Temporal heterogeneity in the animal fossil record driven by proliferation of microbial collagenases

The animal fossil record is a non-uniform archive of evolutionary history in which exceptional preservation diminishes toward the present,^1,2,3 with biomineralized skeletal elements constituting the majority of the fossil record. Preservation of soft tissues requires rare combinations of chemical, biological, and physical conditions that preclude or delay decay until biological substrates can be geologically stabilized via mineralization or maturation.⁴ However, during the late Ediacaran Period (∼579-539 mya) fossilization of soft-bodied macroorganisms was common across a wide range of depositional settings.^5,6 Taphonomic models seeking to explain Ediacaran exceptionalism typically appeal to unusual mineralogical and geochemical conditions or microbiological influence (e.g., Gehling,⁷ Tarhan et al.,⁸ Bykova et al.,⁹ and Bobrovskiy et al.¹⁰), and the Paleozoic decline in exceptional preservation has invariably been explained in terms of expansion of the oxic zone through metazoan bioturbation (though see Cribb et al.¹¹) and enhanced scavenging.¹² We explore the hypothesis that temporal heterogeneity in metazoan exceptional preservation is a consequence of the origin and/or proliferation of microbial collagenases.¹³ Collagenase gene trees reconciled with a time-calibrated phylogeny show that collagenases arose and were produced by obligate anaerobes billions of years before proliferating by lateral gene transfer, approximately coincident with the diversification of early animals. These results support a link between the evolution of collagenases, animals, and the non-uniformity of the fossil record. Proliferation of collagenase-producing microbial lineages occurred in concert with early animal evolution. Evidence also indicates a shift in the locus of collagen degradation within the sediment redox profile, coincident with the decline of exceptional soft-tissue preservation in the marine realm.