Colony formation in Phaeocystis antarctica: connecting molecular mechanisms with iron biogeochemistry
Authors: Bender Sara J. , Moran Dawn M. , McIlvin Matthew R. , Zheng Hong , McCrow John P. , Badger Jonathan , DiTullio Giacomo R. , Allen Andrew E. , Saito Mak A. 
Published: August 2018

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.