Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-03T01:03:24.418Z Has data issue: false hasContentIssue false
  • English
  • Français

Identification of chitin in 200-million-year-old gastropod egg capsules

Published online by Cambridge University Press:  08 April 2016

Marcin Wysokowski ,
Michał Zatoń ,
Vasilii V. Bazhenov ,
Thomas Behm ,
Andre Ehrlich ,
Allison L. Stelling ,
Martin Hog  and
Hermann Ehrlich
Marcin Wysokowski
Affiliation:
Poznań University of Technology, Institute of Chemical Technology and Engineering, M. Skłodowskiej-Curie 2, PL-60965 Poznan, Poland
Michał Zatoń*
Affiliation:
University of Silesia, Faculty of Earth Sciences, Department of Paleontology and Stratigraphy, Będzińska 60, PL-41-200 Sosnowiec, Poland. E-mail: [email protected]
Vasilii V. Bazhenov
Affiliation:
TU Bergakademie Freiberg, Institute of Experimental Physics, Leipziger Straße 23, 09599 Freiberg, Germany. E-mail: [email protected]
Thomas Behm
Affiliation:
TU Bergakademie Freiberg, Institute of Experimental Physics, Leipziger Straße 23, 09599 Freiberg, Germany. E-mail: [email protected]
Andre Ehrlich
Affiliation:
TU Bergakademie Freiberg, Institute of Mineralogy, Brennhausgaße 14, 09599 Freiberg, Germany
Allison L. Stelling
Affiliation:
Department of Mechanical Engineering and Materials Science, Duke University, 90300 Hudson Hall, Durham, North Carolina 27708, U.S.A.
Martin Hog
Affiliation:
TU Dresden, Institute of Bioanalytical Chemistry, Helmholtzstraße 10, 01069 Dresden, Germany
Hermann Ehrlich*
Affiliation:
TU Bergakademie Freiberg, Institute of Experimental Physics, Leipziger Straße 23, 09599 Freiberg, Germany. E-mail: [email protected]
*
∗Corresponding authors.
∗Corresponding authors.
Get access Rights & Permissions [Opens in a new window]

Abstract

Chitin occurs in a variety of invertebrates, especially in arthropod cuticles, but is rarely reported in the fossil record. Although it has been detected in fossils as old as Middle Cambrian and Silurian, the majority of records come from much younger, Cenozoic deposits. In this paper, we report the preservation of chitin in Early Jurassic neritimorph gastropod egg capsules deposited in bivalve shells from prodelta-deltafront and nearshore paleoenvironments of the Holy Cross Mountains, Poland. We used a number of analytical methods to confirm the presence of chitin preserved in these ancient fossils. This is the first record of chitin preservation in Mesozoic deposits that, interestingly, do not follow the conventional Konservat-Lagerstätten manner of preserving soft-bodied and non-biomineralized organisms. We believe that deltaic settings characterized by episodic, high input of fluvial deposits, oligohaline conditions, and oxygen-poor microenvironment within the sediment—as well as early cementation of sediment infilling the shells—were crucial for chitin preservation. The preservation of chitin in such recalcitrant structures as egg capsules and deposits that formed outside conventional Konservat-Lagerstätten conditions renders it likely similar deposits may yield promise for discoveries of similar biological macromolecules.

