Physiological, Ecological, and Evolutionary Studies of Trace Metal Homeostasis in Marine Microbes

Trace metals are important for the catalytic function and proper folding of many proteins, and the complement of trace metals required by an organism depends upon the complement of metal-binding proteins, or metallo-enzymes required. As a result of oxygenic photosynthesis, trace metal bioavailability changed dramatically during the late Archaean and Early Proterozoic, theoretically influencing the biological selection of trace metals for usage. Here several linkages are made between modern physiology, ecology, and genetics and the environmental changes induced by the great oxygenation event. Across all of life, Prokaryotic proteomes are shown to contain more Fe, Mn, and Co-binding proteins, whereas Eukaryotic proteomes are comparatively rich in Zn-binding proteins, trends consistent with the hypothesized changes in trace metal bioavailabilty. The phylogenomic distribution of the gene (sodN) coding for one oxygen-prompted enzymatic innovation, Ni-SOD, reveals a proliferation in marine microbles, particularly in the cyanobacteria, through horizontal gene transfer at the expense of a gene, sodB, that codes for an Fe-SOD. The exchange of a Ni-SOD for Fe-SOD may reduce Fe requirements, a valuable adaptation to the oxygen-induced drop in Fe availability. Consequently, some marine Synechococcus have an obligate requirement for Ni, and these strains control Ni uptake and assimilation through the feedback regulation of a Ni transporter likely acquired during the same transfer event begetting sodN. Possibly as a consequence of the usage of Ni-SOD, Ni appeared to limit cyanobacterial growth in the surface waters of the Gulf of California. Separately, off the coast of Peru where low Fe concentrations limit phytoplankton growth, a diatom-dominated community was unable to utilize added urea for growth unless Ni was added concurrently, a biochemical limitation related to the usage of a Ni-containing urease. Despite nanomolar Ni concentrations in Peru, biophysical modeling implies that the low Fe concentrations result in a saturation of the diatom cell surface with transporters, limiting the uptake of Ni and potentially other metals.