The Grand Unified Theory of Biomineralization: New Evidence from the Great Oxygenation Event Suggests That “Iron Is Master of Them All.”

Although major animal phyla diverged earlier, the ~550 – 520 Ma “Cambrian Explosion” marks the widespread advent of carbonate and phosphate biomineralization, either triggered by an unprecedented lateral genetic transfer or by parallel exaptation of an ancestral biomineralization system in the many separate lineages. The “Grand Unified Theory of Biomineralization” hypothesizes that, because magnetite (Fe₃O₄) biomineralization appears to be the most ancient matrix-mediated biomineral system and is present in most animal groups, its genes served as an ancestral template for exaptation when selection pressures ultimately favored biomineral shells and exoskeletons. This template might have been inherited from an alpha-Proteobacterial ancestor during mitochondrial endosymbiosis in the ancestral eukaryotic lineage.

It long has been thought that mitochondrial endosymbiosis was driven by an increase in oxygen in the Earth's atmosphere. This hypothesis is gaining support as geological age constraints on the “Great Oxygenation Event” (a.k.a. “Oxyatmoversion”) and molecular clock estimates for the origin of mitochondria converge on the same interval somewhat older than 2 billion years ago. This still-imprecisely delineated interval also hosts a remarkable, >160 million year-long positive excursion in the carbon isotopic record of marine carbonates known as the Lomagundi-Jatuli event. We hypothesize that the duration of this excursion represents the time over which respiratory efficiency increased to ultimately match productivity of oxygenic phototrophs.

Mitochondria evolved from an ancestral member of the Rickettsia group, an early-diverging group in the alpha-Proteobacteria. The only group to diverge more basally is composed entirely of magnetotactic members, including the sequenced Magnetococcus marinus MC-1. We suggest that radiation of this magnetotactic bacterial group immediately prior to the evolution of mitochondria indicates that part of the genetic machinery involved in magnetotaxis evolved at this time and may have facilitated mitochondrial endosymbiosis.