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Paleoproteomics is a relatively young and rapidly growing field of molecular science in which proteomics-based sequencing technology is used to resolve species identification and evolutionary relationships of extinct taxa. While complementary to paleogenomics in application, the study of ancient proteins has the potential to reveal older, more complete phylogenies due to the relative stability of amino acids in proteins as compared to the nucleic acids of DNA.[1] Ancient protein studies can further reveal types and sources of recovered tissues,[2] as well as the developmental stages of fossilized specimens.[3] Paleoproteomics can also be extended to archaeological materials such as textiles, animal skins, food remains, and pottery.

Background

Philip Abelson first characterized the findings of ancient amino acid residues from fossilized materials in 1955, proposing that the peptide bonds of proteins might persist for millions of years.[4] These initial discoveries were limited by available methodologies, and so protein sequencing remained an elusive idea for almost four decades. In 2000, mass spectrometry (MS) revealed the presence of osteocalcin in ancient bone samples[5] and ignited a renewed interest in protein’s potential as a tool for molecular paleonotology.[6]

The development of higher resolution instruments further increased the efficiency and depth of ancient protein recovery. In 2012, the first extended fossil bone proteome from a Pleistocene mammoth femur was confidently retrieved and identified,[7] strengthening the future of paleoproteomics research.

Paleoproteomes

Collagen Type I

The analysis of ancient bone proteomes has primarily focused on the identification of collagen type I (COL1), the dominant protein found in mineralized tissues[1],[8],.[9] Collagen is highly conserved across species[10] and comprises about 90% of organic bone compounds. Fibrillar collagens, of which COL1 is categorized, are thought to have evolved from a common metazoan ancestor,[11] thus contributing to their abundance and importance in the fossil record.  

Collagen has also been found to survive much longer than other non-collagenous proteins in fossilized specimens,[12] and the protein remains intact beyond the degradation of ancient DNA (aDNA)[1],.[9] Its tightly coiled triple-helical structure (consisting of two genetically identical alpha-1 chains and a third genetically distinct alpha-2 chain)[10] and hydrophobic composition[1] also make this protein an excellent candidate for survival, even in temperate and humid climates that support the rapid break down of organic molecules.[10]

The taxonomic resolution of collagen has been thoroughly investigated, and it is known that amino acid substitutions can be resolved to the genus level in most medium and large mammals.[1] Species-level identification is also possible, even in small mammal remains from high thermal climates.[13] It is for these reasons that COL1 remains a key protein in paleoproteomics and phylogenetic investigations.

Non-collagenous Proteins

The remaining 10% of organic bone molecules are non-collagenous proteins (NCPs). The most abundant NCP, osteocalcin, is a bone and dentin protein involved in bone assembly, often used as a marker for the bone formation process. Preserved osteocalcin was first detected via mass spectrometry (MALDI-MS) in 10,000 year-old bison bone and a 53-year-old walrus bone,[5] revealing phylogenetic reconstruction potential beyond the temporal limits of aDNA.

More advanced proteomic techniques have enabled the investigation of additional NCPs present in the bone extracellular matrix. Though type I collagen is the longest lived protein identified in fossilized bone specimens, the identification and sequencing of NCPs may allow for a greater taxonomic resolution than collagen-based methods[8],.[12]

Other Proteins

Proteomic analysis has also been applied to other fossilized and ancient materials. The examination of damaged artifacts through the sequencing of their keratin peptides[14] has allowed researchers to discriminate between horn and hoof remains of important species used at archeological sites. The keratin of textiles and animal skins worn by Ötzi, the Iceman, were also identified using peptide mass fingerprinting (PMF) from the ancient samples and from reference species.[15] Immune response proteins have illuminated the presence of infections and diseases in multiple studies of mummified human remains.[8] Additionally, the identification of egg proteins, caseins, whey globulins, and other proteinaceous materials used as binders in the paint of historical artworks has allowed for a better understanding of proper conservation methods.[8]

Sequencing Methods

Analysis of a fossil sample begins with demineralization of the bone/tooth mineral matrix. Trypsin is commonly used to digest the protein residues into peptides which can then be purified and analyzed.[9]

