Submit Article
Asian Journal of Physics  Vol. 31 No 2, 2022, 195-208

Biopolymers in the eggshell of the Argentine Black and White Tegu (Salvator merianae): a Raman microscopy study
Rosa María Susana Álvarez, Alfredo Nicolás Dominguez, Francisco Alejandro Cortez, Oscar Augusto Carlino-Aráoz, and Fernando Horacio Campos-Casal

Abstract

The Argentine Black and White Tegu Salvator merianae is one of the largest South American lizards. The eggs of this reptile, whitish in color and oval in shape, are soft and resistant but permeable to water, evidencing interesting properties to be exploited in the field of biomaterial engineering. This is the first study focused on the organic matrix of the Salvator merianae eggshell. The structural analysis, carried out by Raman microscopy and complemented with transmission electron microscopy and with brightfield and polarized light optical microscopy, reveals an interesting organization of fibrillar polymers. The spatial distribution of collagen and keratins correlates with the morphology of this extraordinary complex system. © Anita Publications. All rights reserved.
Keywords: Collagen, Keratin, Biopolymers, Soft eggshell.

Peer Review Information
Method: Single- anonymous; Screened for Plagiarism? Yes
Buy this Article in Print © Anita Publications. All rights reserved

References

  1. Reisz R R, The Origin and Early Evolutionary History of Amniotes, Trends Ecol Evol, 12(1997)218–222.
  2. Blackburn D G, Stewart J R, Morphological Research on Amniote Eggs and Embryos: An Introduction and Historical Retrospective, J Morphol, 282(2021)1024–1046.
  3. Sander P M, Reproduction in Early Amniotes, Science, 337(2012)806–808.
  4. Starck J M, Stewart J R, Blackburn D G, Phylogeny and Evolutionary History of the Amniote Egg, J Morphol, 282(2021)1080–1122.
  5. Hallmann K, Griebeler E M, Eggshell Types and Their Evolutionary Correlation with Life-History Strategies in Squamates, PLoS One, 10(2015)e0138785; doi.org/10.1371/journal.pone.0138785
  6. Tang W, Zhao B, Chen Y, Du W, Reduced Egg Shell Permeability Affects Embryonic Development and Hatchling Traits in Lycodon rufozonatum and Pelodiscus sinensis, Integr Zool, 13(2018)58–69.
  7. Jee J, Mohapatra B K, Dutta S K, Sahoo G, Sources of Calcium for the Agamid Lizard Psammophilus blanfordanus During Embryonic Development, Acta Herpetol, 11(2016)171–178.
  8. Gough C R, Rivera-Galletti A, Cowan D A, Salas-De La Cruz D, Hu X, Protein and Polysaccharide-Based Fiber Materials Generated From Ionic Liquids: A Review, Molecules, 25(2020)3362; doi.org/10.3390/molecules25153362.
  9. Souza P R, de Oliveira A C, Vilsinski B H, Kipper M J, Martins A F, Polysaccharide-Based Materials Created by Physical Processes: From Preparation to Biomedical Applications, Pharmaceutics, 13(2021)621; doi.org/10.3390/pharmaceutics13050621.
  10. Pančić M, Torres R R, Almeda R, Kiørboe T, Silicified Cell Walls as a Defensive Trait in Diatoms, Proc Royal Soc: Biol Sci, 286(2019)20190184; doi. org/10.1098/rspb.2019.0184.
  11. Le Roy N, Stapane L, Gautron J, Hincke M T, Evolution of the Avian Eggshell Biomineralization Protein Toolkit – New Insights From Multi-Omics, Front Genet, (2021)672433; doi.org/10.3389/fgene.2021.672433.
  12. Chen P Y, McKittrick J, Meyers M A, Biological Materials: Functional Adaptations and Bioinspired Designs, Prog Mater Sci, 57(2012)1492–1704.
  13. Rauscher S, Pomès R, Structural Disorder and Protein Elasticity. In: Fuxreiter M, Tompa P, (eds). Fuzziness. Advances in Experimental Medicine and Biology, (Springer, New York, NY) 2012, p.159-183.
  14. Shavandi A, Silva,T H, Bekhit A A, Bekhit A E-D A, Keratin: Dissolution, Extraction and Biomedical Application. Biomater Sci, 5(2017)1699–1735.
  15. Sorushanova A, Delgado L M, Wu Z, Shologu N, Kshirsagar A, Raghunath R. Mullen A M, Bayon Y, Pandit A, Raghunath M, Zeugolis D I, The Collagen Suprafamily: from Biosynthesis to Advanced Biomaterial Development, Adv Mater, 31(2018)1801651; doi.org/10.1002/adma.201801651.
  16. Packard G C, Packard M J, Evolution of the Cleidoic Egg Among Reptilian Antecedents of Birds, Am Zool, 20(1980)351–362.
