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The Role of Biology in the Fossilization of Embryos and Other Soft-Bodied Organisms: Microbial Biofilms and Lagerstätten

Published online by Cambridge University Press:  21 July 2017

Rudolf A. Raff
Affiliation:
Department of Biology, Indiana University, 150 Myers Hall, 915 E. Third Street, Bloomington, IN 47405 USA
Elizabeth C. Raff
Affiliation:
School of Biological Sciences, University of Sydney, Sydney, NSW 2006, Australia
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Abstract

Soft-tissue fossils are among the most striking and informative remains of extinct organisms. Although relatively rare, they are diverse, ranging from single microbial cells to nuclei and chromosomes; algae; metazoan embryos and larvae; flowers; complete, small, soft-bodied metazoans, metazoan tissues; integumentary structures such as melanosomes; skin texture, vertebrate feathers and hair, insect wings with color patterns, and sometimes even the entire bodies of large animals. The susceptibility of newly dead soft tissues to physical destruction, consumption, and microbial decay makes their preservation unlikely under most taphonomic conditions. In addition, their vulnerability to rapid autolysis, bioturbation, and destructive physical processes requires that rapid biological events must occur as the critical first steps of fossilization. An understanding of the processes by which biological remains enter the fossil record is important in inferring what non-microbial and microbial processes were operative in Lagerstätten. Paleontologists have recognized that microbial biofilms often accompany soft-tissue fossils, and have suggested that bacteria play an active role in soft tissue fossilization, but that role must be determined experimentally with living bacteria and dead tissue.

Marine embryos and marine bacteria are used to investigate the processes that mediate early steps in soft-tissue preservation because they offer simple systems for laboratory investigation of the roles of autolysis-blocking environments, microbial interactions, biofilm formation, and authigenic mineralization in taphonomy. Understanding microbially mediated preservation of embryos may supply new insights into a more general biology of fossilization.

Type
Research Article
Copyright
Copyright © 2014 by The Paleontological Society 

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References

Bailey, J. V., Joye, S. B., Kalanetra, K. M., Flood, B. E., and Corsetti, F. A. 2007. Evidence of giant sulphur bacteria in Neoproterozoic phosphorites. Nature, 445:198201.CrossRefGoogle ScholarPubMed
Barthelemy, R. M., Cuoc, C., Caubit, X., and Brunet, M. 2001. The shell glands in some calanoid copepods (Crustacea). Canadian Journal of Zoology-Revue Canadienne De Zoologie, 79:14901502.Google Scholar
Bengtson, S., Cunningham, J. A., Yin, C. Y., and Donoghue, P. C. J. 2012. A merciful death for the “earliest bilaterian,” Vernanimalcula . Evolution & Development, 14:421427.Google Scholar
Bengtson, S., and Zhao, Y. 1997. Fossilized metazoan embryos from the earliest Cambrian. Science, 277:16451648.Google Scholar
Briggs, D. E. G. 2003. The role of decay and mineralization in the preservation of soft-bodied fossils. Annual Review of Earth and Planetary Sciences, 31:275301.Google Scholar
Briggs, D. E. G. and Kear, A. J. 1994. Decay and mineralization of shrimps. PALAIOS, 9:431456.Google Scholar
