Embryo fossilization is a biological process mediated by microbial biofilms.
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.
Raff
Elizabeth C
EC
Department of Biology and Indiana Molecular Biology Institute, Indiana University, Bloomington, IN 47405, USA. raff@indiana.edu
Schollaert
Kaila L
KL
Nelson
David E
DE
Donoghue
Philip C J
PC
Thomas
Ceri-Wyn
CW
Turner
F Rudolf
FR
Stein
Barry D
BD
Dong
Xiping
X
Bengtson
Stefan
S
Huldtgren
Therese
T
Stampanoni
Marco
M
Chongyu
Yin
Y
Raff
Rudolf A
RA
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
D004269:DNA, Bacterial; D008903:Minerals