Iron-mediated deep-time preservation of osteocytes in a Middle Triassic reptile bone

Surmik, Dawid; Dulski, Mateusz; Kremer, Barbara; Szade, J.; Pawlicki, R

doi:10.1080/08912963.2019.1599884

“…As previously shown (Cadena, 2016;Schweitzer et al, 2014;Surmik et al, 2019;Ullmann, Pandya & Nellermoe, 2019), the in situ analyses presented here, concur with that iron is a very common constituent of fossil osteocytes-like, such as those found in the Late Cretaceous Mongolemys elegans and the Miocene podocnemidid indet. bone samples studied herein (Figs.…”

Section: Discussionsupporting

confidence: 91%

“…Compositionally, the osteocytes-and blood vessels-like from different clades of fossil vertebrates have been shown to commonly be enriched in iron (Cadena, 2016;Schweitzer et al, 2014;Surmik et al, 2019;Ullmann, Pandya & Nellermoe, 2019), an element that has been suggested to play a key role in preserving and even masking identification of proteins in fossil tissues via Fenton reactions (Schweitzer et al, 2014). Other elements typically found in these fossil bone microstructures are carbon, calcium, and silicon (Cadena, 2016;Ullmann, Pandya & Nellermoe, 2019).…”

Section: Introductionmentioning

confidence: 99%

In situ SEM/EDS compositional characterization of osteocytes and blood vessels in fossil and extant turtles on untreated bone surfaces; different preservational pathways microns away

Cadena

¹

2020

PeerJ

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Osteocytes and blood vessels are the main cellular and tissue components of the bone tissue of vertebrates. Evidence of these soft-tissue microstructures has been widely documented in the fossil record of Mesozoic and Cenozoic turtles. However, all these studies have characterized morphologically and elementally these microstructures via isolation from the fossilized bone matrix where they were preserved or in ground sections, which could raise skepticism about the results due to potential cross-contamination or reagents effects. Fossil turtle bones from three different localities with distinct preservation environments and geological settings, including Mongolemys elegans from the Late Cretaceous of Mongolia, Allaeochelys crassesculpta from the Eocene of Germany, and a podocnemidid indet. from the Miocene of Colombia are studied here. Bone from two extant turtle species, Lepidochelys olivacea, and Podocnemis lewyana, as well as a commercial chicken Gallus gallus were used for comparisons. Scanning Electron Microscopy-Energy Dispersive Spectroscopy analyses performed directly on untreated fresh surfaces show that osteocytes-like in the fossil turtle bone are mostly composed of iron and manganese. In contrast, the in situ blood vessels-like of the fossil turtles, as well as those from the extant taxa are rich in elements typically organic in origin (carbon and nitrogen), which are absent to minimally present in the surrounding bone or rock matrix; this suggests a possible endogenous composition for these fossil structures. Also, the results presented here show that although originally both (osteocytes and blood vessels) are organic soft components of bone as evidenced in the extant turtles and chicken, they can experience completely different preservational pathways only microns away from each other in the same fossil bone.

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“…As previously shown (Cadena 2016;Schweitzer et al 2014;Surmik et al 2019;Ullmann et al 2019), the in situ analyses presented here, concur with that iron is a very common constituent of fossil osteocytes-like, such as those found in the Late Cretaceous Mongolemys elegans and the Miocene podocnemidid indet. bone samples studied herein (Figs.…”

Section: Discussionsupporting

confidence: 91%

“…Osteocytes are embedded within the hard-mineralized component of bone throughout life (exceptions being when released by fracture or during remodeling) (Robling & Bonewald 2020), providing them high preservation potential within fossil bones, which has been extensively documented in different clades of vertebrates (e.g., Bailleul et al 2019;Enlow & Brown 1956;Pawlicki & Nowogrodzka-Zagorska 1998;Schweitzer 2011;Schweitzer et al 2013;Surmik et al 2019). Similar preservation of osteocytes-and blood vessels-like has also been documented in fossil turtles, showing that their preservation is independent of geologic time, paleoenvironment, lithology, lineages, and latitude (Cadena 2016;Cadena et al 2013;Cadena & Schweitzer 2012 Something in common to all aforementioned studies are the analytical tools used to study and characterize these fossil bone microstructures, which include principally: 1) ground sections and observation under transmitted and polarized microscopy (Cadena & Schweitzer 2012;Surmik et al 2019); 2) bone demineralization using ethylenediaminetetraacetic acid (EDTA) as a chelating agent (0.5 M, pH 8.0), facilitating release the osteocytes-, blood vessels-, and any other cells-or soft-tissue fibers-like from the bone matrix for their posterior study by transmitted and/or polarized light, scanning and/or transmission electron microscopy and any coupled elemental analyzer, Raman spectroscopy, Fourier-transform infrared spectroscopy (FTIR), immunological and antibody studies (e.g., Alfonso-Rojas & Cadena 2020; Bailleul et al 2019Bailleul et al , 2020Cadena 2016;Saitta et al 2019;Schweitzer et al 2013;Surmik et al 2019;Wiemann et al 2018) The preservation of these soft-tissue microstructures (osteocytes and blood vessels) and their potential original constituents (proteins and DNA) has been questioned and considered a consequence of microbial interactions within fossil bone and its microenvironment or even as a result of cross-contamination in the laboratory (Buckley et al 2017;Kaye et al 2008;Saitta et al 2019). The 'biofilm hypothesis' as a source for soft-tissue preservation in dinosaur bones has been rigorously tested, which identified fundamental morphological, chemical and textural differences between the resultant biofilm structures and those derived from dinosaur bone, demonstrati...…”