Peptide mass fingerprinting

Peptide mass fingerprinting (PMF) is an analytical technique that can be applied to the digested protein mixture. The masses of the unknown peptides can be detected with a mass spectrometer like MALDI (matrix-assisted laser desorption/ionization) or ESI (electrospray ionization), combined with a mass analyzer,[1] and then compared to masses of peptides that are predicted to derive from known proteins.[9]  

Liquid Chromatography-Tandem Mass Spectrometry

The inclusion of liquid chromatography (LC) solvents can enhance peptide electrospray ionization.[9] When combined with mass spectrometry, this allows for a much greater number of peptide ions to be analyzed with improved fragment spectra.[1] Liquid chromatography-mass spectrometry LC-MS can then be performed for peptide mass fingerprinting; however, liquid chromatography-tandem mass spectrometry (LC-MS/MS) is most often used in the case of ancient proteome analysis due to the nature of these complex samples.

De Novo Sequencing

At the present time, protein databases remain limited to particular taxa, so novel protein sequences that differ greatly from those available will not be identified via the protein search engines.[1] Manual interpretation through de novo sequencing remains a viable solution until these databases become more robust, and this technique will allow for identification of amino acid substitutions not previously reported.[16]

A hybrid solution of error-tolerant search algorithms that use protein sequence databases while allowing amino acid substitutions may similarly enable the identification of novel single amino acid polymorphisms (SAPs).[9]

Challenges

Dinosaur Collagen

A 2007 study sparked excitement in the world of paleontology, revealing the alleged discovery of endogenous collagen peptides in 68 mya Tyrannosaurus rex fossils.[17] This claim purported survival beyond experimental decay rates,[6] leading to a storm of controversy in the emerging field. The same team again reported finding similar collagen peptide sequence matches in 2009 from 80 mya hadrosaur fossils belonging to Brachylophosaurus canadensis.[18]

Subsequent studies have reanalyzed the original T. rex sequence data to infer that the sample was predominantly laboratory contaminants, soil bacteria, and bird-like hemoglobin and collagen;[19] the former protein is typically only seen in relatively recent samples[7],.[12] Another exceptionally preserved hadrosaur from the Hell Creek Formation (USA), yielded none of the previous findings despite extensive testing, and only the presence of protein breakdown products were detected[20]

Further experimentation demonstrated that contamination from other specimens present in the T. rex lab cannot be ruled out. Every peptide that was considered unique to both dinosaurs in the 2009 study could be matched to modern ostrich with much greater confidence than could be placed on their own, unique identifications[21]

While there have been several methods described to support the authenticity of paleoproteomics, including immunological or amino acid composition and racemization data, both of these approaches have limitations and are known to yield false-positive reactions in fossils.[22] Great care must be taken to rule out contamination by determining whether sequences differ from those of all extant taxa present in the laboratory environments.[21] Deamidation has also been proposed as an effective method for distinguishing between endogenous and contaminating NCPs, when extraction protocols may permit for this evaluation[9]

Future Perspectives

Paleoproteomics is still a field in its infancy, with most complex proteomes only being discovered in the last decade. However, more and more data is being produced and published each year, adding to protein sequence databases and increasing the potential for sequence matching and appropriate taxonomic relationships to be elucidated. The understanding of protein diagenesis under different environmental conditions will also undoubtedly improve our understanding of temporal survival in the fossil record.

Current proteomic methods greatly suffer from the fact that it is not a true form of sequencing, relying on probability-matching against expected results. While several MS methods are being employed to increase the robustness of retrievable data, these techniques also increase the sensitivities to contamination.[1] It must therefore be imperative to eliminate the possibility of contaminants from experimental data.

Instrumentational capabilities and new methodologies are likely to contribute to further understanding of ancient proteomes, the applications of which may also contribute to the fields of paleontology, archaeology, evolutionary biology, and beyond.

