Synchrotron X-ray absorption spectroscopy of melanosomes in vertebrates and cephalopods: implications for the affinity of Tullimonstrum
Abstract
Screening pigments are essential for vision in animals. Vertebrates use melanins bound in melanosomes as screening pigments, whereas cephalopods are assumed to use ommochromes. In this work, preserved eye melanosomes in the controversial fossil Tullimonstrum (Mazon Creek, IL, USA) are partitioned by size and/or shape into distinct layers. These layers resemble tissue-specific melanosome populations considered unique to the vertebrate eye. Here, we show that extant cephalopod eyes also show tissue-specific size- and/or shape-specific partitioning of melanosomes; these differ from vertebrate melanosomes in the relative abundance of trace metals and in the binding environment of copper. Chemical signatures of melanosomes in the eyes of Tullimonstrum more closely resemble those of modern cephalopods than those of vertebrates, suggesting that an invertebrate affinity for Tullimonstrum is plausible. Melanosome chemistry may thus provide insights into the phylogenetic affinities of enigmatic fossils where melanosome size and/or shape are equivocal.
- Authors:
-
[1];
[1]
- Univ. College Cork, Distillery Fields, Cork (Republic of Ireland)
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
- Fujita Health Univ. Toyoake, Aichi (Japan). School of Health Sciences
- Publication Date:
- Research Org.:
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); European Research Starting Grant
- OSTI Identifier:
- 1604749
- Grant/Contract Number:
- AC02-76SF00515; ERC-2014-StG-637691-ANIVOLEVO
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Additional Journal Information:
- Journal Volume: 286; Journal Issue: 1913; Journal ID: ISSN 0962-8452
- Publisher:
- The Royal Society Publishing
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; fossil soft tissues; Konservat-Lagerstätten; melanosomes; trace metals
Citation Formats
Rogers, Christopher S., Astrop, Timothy I., Webb, Samuel M., Ito, Shosuke, Wakamatsu, Kazumasa, and McNamara, Maria E. Synchrotron X-ray absorption spectroscopy of melanosomes in vertebrates and cephalopods: implications for the affinity of Tullimonstrum. United States: N. p., 2019.
Web. doi:10.1098/rspb.2019.1649.
Rogers, Christopher S., Astrop, Timothy I., Webb, Samuel M., Ito, Shosuke, Wakamatsu, Kazumasa, & McNamara, Maria E. Synchrotron X-ray absorption spectroscopy of melanosomes in vertebrates and cephalopods: implications for the affinity of Tullimonstrum. United States. https://doi.org/10.1098/rspb.2019.1649
Rogers, Christopher S., Astrop, Timothy I., Webb, Samuel M., Ito, Shosuke, Wakamatsu, Kazumasa, and McNamara, Maria E. Wed .
"Synchrotron X-ray absorption spectroscopy of melanosomes in vertebrates and cephalopods: implications for the affinity of Tullimonstrum". United States. https://doi.org/10.1098/rspb.2019.1649. https://www.osti.gov/servlets/purl/1604749.