Briggs, D. E. G., Kear, A. J., Martill, D. M., and Wilby, P. R. 1993. Phosphatization of soft-tissue in experiments and fossils. Journal of the Geological Society, 150:10351038.Google Scholar
Briggs, D. E., Moore, R. A., Shultz, J. W., and Schweigert, G. 2005. Mineralization of soft-part anatomy and invading microbes in the horseshoe crab Mesolimulus from the Upper Jurassic Lagerstatte of Nusplingen, Germany. Proceedings of the Royal Society of London Series B-Biological Sciences, 272:627632.Google ScholarPubMed
Broce, J., Schiffbauer, J. D., Sen Sharma, K., Wang, G., and Xiao, S. H. 2014. Possible animal embryos from the Lower Cambrian (Stage 3) Shuijingtuo Formation, Hubei Province, South China. Journal of Paleontology, 88:385394.Google Scholar
Brown, G. G., and Humphreys, W. 1971. Sperm-egg interactions of Limulus polyphemus with scanning electron microscopy. Journal of Cell Biology, 51:904907.Google Scholar
Chang, J. Y. 1997. A two-stage mechanism for the reductive unfolding of disulfide-containing proteins. Journal of Biological Chemistry, 272:6975.Google Scholar
Chen, J. Y., Bottjer, D. J., Li, G., Hadfield, M. G., Gao, F., Cameron, A. R., Zhang, C. Y., Xian, D. C., Tafforeau, P., Liao, X., and Yin, Z. J. 2009. Complex embryos displaying bilaterian characters from Precambrian Doushantuo phosphate deposits, Weng'an, Guizhou, China. Proceedings of the National Academy of Sciences of the United States of America, 106:1905619060.Google Scholar
Chen, J. Y., Bottjer, D. J., Oliveri, P., Dornbos, S. Q., Gao, F., Ruffins, S., Chi, H. M., Li, C. W., and Davidson, E. H. 2004. Small bilaterian fossils from 40 to 55 million years before the Cambrian. Science, 305:218222.Google Scholar
Cunningham, J. A., Thomas, C. W., Bengtson, S., Kearns, S. L., Xiao, S. H., Marone, F., Stampanoni, M., and Donoghue, P. C. J. 2012a. Distinguishing geology from biology in the Ediacaran Doushantuo biota relaxes constraints on the timing of the origin of bilaterians. Proceedings of the Royal Society of London B-Biological Sciences, 279:23692376.CrossRefGoogle ScholarPubMed
Cunningham, J. A., Thomas, C. W., Bengtson, S., Marone, F., Stampanoni, M., Turner, F. R., Bailey, J. V., Raff, R. A., Raff, E. C., and Donoghue, P. C. 2012b. Experimental taphonomy of giant sulphur bacteria: implications for the interpretation of the embryo-like Ediacaran Doushantuo fossils. Proceedings of the Royal Society of London Series B-Biological Sciences, 279:18571864.Google Scholar
Daniel, J. C., and Chin, K. 2010. The role of bacterially mediated precipitation in the permineralization of bone. PALAIOS, 25:507516.Google Scholar
Darroch, S. A. F., Laflamme, M., Schiffbauer, J. D., and Briggs, D. E. G. 2012. Experimental formation of a microbial death mask. PALAIOS, 27:293303.Google Scholar
Davis, P. G., and Briggs, D. E. G. 1995. Fossilization of feathers. Geology, 23:783786.Google Scholar
Dong, X. P., Cunningham, J. A., Bengtson, S., Thomas, C. W., Liu, J. B., Stampanoni, M., and Donoghue, P. C. J. 2013. Embryos, polyps and medusae of the Early Cambrian scyphozoan Olivooides . Proceedings of the Royal Society of London B-Biological Sciences, 280:20130071.Google Scholar
Dong, X. P., Donoghue, P. C. J., Cheng, H., and Liu, J. B. 2004. Fossil embryos from the Middle and Late Cambrian period of Hunan, South China. Nature, 427:237240.Google Scholar
Donlan, R. M. 2002. Biofilms: Microbial life on surfaces. Emerging Infectious Diseases, 8:881890.Google Scholar
