Abstract
Abstract. Phaeocystis antarctica is an important phytoplankter of the Ross Sea where it dominates the early season bloom after sea ice retreat and is a major contributor to carbon export. The factors that influence Phaeocystis colony formation and the resultant Ross Sea bloom initiation have been of great scientific interest, yet there is little known about the underlying mechanisms responsible for these phenomena. Here, we present laboratory and field studies on Phaeocystis antarctica grown under multiple iron conditions using a coupled proteomic and transcriptomic approach. P. antarctica had a lower iron limitation threshold than a Ross Sea diatom Chaetoceros sp., and at increased iron nutrition (> 120 pM Fe') a shift from flagellate cells to a majority of colonial cells in P. antarctica was observed, implying a role for iron as a trigger for colony formation. Proteome analysis revealed an extensive and coordinated shift in proteome structure linked to iron availability and life cycle transitions with 327 and 436 proteins measured as significantly different between low and high iron in strains 1871 and 1374, respectively. The enzymes flavodoxin and plastocyanin that can functionally replace iron metalloenzymes were observed at low iron treatments consistent with cellular iron-sparing strategies, with plastocyanin having a larger dynamic range. The numerous isoforms of the putative iron-starvation-induced protein (ISIP) group (ISIP2A and ISIP3) had abundance patterns coinciding with that of either low or high iron (and coincident flagellate or the colonial cell types in strain 1871), implying that there may be specific iron acquisition systems for each life cycle type. The proteome analysis also revealed numerous structural proteins associated with each cell type: within flagellate cells actin and tubulin from flagella and haptonema structures as well as a suite of calcium-binding proteins with EF domains were observed. In the colony-dominated samples a variety of structural proteins were observed that are also often found in multicellular organisms including spondins, lectins, fibrillins, and glycoproteins with von Willebrand domains. A large number of proteins of unknown function were identified that became abundant at either high or low iron availability. These results were compared to the first metaproteomic analysis of a Ross Sea Phaeocystis bloom to connect the mechanistic information to the in situ ecology and biogeochemistry. Proteins associated with both flagellate and colonial cells were observed in the bloom sample consistent with the need for both cell types within a growing bloom. Bacterial iron storage and B12 biosynthesis proteins were also observed consistent with chemical synergies within the colony microbiome to cope with the biogeochemical conditions. Together these responses reveal a complex, highly coordinated effort by P. antarctica to regulate its phenotype at the molecular level in response to iron and provide a window into the biology, ecology, and biogeochemistry of this group.
Highlights
A biphasic response in P. antarctica strain 1871 was observed; cultures exhibited a clear single-cell versus colony response to low and high iron, respectively, that was observed by microscopy and readily apparent to the naked eye due to the millimeter size of the colonies
Phaeocystis antarctica is a major contributor to Southern Ocean primary productivity, yet arguably is one of the least well understood of key marine phytoplankton species
These results demonstrate that P. antarctica has evolved to utilize elaborate capabilities to confront the widespread iron scarcity that occurs in the Ross Sea and Southern Ocean, including iron-metalloenzyme-sparing systems and the deployment of transport and other systems that appear to be unique to the flagellate and colonial morphotypes
Summary
The genus Phaeocystis is a cosmopolitan marine phytoplankton group that plays a key role in global carbon and sulfur cycles (Hamm et al, 1999; Matrai et al, 1995; Rousseau et al, 2007; Schoemann et al, 2005; Smith et al, 1991; Solomon et al, 2003; Thingstad and Billen, 1994; Verity et al, 2007). Colony formation of Phaeocystis species, including P. antarctica and P. globosa, has been linked to numerous physiological triggers including the synergistic effects of iron and irradiance (Feng et al, 2010), grazer-induced chemical cues (Long et al, 2007), phosphate concentrations (Riegman et al, 1992), and the presence of different nitrogen species (Riegman and van Boekel, 1996; Smith et al, 2003)
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