Type
Articles
Information
Paleobiology , Volume 40 , Issue 4 , Fall 2014 , pp. 529 - 540
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Adegoke, O. S., Dessauvagie, T. F. J., and Yoloye, V. L. A. 1969. Hemisphaerammina-like egg capsules of Neritina (Gastropoda) from Nigeria. Micropaleontology 15:102–106.Google Scholar
Allison, P. A., and Briggs, D. E. G. 1993. Exceptional fossil record: distribution of soft-tissue preservation through the Phanerozoic. Geology 21:527–530.2.3.CO;2>CrossRefGoogle Scholar
Bandel, K. 1982. Morphologie und Bildung der frühontogenetischen Gehäuse bei conchiferen Mollusken. Facies 7:1–198.Google Scholar
Bierstedt, A., Stankiewicz, B. A., Briggs, D. E. G., and Evershed, R. P. 1998. Quantitative and qualitative analysis of chitin in fossil arthropods using a combination of colorimetric assay and pyrolysis–gas chromatography–mass spectrometry. The Analyst 123:139–145.Google Scholar
Bo, M., Bavestrello, G., Kurek, D., Paasch, S., Brunner, E., Born, R., Galli, R., Stelling, A. L., Sivkov, V. N., Petrova, O. V., Vyalikh, D., Kummer, K., Molodtsov, S. L., Nowak, D., Nowak, J., and Ehrlich, H. 2012. Isolation and identification of chitin in the black coral Parantipathes larix (Anthozoa: Cnidaria). International Journal of Biological Macromolecules 51:129–137.Google Scholar
Boden, N., Sommer, U., and Spindler, K.-D. 1985. Demonstration and characterization of the chitinases in the drosophila Kc cell line. Insect Biochemistry 15:19–23.Google Scholar
Briggs, D. E. G. 1999. Molecular taphonomy of animal and plant cuticles: selective preservation and diagenesis. Philosophical Transactions of the Royal Society of London B 354:7–17.Google Scholar
Briggs, D. E. G., and Gall, J.-C. 1990. The continuum in soft-bodied biotas from transitional environments: a quantitative comparison of Triassic and Carboniferous Konservat-Lagerstätten. Paleobiology 16:204–218.Google Scholar
Brunner, E., Ehrlich, H., Schupp, P., Hedrich, R., Hunoldt, S., Kammer, M., Machill, S., Paasch, S., Bazhenov, V. V., Kurek, D. V., Arnold, T., Brockmann, S., Ruhnow, M., and Born, R. 2009a. Chitin-based scaffolds are an integral part of the skeleton of the marine demosponge Ianthella basta. Journal of Structural Biology 168:539–547.Google Scholar
Brunner, E., Richthammer, P., Ehrlich, H., Paasch, S., Simon, P., Ueberlein, S., and van Pée, K.-H. 2009b. Chitin-based organic networks: an integral part of cell wall biosilica in the diatom Thalassiosira pseudonana. Angewandte Chemie (International Edition) 48:9724–9727.CrossRefGoogle ScholarPubMed
Bulawa, C. E. 1993. Genetics and molecular biology of chitin synthesis in fungi. Annual Reviews 2:505–534.Google Scholar
Cody, G. D., Gupta, N. S., Briggs, D. E. G., Kilcoyne, A. L. D., Summons, R. E., Kenig, F., Plotnick, R. E., and Scott, A. C. 2011. Molecular signature of chitin-protein complex in Paleozoic arthropods. Geology 39:255–258.Google Scholar
Cotta, A. J. B., and Enzweiler, J. 2012. Classical and new procedures of whole rock dissolution for trace element determination by ICP-MS. Geostandards and Geoanalytical Research 36:27–50.CrossRefGoogle Scholar
Cruz-Barraza, J. A., Carballo, J. L., Rocha-Olivares, A., Ehrlich, H., and Hog, M. 2012. Integrative taxonomy and molecular phylogeny of genus Aplysina (Demospongiae: Verongida) from Mexican Pacific. PLoS ONE 7:e42049.Google Scholar
Darmon, S., and Rudall, K. 1950. Infra-red and X-ray studies of chitin. Discussions of the Faraday Society 9:253–260.Google Scholar
Ehrlich, H. 2010. Chitin and collagen as universal and alternative templates in biomineralization. International Geology Review 52:661–699.Google Scholar