Donoghue, P. C. J., Kouchinsky, A., Waloszek, D., Bengtson, S., Dong, X. P., Val'kov, A. K., Cunningham, J. A., and Repetski, J. E. 2006. Fossilized embryos are widespread but the record is temporally and taxonomically biased. Evolution & Development, 8:232238.Google Scholar
Farmer, A. S. D. 1974. Reproduction in Nephrops norvegicus (Decapoda-Nephropidae). Journal of Zoology, 174:161183.Google Scholar
Gehling, J. G. 1999. Microbial mats in terminal Proterozoic siliciclastics: Ediacaran death masks. PALAIOS, 14:4057.Google Scholar
Gilchrist, B. M. 1978. Scanning electron-microscope studies of egg-shell in some Anostraca (Crustacea-Branchiopoda). Cell and Tissue Research, 193:337351.CrossRefGoogle Scholar
Gostling, N. J., Dong, X. P., and Donoghue, P. C. J. 2009. Ontogeny and taphonomy: An experimental taphonomy study of the development of the brine shrimp Artemia salina . Palaeontology, 52:169186.Google Scholar
Gostling, N. J., Thomas, C. W., Greenwood, J. M., Dong, X., Bengtson, S., Raff, E. C., Raff, R. A., Degnan, B. M., Stampanoni, M., and Donoghue, P. C. 2008. Deciphering the fossil record of early bilaterian embryonic development in light of experimental taphonomy. Evolution & Development, 10:339349.CrossRefGoogle ScholarPubMed
Hagadorn, J. W., Xiao, S., Donoghue, P. C., Bengtson, S., Gostling, N. J., Pawlowska, M., Raff, E. C., Raff, R. A., Turner, F. R., Chongyu, Y., Zhou, C., Yuan, X., McFeely, M. B., Stampanoni, M., and Nealson, K. H. 2006. Cellular and subcellular structure of neoproterozoic animal embryos. Science, 314:291294.Google Scholar
Hendrickson, E. L., Wang, T., Dickinson, B. C., Whitmore, S. E., Wright, C. J., Lamont, R. J., and Hackett, M. 2012. Proteomics of Streptococcus gordonii within a model developing oral microbial community. BMC Microbiology, 12:211. doi:10.1186/1471-2180-12-211 Google Scholar
Huldtgren, T., Cunningham, J. A., Yin, C. Y., Stampanoni, M., Marone, F., Donoghue, P. C. J., and Bengtson, S. 2011. Fossilized nuclei and germination structures identify Ediacaran “animal embryos” as encysting protists. Science, 334:16961699.Google Scholar
Iniesto, M., Lopez-Archilla, A. I., Fregenal-Martinez, M., Buscalioni, A. D., and Guerrero, M. C. 2013. Involvement of microbial mats in delayed decay: An experimental essay on fish preservation. PALAIOS, 28:5666.CrossRefGoogle Scholar
James, G. A., Swogger, E., Wolcott, R., Pulcini, E. D., Secor, P., Sestrich, J., Costerton, J. W., and Stewart, P. S. 2008. Biofilms in chronic wounds. Wound Repair and Regeneration, 16:3744.CrossRefGoogle ScholarPubMed
Laflamme, M., Schiffbauer, J. D., Narbonne, G. M., and Briggs, D. E. G. 2011. Microbial biofilms and the preservation of the Ediacara biota. Lethaia, 44:203213.Google Scholar
Love, G. D., Grosjean, E., Stalvies, C., Fike, D. A., Grotzinger, J. P., Bradley, A. S., Kelly, A. E., Bhatia, M., Meredith, W., Snape, C. E., Bowring, S. A., Condon, D. J., and Summons, R. E. 2009. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature, 457:718722.Google Scholar
Maas, A., Braun, A., Dong, X.-P., Donoghue, P. C. J., Müller, K. J., Olempska, E., Repetski, J. E., Siveter, D. J., Stein, M., and Waloszek, D. 2006. The ‘Orsten’—More than a Cambrian Konservat-Lagerstätte yielding exceptional preservation. Paleoworld, 15:266282.Google Scholar
Martill, D. M. 2003. The Santana Formation, p. 351356. In Briggs, D. E. G. and Crowther, P. R. (eds.), Paleobiology II. Blackwell Publishing, Ltd., Oxford, UK.Google Scholar
