Embryo fossilization is a biological process mediated by microbial biofilms

Abstract

Fossilized embryos with extraordinary cellular preservation appear in the Late Neoproterozoic and Cambrian, coincident with the appearance of animal body fossils. It has been hypothesized that microbial processes are responsible for preservation and mineralization of organic tissues. However, the actions of microbes in preservation of embryos have not been demonstrated experimentally. Here, we show that bacterial biofilms assemble rapidly in dead marine embryos and form remarkable pseudomorphs in which the bacterial biofilm replaces and exquisitely models details of cellular organization and structure. The experimental model was the decay of cleavage stage embryos similar in size and morphology to fossil embryos. The data show that embryo preservation takes place in 3 distinct steps: (i) blockage of autolysis by reducing or anaerobic conditions, (ii) rapid formation of microbial biofilms that consume the embryo but form a replica that retains cell organization and morphology, and (iii) bacterially catalyzed mineralization. Major bacterial taxa in embryo decay biofilms were identified by using 16S rDNA sequencing. Decay processes were similar in different taphonomic conditions, but the composition of bacterial populations depended on specific conditions. Experimental taphonomy generates preservation states similar to those in fossil embryos. The data show how fossilization of soft tissues in sediments can be mediated by bacterial replacement and mineralization, providing a foundation for experimentally creating biofilms from defined microbial species to model fossilization as a biological process.bacterial ͉ developmental evolution ͉ metazoan origins ͉ taphonomy ͉ Cambrian

Skull and brain of a 300-million-year-old chimaeroid fish revealed by synchrotron holotomography

“…Its shape, symmetry, and relations to the nerve foramina strongly suggest that it is an exceptionally preserved trace of the actual brain rather than a fortuitous artifact. This peculiar case of mineralization may be explained by the fact that the brain underwent microbially induced phosphatization shortly before decay (16,17). This could have been favored by locally anoxic conditions inside the braincase and an environment probably saturated with calcium phosphate (hence the concretions).…”

The Weng'an Biota (Doushantuo Formation): an Ediacaran window on soft-bodied and multicellular microorganisms

“…Experiments have shown that animal embryos have a relatively high preservation potential, particularly when enclosed in a fertilization envelope, whereas primary larvae have an extremely low likelihood of being preserved (Raff et al 2006;Gostling et al 2008Gostling et al , 2009). In addition, these experiments have identified the likely mechanism for Doushantuo-type preservation: 3D replication of cells by robust bacterial pseudomorphs followed by phosphate mineralization (Raff et al 2008). The diagenetic and subsequent geological processes that the fossil is subjected to can introduce artefacts (e.g.…”

A role for iron and oxygen chemistry in preserving soft tissues, cells and molecules from deep time

“…This 'exceptional preservation' has been observed for decades, but is not addressed by models of fossilization processes wherein an organism is buried and degraded, and spaces left by degrading organics are subsequently filled by precipitation of exogenous minerals. Modes of preservation to explain the persistence of these secondarily mineralized, but originally soft tissues include microbially mediated stabilization [6,7], early diagenetic mineralization or authigenic replacement [8][9][10], 'sulfurization' [11,12] and others (reviewed in [6,13,14]), but few of these preservation modes have been experimentally tested.…”