Ehrlich, H., Krautter, M., Hanke, T., Simon, P., Knieb, C., Heinemann, S., and Worch, H. 2007a. First evidence of the presence of chitin in skeletons of marine sponges, Part II. Glass sponges (Hexactinellida: Porifera). Journal of Experimental Zoology B 308B:473–483.Google Scholar
Ehrlich, H., Maldonado, M., Spindler, K., Eckert, C., Hanke, T., Born, R., Simon, P., Heinemann, S., and Worch, H. 2007b. First evidence of chitin as a component of the skeletal fibers of marine sponges, Part I. Verongidae (Demospongia: Porifera). Journal of Experimental Zoology B 356:347–356.Google Scholar
Ehrlich, H., Kaluzhnaya, O. V., Brunner, E., Tsurkan, M. V., Ereskovsky, A., Ilan, M., Tabachnick, K. R., Bazhenov, V. V., Paasch, S., Kammer, M., Born, R., Stelling, A., Galli, R., Belikov, S., Petrova, O. V., Sivkov, V. V., Vyalikh, D., Hunoldt, S., and Wörheide, G. 2013a. Identification and first insights into the structure and biosynthesis of chitin from the freshwater sponge Spongilla lacustris. Journal of Structural Biology 183:474–483.CrossRefGoogle ScholarPubMed
Ehrlich, H., Rigby, J. K., Botting, J. P., Tsurkan, M., Werner, C., Schwille, P., Petrasek, Z., Pisera, A., Simon, P., Sivkov, V., Vyalikh, D., Molodtsov, L. S., Kurek, D., Kammer, M., Hunoldt, S., Born, R., Stawski, D., Steinhof, A., and Geisler-Wierwille, T. 2013b. Discovery of 505-million-year old chitin in the basal demosponge Vauxia gracilenta. Scientific Reports 3, art. 3497. doi: 10.1038/srep03497.Google Scholar
Ehrlich, H., Kaluzhnaya, O. V., Tsurkan, M. V., Ereskovsky, A., Tabachnick, K. R., Ilan, M., Stelling, A., Galli, R., Petrova, O. V., Nekipelov, S. V., Sivkov, N., Vyalikh, D., Born, R., Behm, T., Ehrlich, A., Chernogor, L. I., Belikov, S., Janussen, D., Bazhenov, V. V., and Wörheide, G. 2013c. First report on chitinous holdfast in sponges (Porifera). Proceedings of the Royal Society of London B 280 (1762):20130339. doi: 10.1098/rspb.2013.0339.Google Scholar
Elorza, M. V., Rico, H., and Sentandreu, R. 1983. Calcofluor White alters the assembly of chitin fibrils in Saccharomyces cerevisiae and Candida albicans cells. Journal of General Microbiology 129:1577–1582.Google Scholar
Fabritius, H.-O., Sachs, C., Triguero, P. R., and Raabe, D. 2009. Influence of structural principles on the mechanics of a biological fiber-based composite material with hierarchical organization: the exoskeleton of the lobster Homarus americanus. Advanced Materials 21:391–400.Google Scholar
Falini, G., and Fermani, S. 2004. Chitin mineralization. Tissue Engineering 10:1–6.CrossRefGoogle ScholarPubMed
Fernandez, J. G., and Ingber, D. E. 2013. Bioinspired chitinous material solutions for environmental sustainability and medicine. Advanced Functional Materials 23:4454–4466.Google Scholar
Flannery, M. B., Stott, A. W., Briggs, D. E. G., and Evershed, R. P. 2001. Chitin in the fossil record: identification and quantification of D-glucosamine. Organic Geochemistry 32:745–754.Google Scholar
Furuhashi, T., Schwarzinger, C., Miksik, I., Smrz, M., and Beran, A. 2009. Molluscan shell evolution with review of shell calcification hypothesis. Comparative Biochemistry and Physiology B 154:351–371.CrossRefGoogle ScholarPubMed
Goffinet, G., and Jeuniaux, C. 1979. Distribution et importance quantitative de la chitine dans les coquilles de mollusques. Cahiers de Biologie Marine 20:341–349.Google Scholar
Gómez Ramıìrez, M., Rojas Avelizapa, L. I., Rojas Avelizapa, N. G., and Cruz Camarillo, R. 2004. Colloidal chitin stained with Remazol Brilliant Blue R, a useful substrate to select chitinolytic microorganisms and to evaluate chitinases. Journal of Microbiological Methods 56:213–219.Google Scholar