Martin, D., Briggs, D. E. G., and Parkes, R. J. 2005. Decay and mineralization of invertebrate eggs. PALAIOS, 20:562572.CrossRefGoogle Scholar
Matzke-Karasz, R., Neil, J. V., Smith, R. J., Symonova, R., Morkovsky, L., Archer, M., Hand, S. J., Cloetens, P., and Tafforeau, P. 2014. Subcellular preservation in giant ostracod sperm from an early Miocene cave deposit in Australia. Proceedings of the Royal Society of London Series B-Biological Sciences, 281:20140394. doi:10.1098/rspb.2014.0394 Google Scholar
McCarty, S. M., Cochrane, C. A., Clegg, P. D., and Percival, S. L. 2012. The role of endogenous and exogenous enzymes in chronic wounds: A focus on the implications of aberrant levels of both host and bacterial proteases in wound healing. Wound Repair and Regeneration, 20:125136.Google Scholar
McCobb, L. M. E., Briggs, D. E. G., Hall, A. R., and Kenward, H. K. 2004. The preservation of invertebrates in 16th century cesspits at St Saviourgate, York. Archaeometry, 46:157169.Google Scholar
McNamara, M. E., Orr, P. J., Alcala, L., Anadon, P., and Penalver, E. 2012. What controls the taphonomy of exceptionally preserved taxa—environment or biology? A case study using frogs from the Miocene Libros Konservat-Lagerstatte (Teruel, Spain). PALAIOS, 27:6377.Google Scholar
McNamara, M. E., Orr, P. J., Kearns, S. L., Alcala, L., Anadon, P., and Penalver-Molla, E. 2009. Soft-tissue preservation in Miocene frogs from Libros, Spain: Insights into the genesis of decay microenvironments. PALAIOS, 24:104117.Google Scholar
McNamara, M. E., Orr, P. J., Kearns, S. L., Alcala, L., Anadon, P., and Penalver-Molla, E. 2010a. Exceptionally preserved tadpoles from the Miocene of Libros, Spain: ecomorphological reconstruction and the impact of ontogeny upon taphonomy. Lethaia, 43:290306.CrossRefGoogle Scholar
McNamara, M., Orr, P. J., Kearns, S. L., Alcala, L., Anadon, P., and Penalver-Molla, E. 2010b. Organic preservation of fossil musculature with ultracellular detail. Proceedings of the Royal Society of London Series B-Biological Sciences, 277:423427.Google Scholar
Mindrinos, M. N., Petri, W. H., Galanopoulos, V. K., Lombard, M. F., and Margaritis, L. H. 1980. Crosslinking of the Drosophila chorion involves a peroxidase. Wilhelm Rouxs Archives of Developmental Biology, 189:187196.Google Scholar
Nobbs, A. H., Lamont, R. J., and Jenkinson, H. F. 2009. Streptococcus adherence and colonization. Microbiology and Molecular Biology Reviews, 73:407450.Google Scholar
Nutzel, A., Lehnert, O., and Fryda, J. 2006. Origin of planktotrophy—evidence from early molluscs. Evolution & Development, 8:325330.CrossRefGoogle ScholarPubMed
O'Brien, N. R., Meyer, H. W., and Harding, I. C. 2008. The role of biofilms in fossil preservation, Florissant Formation, Colorado, p. 1931. In Meyer, H. W. and Smith, D. M. (eds.), Paleontology of the Upper Eocene Florissant Formation, Colorado. Geological Society of America Special Paper 435, The Geological Society of America, Boulder, CO.Google Scholar
Pang, K., Tang, Q., Schiffbauer, J. D., Yao, J., Yuan, X., Wan, B., Chen, L., Ou, Z., and Xiao, S. 2013. The nature and origin of nucleus-like intracellular inclusions in Paleoproterozoic eukaryote microfossils. Geobiology, 11:499510.Google Scholar
Peterson, J. E., Lenczewski, M. E., and Scherer, R. P. 2010. Influence of microbial biofilms on the preservation of primary soft tissue in fossil and extant archosaurs. PloS One, e13334. doi:10.1371/journal.pone.0013334.Google Scholar