@article{osti_1604749,
title = {Synchrotron X-ray absorption spectroscopy of melanosomes in vertebrates and cephalopods: implications for the affinity of Tullimonstrum},
author = {Rogers, Christopher S. and Astrop, Timothy I. and Webb, Samuel M. and Ito, Shosuke and Wakamatsu, Kazumasa and McNamara, Maria E.},
abstractNote = {Screening pigments are essential for vision in animals. Vertebrates use melanins bound in melanosomes as screening pigments, whereas cephalopods are assumed to use ommochromes. In this work, preserved eye melanosomes in the controversial fossil Tullimonstrum (Mazon Creek, IL, USA) are partitioned by size and/or shape into distinct layers. These layers resemble tissue-specific melanosome populations considered unique to the vertebrate eye. Here, we show that extant cephalopod eyes also show tissue-specific size- and/or shape-specific partitioning of melanosomes; these differ from vertebrate melanosomes in the relative abundance of trace metals and in the binding environment of copper. Chemical signatures of melanosomes in the eyes of Tullimonstrum more closely resemble those of modern cephalopods than those of vertebrates, suggesting that an invertebrate affinity for Tullimonstrum is plausible. Melanosome chemistry may thus provide insights into the phylogenetic affinities of enigmatic fossils where melanosome size and/or shape are equivocal.},
doi = {10.1098/rspb.2019.1649},
journal = {Proceedings of the Royal Society B: Biological Sciences},
number = 1913,
volume = 286,
place = {United States},
year = {Wed Oct 23 00:00:00 EDT 2019},
month = {Wed Oct 23 00:00:00 EDT 2019}
}
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Cited by: 8 works
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Figures / Tables:
Figure 1: Anatomy of extant cephalopod and vertebrate eyes. Schematic illustrations of ($a$) cephalopod eye and ($b$) vertebrate eye with, inset, detail of tissue layers. ($c$) Histological sections and scanning electron micrographs (SEM) of eyes in Loligo, Octopus, Sepia and Petromyzon. Sections are stained with Warthin-Starry; melanin appears black. Allmore »
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Works referenced in this record:
ATHENA , ARTEMIS , HEPHAESTUS : data analysis for X-ray absorption spectroscopy using IFEFFIT
journal, June 2005
- Ravel, B.; Newville, M.
- Journal of Synchrotron Radiation, Vol. 12, Issue 4
Intraocular distribution of melanin in human, monkey, rabbit, minipig and dog eyes
journal, May 2012
- Durairaj, Chandrasekar; Chastain, James E.; Kompella, Uday B.
- Experimental Eye Research, Vol. 98
Physical and Chemical Characterization of Iris and Choroid Melanosomes Isolated from Newborn and Mature Cows¶
journal, May 2005
- Hong, Lian; Simon, John D.
- Photochemistry and Photobiology, Vol. 81, Issue 3
Tissue-specific geometry and chemistry of modern and fossilized melanosomes reveal internal anatomy of extinct vertebrates
journal, August 2019
- Rossi, Valentina; McNamara, Maria E.; Webb, Sam M.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 36
Comparisons of the Structural and Chemical Properties of Melanosomes Isolated from Retinal Pigment Epithelium, Iris and Choroid of Newborn and Mature Bovine Eyes¶
journal, May 2005
- Liu, Yan; Hong, Lian; Wakamatsu, Kazumasa
- Photochemistry and Photobiology, Vol. 81, Issue 3
Acid hydrolysis reveals a low but constant level of pheomelanin in human black to brown hair
journal, December 2017
- Ito, Shosuke; Miyake, Shiho; Maruyama, Shoji
- Pigment Cell & Melanoma Research, Vol. 31, Issue 3
Melanogenesis in the Ink Gland of Sepia officinalis
journal, October 2003
- Palumbo, Anna
- Pigment Cell Research, Vol. 16, Issue 5
The eyes of Tullimonstrum reveal a vertebrate affinity
journal, April 2016
- Clements, Thomas; Dolocan, Andrei; Martin, Peter
- Nature, Vol. 532, Issue 7600
Immunoelectron-microscopic study of G-protein distribution in photoreceptor cells of the cephalopod Sepia officinalis
journal, June 1995
- Schraermeyer, Ulrich; Stieve, Hennig; Rack, Michael
- Tissue and Cell, Vol. 27, Issue 3
The MicroAnalysis Toolkit: X-ray Fluorescence Image Processing Software
conference, January 2011
- Webb, S. M.; McNulty, Ian; Eyberger, Catherine
- THE 10TH INTERNATIONAL CONFERENCE ON X-RAY MICROSCOPY, AIP Conference Proceedings
Physical and Chemical Characterization of Iris and Choroid Melanosomes Isolated from Newborn and Mature Cows¶
journal, January 2005
- Hong, Lian; Simon, John D.
- Photochemistry and Photobiology, Vol. 81, Issue 3
X-ray absorption edge determination of the oxidation state and coordination number of copper. Application to the type 3 site in Rhus vernicifera laccase and its reaction with oxygen
journal, October 1987
- Kau, Lung Shan; Spira-Solomon, Darlene J.; Penner-Hahn, James E.
