unknown. Among the coccolithophores, Emiliania huxleyi demonstrates a Co-Zn substitution capability (Sunda and Huntsman 1995), although a Cd substitution capability for Zn has not yet been reported for this organism (Sunda and Huntsman 2000). In stark contrast to these centric diatoms and coccolithophores, the marine cyanobacteria (e.g., Prochlorococcus and Synechococcus) have an absolute Co requirement and a small to nondetectable zinc requirement, and appear incapable of Zn-Co substitution (Sunda and Huntsman 1995; Saito et al. 2002). In addition to these biochemical differences, the metal acquisition capabilities of different groups of phytoplankton can also vary significantly. This is largely because of the presence of organic metal–ligand complexes in seawater that can interfere with the metal ion transport machinery of the phytoplankton cells (Bruland 1992; Saito and Moffett 2001; Ellwood 2004 and references therein). At this time, little is known about how different eukaryotic phytoplankton groups interact with metal–ligand complexes, although there is some evidence that the cyanobac1 Corresponding author ([email protected]).