Literature DB >> 19047625

Embryo fossilization is a biological process mediated by microbial biofilms.

Elizabeth C Raff1, Kaila L Schollaert, David E Nelson, Philip C J Donoghue, Ceri-Wyn Thomas, F Rudolf Turner, Barry D Stein, Xiping Dong, Stefan Bengtson, Therese Huldtgren, Marco Stampanoni, Yin Chongyu, Rudolf A Raff.   

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.

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Year:  2008        PMID: 19047625      PMCID: PMC2614766          DOI: 10.1073/pnas.0810106105

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  12 in total

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Journal:  Nat Rev Microbiol       Date:  2004-02       Impact factor: 60.633

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Journal:  Proc Biol Sci       Date:  2005-03-22       Impact factor: 5.349

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Review 4.  Microbial lithification in marine stromatolites and hypersaline mats.

Authors:  Christophe Dupraz; Pieter T Visscher
Journal:  Trends Microbiol       Date:  2005-09       Impact factor: 17.079

5.  Experimental taphonomy shows the feasibility of fossil embryos.

Authors:  Elizabeth C Raff; Jeffrey T Villinski; F Rudolf Turner; Philip C J Donoghue; Rudolf A Raff
Journal:  Proc Natl Acad Sci U S A       Date:  2006-03-29       Impact factor: 11.205

6.  Synchrotron X-ray tomographic microscopy of fossil embryos.

Authors:  Philip C J Donoghue; Stefan Bengtson; Xi-ping Dong; Neil J Gostling; Therese Huldtgren; John A Cunningham; Chongyu Yin; Zhao Yue; Fan Peng; Marco Stampanoni
Journal:  Nature       Date:  2006-08-10       Impact factor: 49.962

7.  Cellular and subcellular structure of neoproterozoic animal embryos.

Authors:  James W Hagadorn; Shuhai Xiao; Philip C J Donoghue; Stefan Bengtson; Neil J Gostling; Maria Pawlowska; Elizabeth C Raff; Rudolf A Raff; F Rudolf Turner; Yin Chongyu; Chuanming Zhou; Xunlai Yuan; Matthew B McFeely; Marco Stampanoni; Kenneth H Nealson
Journal:  Science       Date:  2006-10-13       Impact factor: 47.728

8.  Deciphering the fossil record of early bilaterian embryonic development in light of experimental taphonomy.

Authors:  Neil J Gostling; Ceri-Wyn Thomas; Jenny M Greenwood; Xiping Dong; Stefan Bengtson; Elizabeth C Raff; Rudolf A Raff; Bernard M Degnan; Marco Stampanoni; Philip C J Donoghue
Journal:  Evol Dev       Date:  2008 May-Jun       Impact factor: 1.930

9.  Fossil preservation in the Neoproterozoic Doushantuo phosphorite Lagerstatte, South China.

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Journal:  Lethaia       Date:  1999-09       Impact factor: 2.247

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  13 in total

1.  Experimental taphonomy of giant sulphur bacteria: implications for the interpretation of the embryo-like Ediacaran Doushantuo fossils.

Authors:  J A Cunningham; C-W Thomas; S Bengtson; F Marone; M Stampanoni; F R Turner; J V Bailey; R A Raff; E C Raff; P C J Donoghue
Journal:  Proc Biol Sci       Date:  2011-12-07       Impact factor: 5.349

2.  Distinguishing geology from biology in the Ediacaran Doushantuo biota relaxes constraints on the timing of the origin of bilaterians.

Authors:  John A Cunningham; Ceri-Wyn Thomas; Stefan Bengtson; Stuart L Kearns; Shuhai Xiao; Federica Marone; Marco Stampanoni; Philip C J Donoghue
Journal:  Proc Biol Sci       Date:  2012-02-08       Impact factor: 5.349

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

Authors:  Alan Pradel; Max Langer; John G Maisey; Didier Geffard-Kuriyama; Peter Cloetens; Philippe Janvier; Paul Tafforeau
Journal:  Proc Natl Acad Sci U S A       Date:  2009-03-09       Impact factor: 11.205

4.  Bacterial community associated with healthy and diseased reef coral Mussismilia hispida from eastern Brazil.

Authors:  Alinne Pereira de Castro; Samuel Dias Araújo; Alessandra M M Reis; Rodrigo L Moura; Ronaldo B Francini-Filho; Georgios Pappas; Thiago Bruce Rodrigues; Fabiano L Thompson; Ricardo H Krüger
Journal:  Microb Ecol       Date:  2010-03-30       Impact factor: 4.552

5.  Influence of microbial biofilms on the preservation of primary soft tissue in fossil and extant archosaurs.

Authors:  Joseph E Peterson; Melissa E Lenczewski; Reed P Scherer
Journal:  PLoS One       Date:  2010-10-12       Impact factor: 3.240

6.  Tiny sea anemone from the Lower Cambrian of China.

Authors:  Jian Han; Shin Kubota; Hiro-omi Uchida; George D Stanley; Xiaoyong Yao; Degan Shu; Yong Li; Kinya Yasui
Journal:  PLoS One       Date:  2010-10-13       Impact factor: 3.240

7.  Experimental taphonomy of Artemia reveals the role of endogenous microbes in mediating decay and fossilization.

Authors:  Aodhán D Butler; John A Cunningham; Graham E Budd; Philip C J Donoghue
Journal:  Proc Biol Sci       Date:  2015-06-07       Impact factor: 5.349

8.  Mineralization of Alvinella polychaete tubes at hydrothermal vents.

Authors:  M N Georgieva; C T S Little; A D Ball; A G Glover
Journal:  Geobiology       Date:  2014-12-30       Impact factor: 4.407

9.  Involvement of microbial mats in early fossilization by decay delay and formation of impressions and replicas of vertebrates and invertebrates.

Authors:  Miguel Iniesto; Ángela D Buscalioni; M Carmen Guerrero; Karim Benzerara; David Moreira; Ana I López-Archilla
Journal:  Sci Rep       Date:  2016-05-10       Impact factor: 4.379

10.  First Record of Soft Tissue Preservation in the Upper Devonian of Poland.

Authors:  Michał Zatoń; Krzysztof Broda
Journal:  PLoS One       Date:  2015-11-11       Impact factor: 3.240

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