Declining metal availability in the Mesozoic seawater reflected in phytoplankton succession

Variable trace metal concentrations in the Precambrian ocean were closely linked to oxygen availability, although less is known about the drivers of seawater trace metal chemistry after the spread of complex life into the Phanerozoic eon. A major phytoplankton succession took place at the transition from the Palaeozoic to the Mesozoic era (~250 Myr ago), from an ocean dominated by the green Archaeplastida to secondary endosymbiotic algae with red-algal-derived plastids. Here, our comparative genomic analysis of 26 complete proteomes and metal domain analysis of additional 608 partially complete sequences of phytoplankton reveal that groups with different evolutionary history have distinct metal-binding proteins and contrasting metal acquisition strategies, adapted to differing availability of trace metals. The secondary-endosymbiont-bearing lineages are better adapted to well-oxygenated, nutrient-poor environments. This is supported by an enhanced thiol-based binding affinity of their transporters, coupled with minimized proteomic requirement for trace elements such as iron, copper and zinc at both protein and domain levels. Such different metal requirements across these lineages suggest a drastic decline in open-ocean trace metal concentrations at the inception of the Mesozoic, contributing to the shifts in phytoplankton communities that drove major changes in ocean chemical buffering.