Section: Introductionmentioning

confidence: 99%

“…Compositionally, the osteocytes-and blood vessels-like from different clades of fossil vertebrates have been shown to commonly be enriched in iron (Cadena 2016;Schweitzer et al 2014;Surmik et al 2019;Ullmann et al 2019), an element that has been suggested to play a key role in preserving and even masking identification of proteins in fossil tissues via Fenton reactions (Schweitzer et al 2014). Other elements typically found in these fossil bone microstructures are carbon, calcium, and silicon (Cadena 2016;Ullmann et al 2019).…”

Section: Introductionmentioning

confidence: 99%

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Peer Review #2 of "In situ SEM/EDS compositional characterization of osteocytes and blood vessels in fossil and extant turtles on untreated bone surfaces; different preservational pathways microns away (v0.1)"

2020

0

View full text Add to dashboard Cite

Osteocytes and blood vessels are the main cellular and tissue components of the bone tissue of vertebrates. Evidence of these soft-tissue microstructures has been widely documented in the fossil record of Mesozoic and Cenozoic turtles. However, all these studies have characterized morphologically and elementally these microstructures via isolation from the fossilized bone matrix where they were preserved or in ground sections, which could raise skepticism about the results due to potential cross-contamination or reagents effects. Fossil turtle bones from three different localities with distinct preservation environments and geological settings, including Mongolemys elegans from the Late Cretaceous of Mongolia, Allaeochelys crassesculpta from the Eocene of Germany, and a podocnemidid indet. from the Miocene of Colombia are studied here. Bone from two extant turtle species, Lepidochelys olivacea, and Podocnemis lewyana, as well as a commercial chicken Gallus gallus were used for comparisons. Scanning Electron Microscopy-Energy Dispersive Spectroscopy analyses performed directly on untreated fresh surfaces show that osteocytes-like in the fossil turtle bone are mostly composed of iron and manganese. In contrast, the in situ blood vessels-like of the fossil turtles, as well as those from the extant taxa are rich in elements typically organic in origin (carbon and nitrogen), which are absent to minimally present in the surrounding bone or rock matrix; this suggests a possible endogenous composition for these fossil structures. Also, the results presented here show that although originally both (osteocytes and blood vessels) are organic soft components of bone as evidenced in the extant turtles and chicken, they can experience completely different preservational pathways only microns away from each other in the same fossil bone.

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An Upper Miocene marine turtle from Panama that preserves osteocytes with potential DNA

Cadena,

Gracia,

Combita-Romero

2023

Journal of Vertebrate Paleontology

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Lepidochelys is a genus of extant marine turtles that includes the critically endangered Kemp's Ridley turtle. The evolutionary history of this genus is poorly understood due to the lack of an undisputed fossil record for the group. Here we describe a partially preserved carapace from the Upper Miocene Chagres Formation of Panama, which represents the oldest fossil record of Lepidochelys. The specimen has rectangular, anteroposteriorly short pleural scutes, a characteristic shared with members of Lepidochelys. It is potentially closely related to L. olivacea because it shares a similar number of pleurals, but its precise taxonomic status remains uncertain. We discuss the ecological role that a marine turtle played in the paleoecosystem of the Chagres Formation. The new specimen exhibits exceptional preservation of bone sutures, sulci, sculpturing, and bone microstructure, including remains of blood vessels, collagen fibers, and osteocytes. This is the first time that a histochemical stain (DAPI) indicates preservation of a compound consistent with DNA in a fossil vertebrate outside Dinosauria. These data demonstrate the potential for DNA to persist in specimens that are both millions of years old and are from lower latitudes, which challenges traditional paradigms of biomolecular preservation.

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Iron-mediated deep-time preservation of osteocytes in a Middle Triassic reptile bone

Cited by 8 publications

References 51 publications

In situ SEM/EDS compositional characterization of osteocytes and blood vessels in fossil and extant turtles on untreated bone surfaces; different preservational pathways microns away

In situ SEM/EDS compositional characterization of osteocytes and blood vessels in fossil and extant turtles on untreated bone surfaces; different preservational pathways microns away

Peer Review #2 of "In situ SEM/EDS compositional characterization of osteocytes and blood vessels in fossil and extant turtles on untreated bone surfaces; different preservational pathways microns away (v0.1)"

An Upper Miocene marine turtle from Panama that preserves osteocytes with potential DNA

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