Reconstructed ancestral enzymes suggest long-term cooling of Earth's photic zone since the Archean

Paleotemperatures inferred from the isotopic compositions (delta O-18 and delta Si-30) of marine cherts suggest that Earth's oceans cooled from 70 +/- 15 degrees C in the Archean to the present similar to 15 degrees C. This interpretation, however, has been subject to question due to uncertainties regarding oceanic isotopic compositions, diagenetic or metamorphic resetting of the isotopic record, and depositional environments. Analyses of the thermostability of reconstructed ancestral enzymes provide an independent method by which to assess the temperature history inferred from the isotopic evidence. Although previous studies have demonstrated extreme thermostability in reconstructed archaeal and bacterial proteins compatible with a hot early Earth, taxa investigated may have inhabited local thermal environments that differed significantly from average surface conditions. We here present thermostability measurements of reconstructed ancestral enzymatically active nucleoside diphosphate kinases (NDKs) derived from light-requiring prokaryotic and eukaryotic phototrophs having widely separated fossil-based divergence ages. The ancestral environmental temperatures thereby determined for these photic-zone organisms-shown in modern taxa to correlate strongly with NDK thermostability-are inferred to reflect ancient surface-environment paleotemperatures. Our results suggest that Earth's surface temperature decreased over geological time from similar to 65-80 degrees C in the Archean, a finding consistent both with previous isotope-based and protein reconstruction-based interpretations. Interdisciplinary studies such as those reported here integrating genomic, geologic, and paleontologic data hold promise for providing new insight into the coevolution of life and environment over Earth history.