Gradstein, F., Ogg, J., Schmitz, M., and Ogg, G. 2012. The geologic time scale 2012. Elsevier, Amsterdam.Google Scholar
Gupta, N. S., and Briggs, D. E. G. 2011. Taphonomy of animal organic skeletons through time. Pp. 199–221inAllison, P. A. and Bottjer, D. J., eds. Taphonomy: process and bias through time. Topics in Geobiology 38. Springer, Dordrecht.Google Scholar
Gupta, N. S., Briggs, D. E. G., Collinson, M. E., Evershed, R. P., Michels, R., and Pancost, R. D. 2007. Molecular preservation of plant and insect cuticles from the Oligocene Enspel Formation, Germany: evidence against derivation of aliphatic polymer from sediment. Organic Geochemistry 38:404–418.Google Scholar
Heinemann, F., Launspach, M., Gries, K., and Fritz, M. 2011. Gastropod nacre : structure, properties and growth—biological, chemical and physical basics. Biophysical Chemistry 153:126–153.Google Scholar
Herth, W. 1980. Calcofluor White and Congo Red inhibit chitin microfibril assembly of Poterioochromonas: evidence for a gap between polymerization and microfibril formation. Journal of Cell Biology 87:442–450.Google Scholar
Herth, W., and Schnepf, E. 1980. The fluorochrome, Calcofluor White, binds oriented to structural polysaccharide fibrils. Protoplasma 105:129–133.Google Scholar
Imai, K., Noda, Y., Adachi, H., and Yoda, K. 2005. A novel endoplasimic reticulum membrane protein Rcr1 regulates chitin deposition in the cell wall of Saccharomyces cerevisiae. Journal of Biological Chemistry 280:8275–8284.Google Scholar
Jeuniaux, C. 1963. Chitine et chitinolyse. Masson, Paris.Google Scholar
Kaiser, P., and Voigt, E. 1977. Über eine Schneckenlaich gedeutete Eiablage in einer Schale von Pseudopecten aus dem Lias von Salzgitter. Paläontologische Zeitschrift 51:5–11.Google Scholar
Kaiser, P., 1983. Fossiler Schneckenlaich in Ammonitenwohnkammern. Lethaia 16:145–156.Google Scholar
Kano, Y., and Fukumori, H. 2010. Predation on hardest molluscan eggs by confamilial snails (Neritidae) and its potential significance in egg-laying site selection. Journal of Molluscan Studies 76:360–366.Google Scholar
Kjartansson, G. T., Zivanovic, S., Kristbergsson, K., and Weiss, J. 2006. Sonication-assisted extraction of chitin from North Atlantic shrimps (Pandalus borealis). Journal of Agricultural and Food Chemistry 54:5894–5902.Google Scholar
Lavall, R. L., Assis, O. B. G., and Campana-Filho, S. P. 2007. Beta-chitin from the pens of Loligo sp.: extraction and characterization. Bioresource Technology 98:2465–2472.Google Scholar
Lease, H. M., and Wolf, B. O. 2010. Exoskeletal chitin scales isometrically with body size in terrestrial insects. Journal of Morphology 271:759–768.Google Scholar
Matsuoka, H., Yang, H. C., Homma, T., Nemoto, Y., Yamada, S., Sumita, O., Takatori, K., and Kurata, H. 1995. Use of Congo Red as a microscopic fluorescence indicator of hyphal growth. Applied Microbiology and Biotechnology 43:102–108.Google Scholar
Michels, J., and Büntzow, M. 2010. Assessment of Congo Red as a fluorescence marker for the exoskeleton of small crustaceans and the cuticle of polychaetes. Journal of Microscopy 238:95–101.Google Scholar
Miller, R. F. 1991. Chitin paleoecology. Biochemical Systematics and Ecology 19:401–411.Google Scholar
Muzzarelli, R. A. A. 1977. Chitin. Pergamon, New York.Google Scholar
Neuerburg, G. J. 1961. A method of mineral separation using hydrofluoric acid. The American Mineralogist 46:1501.Google Scholar
Nicol, S., and Hosie, G. W. 1993. Chitin production by krill. Biochemical Systematics and Ecology 21:181–184.Google Scholar
Orr, P. J., Benton, M. J., and Briggs, D. E. G. 2003. Post-Cambrian closure of the deep-water slope-basin taphonomic window. Geology 31:769–772.Google Scholar
