Unlocking Phytoplankton Metallomes with Comparative Analysis of Metal Quotas, Quantitative Proteomics, and Inferred Metalloproteomes

Metalloproteins,
which can bind with one or more metals, are the
basis of many important biological processes in a marine environment.
The metalloproteome data for phytoplankton are limited, hindering
our understanding of trace metal requirements and their biological
function in these primary producers. Here, we conducted a semiquantitative
analysis of metal requirements using a protein modeling approach across
several phytoplankton species, including the chlorophytes Ostreococcus tauri and Chlamydomonas
reinhardtii, the haptophyte Geophyracapsa
huxleyi, and the cyanobacterium Synechocystis. Our results show strong alignment between trace metal requirements
inferred from the proteome and those measured by ICP-MS, with the
metalloproteome providing deeper insights into the biological roles
of each metal compared with ICP-MS, which indicates only cellular
metal abundance. Among all metalloproteins, those containing Mg are
the most abundant in all phytoplankton studied here. Among the trace
elements, Zn, Fe, and Mn are the most abundant cofactors found in
phytoplankton proteins. The cyanobacterium has a much higher percentage
of Fe in its expressed proteome compared to the eukaryotes studied
here, agreeing with findings from previous comparative genomic studies
that trace element requirements are different in prokaryotic and eukaryotic
phytoplankton. Using G. huxleyi strains
from distinct oceanic environments, we further demonstrated that their
metalloproteome can be used to identify limiting metals and understand
the strategies that phytoplankton use to adapt to specific environments.
These findings enhance our understanding of the interactions between
biota and their metal environments.