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.