Peters, W. 1972. Occurrence of chitin in Mollusca. Comparative Biochemistry and Physiology B 41B:541–550.Google Scholar
Pieńkowski, G. 2004. The epicontinental Lower Jurassic of Poland. Polish Geological Institute Special Papers 12:1–154.Google Scholar
Poulicek, M. 1983. Chitin in gastropod operculi. Biochemical Systematics and Ecology 11:47–54.Google Scholar
Poulicek, M., and Jeuniaux, C. 1991. Chitin biodegradation in marine environments: an experimental approach. Biochemical Systematics and Ecology 19:385–394.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 63:1083–1095.Google Scholar
Schiffman, J. D., and Schauer, C. L. 2009. Solid state characterization of α-chitin from Vanessa cardui Linnaeus wings. Materials Science and Engineering C 29:1370–1374.Google Scholar
Soliman, G. N. 1987. A scheme for classifying gastropod egg masses with special reference to those from the northwestern Red Sea. Journal of Molluscan Studies 53:1–12.Google Scholar
Sommer, U., and Spindler, K.-D. 1991. Demonstration of β-N-acetyl-D-glucosaminidase in Drosophilia Kc-cells. Archives of Insect Biochemistry and Physiology 17:3–13.Google Scholar
Stankiewicz, B. A., Briggs, D. E. G., Evershed, R. P., Flannery, M. B., and Wuttke, M. 1997a. Preservation of chitin in 25-million-year-old fossils. Science 276:1541–1543.Google Scholar
Stankiewicz, B. A., Briggs, D. E. G., Evershed, R. P., and Duncan, I. J. 1997b. Chemical preservation of insect cuticle from the Pleistocene asphalt deposits of California, USA. Geochimica et Cosmochimica Acta 61:2247–2252.Google Scholar
Taylor, V. F., Toms, A., and Longerich, H. P. 2002. Acid digestion of geological and environmental samples using open-vessel focused microwave digestion. Analytical and Bioanalytical Chemistry 372:360–365.Google Scholar
Tóth, G., and Zechmeister, L. 1939. Chitin content of the mandible of the snail (Helix pomatia). Nature 144:1049.Google Scholar
Wan, A. C. A., and Tai, B. C. U. 2013. Chitin—a promising biomaterial for tissue engineering and stem cell technologies. Biotechnology Advances 31:1776–1785.Google Scholar
Weaver, P. G., Doguzhaeva, L. A., Lawver, D. R., Tacker, R. C., Ciampaglio, C. N., Crate, J. M., and Zheng, W. 2011. Characterization of organics consistent with β-chitin preserved in the Late Eocene cuttlefish Mississaepia mississippiensis. PLoS ONE 6:e28195.Google Scholar
Weiner, S., and Traub, W. 1980. X-ray diffraction study of the insoluble organic matrix of mollusk shells. FEBS Letters 111:311–316.Google Scholar
Weiss, I. M., and Schönitzer, V. 2006. The distribution of chitin in larval shells of the bivalve mollusk Mytilus galloprovincialis. Journal of Structural Biology 153:264–277.Google Scholar
Winkler, L. R. 1960. Localization and proof of chitin in the opisthobranch mollusks Aplysia californica Cooper and Bulla gmtldiana (Pilsbry), with an enzymochromatographic method for chitin demonstration. Pacific Science 14:304–307.Google Scholar
Wysokowski, M., Bazhenov, V. V., Tsurkan, M. V., Galli, R., Stelling, A. L., Stöcker, H., Kaiser, S., Niederschlag, E., Gärtner, G., Behm, T., Ilan, M., Petrenko, A. Y., Jesionowski, T., and Ehrlich, H. 2013. Isolation and identification of chitin in three-dimensional skeleton of Aplysina fistularis marine sponge. International Journal of Biological Macromolecules 62:94–100.Google Scholar
Zatoń, M., Niedźwiedzki, G., and Pieńkowski, G. 2009. Gastropod egg capsules preserved on bivalve shells from the Lower Jurassic (Hettangian) of Poland. Palaios 24:568–577.Google Scholar
Zatoń, M., Taylor, P. D., and Jagt, J. W. M. 2013. Late Cretaceous gastropod egg capsules from the Netherlands preserved by bioimmuration. Acta Palaeontologica Polonica 58:351–355.Google Scholar