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Influence of cobalamin scarcity on diatom molecularphysiology and identification of a cobalaminacquisition protein
From Erin M. Bertranda,b,1, Andrew E. Allenc, Christopher L. Dupontc, Trina M. Norden-Krichmarc, Jing Baic, Ruben E. Valasc,
and Mak A. Saitoa,2
Diatoms are responsible for ∼40% of marine primary production
and are key players in global carbon cycling. There is mounting
evidence that diatom growth is influenced by cobalamin (vitamin
B12) availability. This cobalt-containing micronutrient is only produced
by some bacteria and archaea but is required by many diatoms
and other eukaryotic phytoplankton. Despite its potential
importance, little is known about mechanisms of cobalamin acquisition
in diatoms or the impact of cobalamin scarcity on diatom
molecular physiology. Proteomic profiling and RNA-sequencing
transcriptomic analysis of the cultured diatoms Phaeodactylum tricornutum
and Thalassiosira pseudonana revealed three distinct
strategies used by diatoms to cope with low cobalamin: increased
cobalamin acquisition machinery, decreased cobalamin demand,
and management of reduced methionine synthase activity through
changes in folate and S-adenosyl methionine metabolism. One previously
uncharacterized protein, cobalamin acquisition protein 1
(CBA1), was up to 160-fold more abundant under low cobalamin
availability in both diatoms. Autologous overexpression of CBA1
revealed association with the outside of the cell and likely endoplasmic
reticulum localization. Cobalamin uptake rates were elevated in
strains overexpressing CBA1, directly linking this protein to cobalamin
acquisition. CBA1 is unlike characterized cobalamin acquisition
proteins and is the only currently identified algal protein known to
be implicated in cobalamin uptake. The abundance andwidespread
distribution of transcripts encoding CBA1 in environmental samples
suggests that cobalamin is an important nutritional factor for
phytoplankton. Future study of CBA1 and other molecular signatures
of cobalamin scarcity identified here will yield insight into
the evolution of cobalamin utilization and facilitatemonitoring of
cobalamin starvation in oceanic diatom communities.
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