CHLOROPLASTS, MITOCHONDRIA, AND THE EUKARYOTIC PRESENCE IN PROTEROZOIC OCEANS

In eukaryotic cells, the principal organelles of energy metabolism derive from once independent bacteria, captured during the Proterozoic Eon as endosymbionts and subsequently reduced to metabolic slavery. These events are generally (and rightly) viewed as keys to the evolutionary success of the domain, but in Proterozoic oceans they may have proved a mixed blessing. Increasing geochemical data support the view that for much of the Proterozoic Eon, modestly oxic surface waters lay above an oxygen minimum zone that tended toward euxinia. Under these conditions, fixed nitrogen would have been limited within the mixed layer. Eukaryotes gained the ability to photosynthesize from cyanobacterial endosymbionts, but the capacity to fix nitrogen was not transferred. Thus, in the photic zone of Proterozoic oceans, ecological advantage would accrue to photosynthetic bacteria capable of nitrogen fixation. Mitochondrial function may also have been compromised in Proterozoic oceans because sulfide interferes with cytochrome c oxidase, inhibiting respiration. In Proterozoic oceans, therefore, where the threat of upward mixing sulfide was real and persistent, eukaryotes may have been challenged in most marine environments, leaving fresh waters and coastal marine environments as likely spots for early diversification. New geochemical data suggest that the oceans began the long transition to their modern, fully oxic state about 800 million years ago, when sulfide began to retreat in subsurface water masses. Consistent with expected the physiological consequences of such a transition, fossils show a marked increase in the diversity and environmental amplitude of eukaryotic organisms at this time. Molecular biomarkers independently suggest an enhanced ecological importance of marine eukaryotes after 800 Ma. Thus, the tremendous physiological possibilities conferred by endosymbiotically acquired organelles may have realized their full ecological and evolutionary potential long after the origin of eukaryotic cells, as changing ocean chemistry opened a broad range of marine environments to colonization by eukaryotes capable of aerobic respiration and, in some cases, photosynthesis.