title: 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.
authors.affiliation: Department of Biology and Indiana Molecular Biology Institute, Indiana University, Bloomington, IN 47405, USA. raff@indiana.edu
authors.forename: Elizabeth C
authors.initials: EC
authors.lastname: Raff
authors.forename: Kaila L
authors.initials: KL
authors.lastname: Schollaert
authors.forename: David E
authors.initials: DE
authors.lastname: Nelson
authors.forename: Philip C J
authors.initials: PC
authors.lastname: Donoghue
authors.forename: Ceri-Wyn
authors.initials: CW
authors.lastname: Thomas
authors.forename: F Rudolf
authors.initials: FR
authors.lastname: Turner
authors.forename: Barry D
authors.initials: BD
authors.lastname: Stein
authors.forename: Xiping
authors.initials: X
authors.lastname: Dong
authors.forename: Stefan
authors.initials: S
authors.lastname: Bengtson
authors.forename: Therese
authors.initials: T
authors.lastname: Huldtgren
authors.forename: Marco
authors.initials: M
authors.lastname: Stampanoni
authors.forename: Yin
authors.initials: Y
authors.lastname: Chongyu
authors.forename: Rudolf A
authors.initials: RA
authors.lastname: Raff
mesh_terms: D000332:Aerobiosis; D000693:Anaerobiosis; D000818:Animals; D047329:Anthocidaris / Q000196:embryology; D001329:Autolysis; D001419:Bacteria / Q000235:genetics / Q000254:growth & development*; D018441:Biofilms; D005075:Biological Evolution; D004269:DNA, Bacterial; D004625:Embryo, Nonmammalian / Q000382:microbiology* / Q000648:ultrastructure; D005580:Fossils; D008854:Microscopy, Electron; D008903:Minerals
chemical_list: D004269:DNA, Bacterial; D008903:Minerals