  17. Packard M J, DeMarco V G (1991). Eggshell structure and formation in eggs of oviparous reptiles. In: D. C. Deeming & M. W. J. Ferguson (Eds.), Egg incubation: Its effects on embryonic development in birds and reptiles. (Cambridge University Press) 1991, p. 53–69.
  18. Makkar S, Liyanage R, Kannan L, Packialakshmi B, Lay J O (Jr), Rath N C, Chicken Egg Shell Membrane Associated Proteins and Peptides, J Agric Food Chem, 63(2015)9888–9898.
  19. Hallmann K, Griebeler E, Eggshell Types and Their Evolutionary Correlation with Life-History Strategies in Squamates, PLoS One, 10(2015); doi.org/10.1371/journal.pone.0138785.
  20. Jarnevich C S, Hayes M A, Fitzgerald L A, Yackel Adams A A, Falk B G, Collier M A M, Bonewell L R, Klug P Naretto E S, Reed R N, Modeling the Distributions of Tegu Lizards in Native and Potential Invasive Ranges, Sci Rep, 8(2018)10193; doi.org/10.1038/s41598-018- 28468-w.
  21. Murphy J C, Jowers M J, Lehtinen R M, Charles S P, Colli G R, Peres A K (Jr), Hendry C R, Pyron R A, Cryptic, sympatric diversity in tegu lizards of the Tupinambis teguixin group (Squamata, Sauria, Teiidae) and the description of three new species, PLoS One, 11(2016)1–30.
  22. Manes M E, Principles for the Productive Breeding of Tegu Lizards. Bilingual Spanish-English Edition. Facultad de Agronomía y Zootecnia, Universidad Nacional de Tucumán, Tucumán, Argentina. 2016
  23. Campos-Casal F H, Cortez F A, Gomez E I, Chamut S N, Chemical Composition and Microstructure of Recently Oviposited Eggshells of Salvator merianae (Squamata: Teiidae), Herpetol Conserv Biol, 15 (2020)25–40.
  24. Choi S, Han S, Kim N H, Lee Y N, A Comparative Study of Eggshells of Gekkota With Morphological, Chemical Compositional and Crystallographic Approaches and its Evolutionary Implications. PloS One, 13(2018)1–31.
  25. Goor O J G M, Hendrikse S I S, Dankers P Y W, Meijer E W. From Supramolecular Polymers to Multi-Component Biomaterials, Chem Soc Rev, 46(2017)6621–6637.
  26. Committee for the Update of the Guide for the Care and Use of Laboratory Animals. 8th edn, National Academy of Sciences, USA, 2011.
  27. Karnovsky M J, A Formaldehyde-Glutaraldehyde Fixative of High Osmolality For Use in Electron Microscopy, J Cell Biol, 27(1965)137–138A.
  28. Suvarna K, Layton C, Bancroft J D, Bancroft’s Theory and Practice of Histological Techniques. 7th edn. Churchill Livingstone Elsevier, (eds). London, UK, 2008.
  29. Junqueira L C U U, Bignolas G, Brentani R R, Picrosirius Staining Plus Polarization Microscopy, a Specific Method for Collagen Detection in Tissue Sections, Histochem J, 11(1979)447–455.
  30. Martoja R, Martoja PM, Técnicas de Histología Animal. 1ra Edición. Toray-Masson, (eds) Barcelona, España.1970.
  31. Baer C K, Guidelines on euthanasia of nondomestic animals. Yulee Fla, American Association of Zoo Veterinarians (eds). Florida, USA. 2006, p. 111.
  32. Savitzky A, Golay M J E, Smoothing and Differentiation of Data by Simplified Least Squares Procedures, Anal Chem, 36(1964)1627–1639.
  33. Rizo G, Roldán-Olarte M, Miceli D C, Jiménez L E, Álvarez R M S, Structural modifications induced by an in vitro maturation process in zona pellucida glycoproteins of bovine oocytes. A Raman microspectroscopy análisis, RSC Adv, 6(2016)83429–83437.
  34. Berton A, Godeau G, Emonard H, Baba K, Bellon P, Hornebeck W, Bellon G, Analysis of the ex vivo specificity of human gelatinases A and B towards skin collagen and elastic fibers by computerized morphometry, Matrix Biol, 19(2000)139–148.
  35. Vogel B, Siebert H, Hofmann U, Frantz S, Determination of collagen content within picrosirius red stained paraffin-embedded tissue sections using fluorescence microscopy, Methods X, 2(2015)124–134.
  36. Dayan D, Hiss Y, Hirshberg A, Bubis J J, Wolman M, Are the polarization colors of Picrosirius red-stained collagen determined only by the diameter of the fibers?, Histochemistry, 93(1989)27–29.
  37. Montes G S, Junqueira L C U, The use of the Picrosirus-polarization method for the study of the biopathology of collagen, Mem Inst Oswaldo Cruz, 86(1991)1–11.
  38. Sexton O J, Veith G M, Phillips D M, Ultrastructure of the eggshell of two species of anoline lizards, J Exp Zool, 207(1979)227–236.