Peterson, K. J. 2005. Macroevolutionary interplay between planktic larvae and benthic predators. Geology, 33:929932.CrossRefGoogle Scholar
Pinheiro, F. L., Horn, B. L. D., Schultz, C. L., de Andrade, J. A. F. G., and Sucerquia, P. A. 2012. Fossilized bacteria in a Cretaceous pterosaur headcrest. Lethaia, 45:495499.Google Scholar
Pyle, L. J., Narbonne, G. M., Nowlan, G. S., Xiao, S. H., and James, N. P. 2006. Early Cambrian metazoan eggs, embryos, and phosphatic microfossils from northwestern Canada. Journal of Paleontology, 80:811825.Google Scholar
Raff, E. C., Andrews, M. E., Turner, F. R., Toh, E., Nelson, D. E., and Raff, R. A. 2013. Contingent interactions among biofilm-forming bacteria determine preservation or decay in the first steps toward fossilization of marine embryos. Evolution & Development, 15:243256.Google Scholar
Raff, E. C., Schollaert, K. L., Nelson, D. E., Donoghue, P. C., Thomas, C. W., Turner, F. R., Stein, B. D., Dong, X., Bengtson, S., Huldtgren, T., Stampanoni, M., Chongyu, Y., and Raff, R. A. 2008. Embryo fossilization is a biological process mediated by microbial biofilms. Proceedings of the National Academy of Sciences of the United States of America, 105:1936019365.Google Scholar
Raff, E. C., Villinski, J. T., Turner, F. R., Donoghue, P. C., and Raff, R. A. 2006. Experimental taphonomy shows the feasibility of fossil embryos. Proceedings of the National Academy of Sciences of the United States of America, 103:58465851.Google Scholar
Raff, R. A. 2008. Origins of the other metazoan body plans: the evolution of larval forms. Philosophical Transactions of the Royal Society of London B-Biological Sciences, 363:14731479.Google Scholar
Raff, R. A., Andrews, M. E., Pearson, R. L., Turner, F. R., Saur, S. T., Thomas, D. C., Eagan, J. L., and Raff, E. C. In press. Microbial ecology and biofilms in the taphonomy of soft tissues. PALAIOS.Google Scholar
Sagemann, J., Bale, S. J., Briggs, D. E. G., and Parkes, R. J. 1999. Controls on the formation of authigenic minerals in association with decaying organic matter: An experimental approach. Geochimica Et Cosmochimica Acta, 63:10831095.Google Scholar
Sansom, R. S. 2014. Experimental decay of soft tissues, p. 217236. In Laflamme, M., Schiffbauer, J. D., and Darroch, S. A. F. (eds.), Reading and Writing of the Fossil Record: Preservational Pathways to Exceptional Fossilization. The Paleontological Society Papers 20. Yale Press, New Haven, CT.Google Scholar
Schiffbauer, J. D., and Laflamme, M. 2012. Lagerstatten through time: a collection of exceptional preservational pathways from the terminal Neoproterozoic through today. PALAIOS, 27:275278.Google Scholar
Schiffbauer, J. D., Wallace, A. F., Broce, J., and Xiao, S. 2014. Exceptional fossil conservation through phosphatization, p. 5982. In Laflamme, M., Schiffbauer, J. D., and Darroch, S. A. F. (eds.), Reading and Writing of the Fossil Record: Preservational Pathways to Exceptional Fossilization. The Paleontological Society Papers 20. Yale Press, New Haven, CT.Google Scholar
Schiffbauer, J. D., Xiao, S. H., Sen Sharma, K., and Wang, G. 2012. The origin of intracellular structures in Ediacaran metazoan embryos. Geology, 40:223226.Google Scholar
Schopf, J. M. 1975. Modes of fossil preservation. Review of Paleobotany and Palynology, 20:2753.Google Scholar
Signor, P. W., and Vermeil, G. J. 1994. The plankton and the benthos—origins and early history of an evolving relationship. Paleobiology, 20:297319.Google Scholar