- Journal of the American Chemical Society, Vol. 109, Issue 21
Chemical, experimental, and morphological evidence for diagenetically altered melanin in exceptionally preserved fossils
journal, September 2015
- Colleary, Caitlin; Dolocan, Andrei; Gardner, James
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 41
Physical and Chemical Characterization of Iris and Choroid Melanosomes Isolated from Newborn and Mature Cows
journal, January 2005
- Hong, Lian; Simon, John D.
- Photochemistry and Photobiology
Evolution of eyes
journal, August 2000
- Fernald, Russell D.
- Current Opinion in Neurobiology, Vol. 10, Issue 4
The Usefulness of 4-Amino-3-hydroxyphenylalanine as a Specific Marker of Pheomelanin
journal, June 2002
- Wakamatsu, Kazumasa; Ito, Shosuke; Rees, Jonathan L.
- Pigment Cell Research, Vol. 15, Issue 3
Fossil insect eyes shed light on trilobite optics and the arthropod pigment screen
journal, August 2019
- Lindgren, Johan; Nilsson, Dan-Eric; Sjövall, Peter
- Nature, Vol. 573, Issue 7772
In vivo Optical Coherence Tomography of Light-Driven Melanosome Translocation in Retinal Pigment Epithelium
journal, September 2013
- Zhang, Qiu-Xiang; Lu, Rong-Wen; Messinger, Jeffrey D.
- Scientific Reports, Vol. 3, Issue 1
The ‘Tully Monster’ is not a vertebrate: characters, convergence and taphonomy in Palaeozoic problematic animals
journal, February 2017
- Sallan, Lauren; Giles, Sam; Sansom, Robert S.
- Palaeontology, Vol. 60, Issue 2
Current Understanding of the Binding Sites, Capacity, Affinity, and Biological Significance of Metals in Melanin
journal, July 2007
- Hong, Lian; Simon, John D.
- The Journal of Physical Chemistry B, Vol. 111, Issue 28
Comparisons of the Structural and Chemical Properties of Melanosomes Isolated from Retinal Pigment Epithelium, Iris and Choroid of Newborn and Mature Bovine Eyes¶
journal, January 2005
- Liu, Yan; Hong, Lian; Wakamatsu, Kazumasa
- Photochemistry and Photobiology, Vol. 81, Issue 3
Adsorption of Pb(II) and Cd(II) by Squid Ommastrephes bartrami Melanin
journal, January 2009
- Chen, Shiguo; Xue, Changhu; Wang, Jingfeng
- Bioinorganic Chemistry and Applications, Vol. 2009
Trace Metals as Biomarkers for Eumelanin Pigment in the Fossil Record
journal, June 2011
- Wogelius, R. A.; Manning, P. L.; Barden, H. E.
- Science, Vol. 333, Issue 6049
Diverse immune functions of hemocyanins
journal, July 2014
- Coates, Christopher J.; Nairn, Jacqueline
- Developmental & Comparative Immunology, Vol. 45, Issue 1
How Complexity Originates: The Evolution of Animal Eyes
journal, December 2015
- Oakley, Todd H.; Speiser, Daniel I.
- Annual Review of Ecology, Evolution, and Systematics, Vol. 46, Issue 1
Primitive soft-bodied cephalopods from the Cambrian
journal, May 2010
- Smith, Martin R.; Caron, Jean-Bernard
- Nature, Vol. 465, Issue 7297
Fine Structure of Melanogenesis in the Ink Sac of Sepia offidnalis
journal, February 1994
- Schraermeyer, Ulrich
- Pigment Cell Research, Vol. 7, Issue 1
Melanin fate in the human epidermis: a reassessment of how best to detect and analyse histologically
journal, June 2016
- Joly-Tonetti, Nicolas; Wibawa, Judata I. D.; Bell, Mike
- Experimental Dermatology, Vol. 25, Issue 7
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