  39. Chang Y, Chen P Y, Hierarchical structure and mechanical properties of snake (Naja atra) and turtle (Ocadia sinensis) eggshells, Acta Biomater, 31(2016)33–49.
  40. Kodali V K, Gannon S A, Paramasivam S, Raje S, Polenova T, Thorpe C, A novel disulfide-rich protein motif from avian eggshell membranes, PloS One, 6(2011)1–11.
  41. Revell C K, Jensen O E, Shearer T, Lu Y, Holmes D F, Kadler K E, Collagen fibril assembly: New approaches to unanswered questions, Matrix Biol Plus, 12(2021)100079; doi.org/10.1016/j.mbplus.2021.100079.
  42. Al Makhzoomi A K, Kirk T B, Dye D E, Allison G T, Contribution of glycosaminoglycans to the structural and mechanical properties of tendons – A multiscale study, J Biomech, 128(2021)110796; doi.org/10.1016/j.jbiomech.2021.110796.
  43. Jimenez L E, Roldán-Olarte M, Álvarez R M S, Raman Microscopy Analysis of the Biochemical Changes in the Cytoplasm of Bovine Oocytes Induced by an In Vitro Maturation Process: Interference of the Zona Pellucida, ChemistrySelect, 4(2019)3706 –3716.
  44. Kuzuhara A, Fujiwara N, Hori T, Analysis of internal structure changes in black human hair keratin fibers with aging using Raman spectroscopy, Biopolymers, 87(2007)134–140.
  45. Essendoubi M, Meunier M, Scandolera A, Gobinet C, Manfait M, Lambert C, Auriol D, Reynaud R, Piot O, Conformation changes in human hair keratin observed using confocal Raman spectroscopy after active ingredient application, Int J Cosmet Sci, 41(2019)203–212.
  46. Garcia Martinez M, Bullock A J, MacNeil S, Rehman I U, Characterisation of structural changes in collagen with Raman spectroscopy, Appl Spectrosc Rev, 54(2019)509–542.
  47. Bonifacio A, Beleites C, Vittur F, Marsich E, Semeraro S, Paoletti S, Sergo V, Chemical imaging of articular cartilage sections with Raman mapping, employing uni- and multi-variate methods for data analysis, Analyst, 135(2010)3193–3204.
  48. Feng X, Fox M C, Reichenberg J S, Lopes F C P S, Sebastian K R, Markey M K, Tunnell J W, Biophysical basis of skin cancer margin assessment using Raman spectroscopy, Biomed Opt Express, 10(2019)104; doi.org/10.1364/boe.10.000104.
  49. Nguyen T T, Gobinet C, Feru J, Brassart-Pasco S, Manfait M, Piot O, Characterization of type I and IV collagens by Raman microspectroscopy: Identification of spectral markers of the dermo-epidermal junction, Spectrosc Int J, 27(2012)421–427.
  50. Cárcamo J J, Aliaga A E, Clavijo R E, Brañes M R, Campos-Vallette M M, Raman study of the shockwave effect on collagens, Spectrochim Acta, 86A(2012)360–365.
  51. Rintoul L, Carter E A, Stewart S D, Fredericks P M, Keratin orientation in wool and feathers by polarized Raman spectroscopy, Biopolymers, 57(2000)19–28.
  52. Bazylewski P, Divigalpitiya R, Fanchini G, In situ Raman spectroscopy distinguishes between reversible and irreversible thiol modifications in l-cysteine, RSC Advances, 7(2017)2964–2970.
  53. Alimova A, Chakraverty R, Muthukattil R, Elder S, Katz A, Sriramoju V, Lipper S, Alfano R R, (2009). In vivo molecular evaluation of guinea pig skin incisions healing after surgical suture and laser tissue welding using Raman spectroscopy, J Photochem Photobiol B Biol, 96(2009)178–183.
  54. Kim J, Feng J, Jones C A R, Mao X, Sander L M, Levine H, Sun B, Stress-induced plasticity of dynamic collagen networks, Nat Commun, 8(2017)842; doi.org/10.1038/s41467-017-01011-7.
  55. Trauth S E, Fagerberg W R, Ultrastructure and stereology of the eggshell in Cnemidophorus sexlineatus (Lacertilia: Teiidae), Copeia, (1984)826–832; doi.org/10.2307/1445324.
  56. Trauth S E, McAllister C T, Chen W, Microscopic eggshell characteristics in the Collared Lizard, Crotaphytus collaris (Sauria: Crotaphytidae), Southwest Nat, 39(1994)45–52.
  57. Grolik M, Szczubialka K, Wowra B, Dobrowolski D, Orzechowska-Wylegala B, Wylegala E, Nowakowska M, Corneal epithelial scaffolds based on chitosan membranes containing collagen and keratin, Int J Polym Mater, 64(2014)140–148.

Article 

Biopolymers-in-the-eggshell-of-the-Argentine-Black-and-White-Tegu-Salvator-merianae-a-Raman-microscopy-studyDownload

Related Posts