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      Characterization of Organics Consistent with β-Chitin Preserved in the Late Eocene Cuttlefish Mississaepia mississippiensis

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          Abstract

          Background

          Preservation of original organic components in fossils across geological time is controversial, but the potential such molecules have for elucidating evolutionary processes and phylogenetic relationships is invaluable. Chitin is one such molecule. Ancient chitin has been recovered from both terrestrial and marine arthropods, but prior to this study had not been recovered from fossil marine mollusks.

          Methodology/Principal Findings

          Organics consistent with β-chitin are recovered in cuttlebones of Mississaepia mississippiensis from the Late Eocene (34.36 million years ago) marine clays of Hinds County, Mississippi, USA. These organics were determined and characterized through comparisons with extant taxa using Scanning Electron Microscopy/Energy Dispersive Spectrometry (SEM/EDS), Field Emission Scanning Electron Microscopy (Hyperprobe), Fourier Transmission Infrared Spectroscopy (FTIR) and Immunohistochemistry (IHC).

          Conclusions/Significance

          Our study presents the first evidence for organics consistent with chitin from an ancient marine mollusk and discusses how these organics have been degraded over time. As mechanisms for their preservation, we propose that the inorganic/organic lamination of the cuttlebone, combined with a suboxic depositional environment with available free Fe 2+ ions, inhibited microbial or enzymatic degradation.

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          Organic preservation of non-mineralizing organisms and the taphonomy of the Burgess Shale

          Nicholas J Butterfield (1990)
          Organic preservation of non-mineralizing animals constitutes an important part of the paleontological record, yet the processes involved have not been investigated in detail. Organic-walled fossils are generally explicable as a coincidence of original, relatively recalcitrant, extra-cellular materials and more or less anti-biotic depositional circumstances. One of the most pervasive natural inhibitors of biodegradation results from substrate and enzyme adsorption onto, and within, clay minerals; such interactions are likely responsible for many of the organic-walled fossils preserved in clastic sediments. Close examination of the fossilLagerstätteof the Burgess Shale (Middle Cambrian, British Columbia) reveals that most of its so-called soft-bodied fossils are composed of primary (although kerogenized) organic carbon. Their preservation can be attributed to pervasive clay-organic interactions as the organisms were transported in a moving sediment cloud and buried with all cavities and spaces permeated with fine grained clays. The organic-walled Burgess Shale fossils were studied both in petrographic thin section and isolated from the rock matrix, following careful acid maceration. Isotopic analysis of bulk organic and carbonate carbon yielded values consistent with a normal marine paleoenvironment. Anatomical and histological consideration of the enigmatic Burgess wormAmiskwiasuggest that it may in fact be a chaetognath, while the putative chordatePikaiaappears not to be related to modern cephalochordates.
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            Biomolecular characterization and protein sequences of the Campanian hadrosaur B. canadensis.

            John Horner, Steven Lane, John Neveu … (2009)
            Molecular preservation in non-avian dinosaurs is controversial. We present multiple lines of evidence that endogenous proteinaceous material is preserved in bone fragments and soft tissues from an 80-million-year-old Campanian hadrosaur, Brachylophosaurus canadensis [Museum of the Rockies (MOR) 2598]. Microstructural and immunological data are consistent with preservation of multiple bone matrix and vessel proteins, and phylogenetic analyses of Brachylophosaurus collagen sequenced by mass spectrometry robustly support the bird-dinosaur clade, consistent with an endogenous source for these collagen peptides. These data complement earlier results from Tyrannosaurus rex (MOR 1125) and confirm that molecular preservation in Cretaceous dinosaurs is not a unique event.
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              Mollusk shell formation: mapping the distribution of organic matrix components underlying a single aragonitic tablet in nacre.