Silas, E. G., Muthu, M. S., Pillai, N. N., and George, K. V. 1979. Larval development—Penaeus monodon Fabricius. CMFRI Bulletin, 28:212.Google Scholar
Siveter, D. J., Siveter, D. J., Sutton, M. D., and Briggs, D. E. G. 2007. Brood care in a Silurian ostracod. Proceedings of the Royal Society B-Biological Sciences, 274:465469.Google Scholar
Siveter, D. J., Tanaka, G., Farrell, U. C., Martin, M. J., Siveter, D. J., and Briggs, D. E. G. 2014. Exceptionally preserved 450-million-year-old Ordovician ostracods with brood care. Current Biology, 24:801806.Google Scholar
Skawina, A. 2010. Experimental decay of gills in freshwater bivalves as a key to understanding their preservation in Upper Triassic lacustrine deposits. PALAIOS, 25:215220.Google Scholar
Steiner, M., and Reitner, J. 2001. Evidence of organic structures in Ediacara-type fossils and associated microbial mats. Geology, 29:11191122.Google Scholar
Steiner, M., Zhu, M., Li, G., Qian, Y., and Erdtmann, B.-D. 2004. New early Cambrian bilaterian embryos and larvae from China. Geology, 32:833836.Google Scholar
Stoodley, P., Sauer, K., Davies, D. G., and Costerton, J. W. 2002. Biofilms as complex differentiated communities. Annual Review of Microbiology, 56:187209.Google Scholar
Toporski, J. K. W., Steele, A., Westall, F., Avci, R., Martill, D. M., and McKay, D. S. 2002. Morphologic and spectral investigation of exceptionally well-preserved bacterial biofilms from the Oligocene Enspel Formation, Germany. Geochimica et Cosmochimica Acta, 66:17731791.Google Scholar
Wang, B., Zhao, F. C., Zhang, H. C., Fang, Y., and Zheng, D. R. 2012. Widespread pyritization of insects in the early Cretaceous Jehol Biota. PALAIOS, 27:708712.Google Scholar
Wong, J. L., and Wessel, G. M. 2004. Major components of a sea urchin block to polyspermy are structurally and functionally conserved. Evolution & Development, 6:134153.Google Scholar
Xiao, S. H., Hagadorn, J. W., Zhou, C. M., and Yuan, X. L. 2007. Rare helical spheroidal fossils from the Doushantuo Lagerstatte: Ediacaran animal embryos come of age? Geology, 35:115118.Google Scholar
Xiao, S. H., and Knoll, A. H. 2000. Phosphatized animal embryos from the Neoproterozoic Doushantuo Formation at Weng'An, Guizhou, South China. Journal of Paleontology, 74:767788.Google Scholar
Xiao, S., Knoll, A. H., Schiffbauer, J. D., Zhou, C., and Yuan, X. 2012. Comment on “Fossilized nuclei and germination structures identify Ediacaran ‘animal embryos’ as encysting protists.” Science, 335:1169.Google Scholar
Xiao, S. H., and Schiffbauer, J. D. 2009. Microfossil phosphatization and its astrobiological implications, p. 89118. In Seckbach, J. and Walsh, M. (eds.), From Fossils to Astrobiology: Cellular Origin, Life in Extreme Habitats and Astrobiology. Springer.Google Scholar
Xiao, S. H., Schiffbauer, J. D., McFadden, K. A., and Hunter, J. 2010. Petrographic and SIMS pyrite sulfur isotope analyses of Ediacaran chert nodules: Implications for microbial processes in pyrite rim formation, silicification, and exceptional fossil preservation. Earth and Planetary Science Letters, 297:481495.Google Scholar
Xiao, S. H., Zhang, Y., and Knoll, A. H. 1998. Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature, 391:553558.Google Scholar
Yin, L. M., Zhu, M. Y., Knoll, A. H., Yuan, X. L., Zhang, J. M., and Hu, J. 2007. Doushantuo embryos preserved inside diapause egg cysts. Nature, 446:661663.Google Scholar