              Fabio Nudelman, Lia Addadi, Steve Weiner … (2006)
              Control over mineral formation in mollusk shells is exerted by the macromolecules of the organic matrix. Using histochemical methods, we mapped the carboxylates and sulfates of proteins and polysaccharides on the surfaces of decalcified interlamellar matrices from the nacreous shell layer of the cephalopod Nautilus pompilius, expanding upon an earlier study by Crenshaw and Ristedt [Crenshaw, M.A., Ristedt, H., 1976. The histochemical localization of reactive groups in septal nacre from Nautilus pompilius. In: Watabe, N., Wilbur, K.M. (Ed.), The Mechanisms of Mineralization in the Invertebrates and Plants. University of South Carolina Press, Colombia, pp. 355-367]. We observed four different zones underlying a single crystal: (1) a central spot rich in carboxylates; (2) a central ring-shaped area rich in sulfates; (3) an area between the central nucleation region and the imprint periphery containing carboxylates, and (4) the intertabular matrix, rich in carboxylates and sulfates. We also mapped matrix functional groups on the nacreous matrix surfaces of the bivalve Atrina rigida, but did not identify well-defined zones. Immuno-mapping of the constituents of the aragonite-nucleating protein fraction from Atrina nacre showed that these macromolecules are located both in the intertabular matrix and in the center of the crystal imprints for both Atrina and Nautilus matrix surfaces. Their presence at the latter location is consistent with their purported role in aragonite nucleation. The observed differentiation in the distribution of matrix components and their functional groups shows that the different stages of single crystal growth are highly controlled by the matrix.
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                Author and article information

                Contributors
                : Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, USA )
                ISSN (Electronic): 1932-6203
                Publication date Collection: 2011
                Publication date (Electronic): 23 November 2011
                Volume: 6
                Issue: 11
                Electronic Location Identifier: e28195
                Affiliations
                [1 ]Research and Collections, North Carolina Museum of Natural Sciences, Raleigh, North Carolina, United States of America
                [2 ]Department of Palaeozoology, Swedish Museum of Natural History, Stockholm, Sweden
                [3 ]Department of Earth Sciences, Montana State University, Bozeman, Montana, United States of America
                [4 ]Earth and Environmental Sciences, Wright State University, Celina, Ohio, United States of America
                [5 ]Analytical Chemistry, FAI Materials Testing Lab Incorporated, Marietta, Georgia, United States of America
                [6 ]Department of Marine, Earth and Atmospheric Sciences, North Carolina State University, Raleigh, North Carolina, United States of America
                Paleontological Institute of Russian Academy of Science, United States of America
                Author notes

                Conceived and designed the experiments: PW LD DL RT CC JC WZ. Performed the experiments: PW LD DL RT JC WZ. Analyzed the data: PW LD DL RT CC JC WZ. Contributed reagents/materials/analysis tools: PW LD DL RT CC JC WZ. Wrote the paper: PW LD DL RT CC JC WZ.

                Article
                Publisher ID: PONE-D-11-08442
                DOI: 10.1371/journal.pone.0028195
                PMC ID: 3223232
                PubMed ID: 22132239
                SO-VID: d45c9ebb-99e3-4e45-b868-5db01dd265c6
                Copyright © Weaver et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                Date received : 9 May 2011
                Date accepted : 2 November 2011
                Page count
                Pages: 9
                Categories
                Subject: Research Article
                Subject: Biology
                Subject: Biochemistry
                Subject: Paleontology
                Subject: Invertebrate Paleontology
                Subject: Taphonomy
                Subject: Chemistry
                Subject: Geochemistry
                Subject: Biogeochemistry
                Subject: Organic Chemistry
                Subject: Organic Compounds
                Subject: Earth Sciences
                Subject: Geochemistry
                Subject: Biogeochemistry
                Subject: Paleontology
                Subject: Invertebrate Paleontology
                Subject: Paleobiology
                Subject: Taphonomy
                Subject: Materials Science
                Subject: Biomaterials
                Subject: Materials Characterization

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