References

  1. ^ a b c d e f g h i Buckley, Michael (2019), Lindqvist, Charlotte; Rajora, Om P. (eds.), "Paleoproteomics: An Introduction to the Analysis of Ancient Proteins by Soft Ionisation Mass Spectrometry", Paleogenomics: Genome-Scale Analysis of Ancient DNA, Population Genomics, Cham: Springer International Publishing, pp. 31–52, doi:10.1007/13836_2018_50, ISBN 978-3-030-04753-5, retrieved 2021-03-20
  2. ^ Buckley, Michael; Harvey, Virginia L.; Chamberlain, Andrew T. (July 2017). "Species identification and decay assessment of Late Pleistocene fragmentary vertebrate remains from Pin Hole Cave (Creswell Crags, UK) using collagen fingerprinting". Boreas. 46 (3): 402–411. doi:10.1111/bor.12225.
  3. ^ Sawafuji, Rikai; Cappellini, Enrico; Nagaoka, Tomohito; Fotakis, Anna K.; Jersie-Christensen, Rosa Rakownikow; Olsen, Jesper V.; Hirata, Kazuaki; Ueda, Shintaroh (June 2017). "Proteomic profiling of archaeological human bone". Royal Society Open Science. 4 (6): 161004. Bibcode:2017RSOS....461004S. doi:10.1098/rsos.161004. ISSN 2054-5703. PMC 5493901. PMID 28680659.
  4. ^ Abelson, Philip (1955). "Paleobiochemistry: organic constituents of fossils". Yearbook. 54: 107–109 – via Carnegie Institution of Washington.
  5. ^ a b Ostrom, Peggy H; Schall, Michael; Gandhi, Hasand; Shen, Tun-Li; Hauschka, Peter V; Strahler, John R; Gage, Douglas A (March 2000). "New strategies for characterizing ancient proteins using matrix-assisted laser desorption ionization mass spectrometry". Geochimica et Cosmochimica Acta. 64 (6): 1043–1050. Bibcode:2000GeCoA..64.1043O. doi:10.1016/S0016-7037(99)00381-6.
  6. ^ a b Nielsen-Marsh, Christina (2002-06-01). "Biomolecules in fossil remains: Multidisciplinary approach to endurance". The Biochemist. 24 (3): 12–14. doi:10.1042/bio02403012. ISSN 0954-982X.
  7. ^ a b Cappellini, Enrico; Jensen, Lars J.; Szklarczyk, Damian; Ginolhac, Aurélien; da Fonseca, Rute A. R.; Stafford, Thomas W.; Holen, Steven R.; Collins, Matthew J.; Orlando, Ludovic; Willerslev, Eske; Gilbert, M. Thomas P. (2011-12-14). "Proteomic Analysis of a Pleistocene Mammoth Femur Reveals More than One Hundred Ancient Bone Proteins". Journal of Proteome Research. 11 (2): 917–926. doi:10.1021/pr200721u. ISSN 1535-3893. PMID 22103443.
  8. ^ a b c d Giuffrida, Maria Gabriella; Mazzoli, Roberto; Pessione, Enrica (2018-05-08). "Back to the past: deciphering cultural heritage secrets by protein identification". Applied Microbiology and Biotechnology. 102 (13): 5445–5455. doi:10.1007/s00253-018-8963-z. hdl:2318/1670455. ISSN 0175-7598. PMID 29737392. S2CID 13691178.
  9. ^ a b c d e f g Cappellini, Enrico; Prohaska, Ana; Racimo, Fernando; Welker, Frido; Pedersen, Mikkel Winther; Allentoft, Morten E.; de Barros Damgaard, Peter; Gutenbrunner, Petra; Dunne, Julie; Hammann, Simon; Roffet-Salque, Mélanie (2018-06-20). "Ancient Biomolecules and Evolutionary Inference". Annual Review of Biochemistry. 87 (1): 1029–1060. doi:10.1146/annurev-biochem-062917-012002. ISSN 0066-4154. PMID 29709200.
  10. ^ a b c Buckley, Michael (2015-05-07). "Ancient collagen reveals evolutionary history of the endemic South American 'ungulates'". Proceedings of the Royal Society B: Biological Sciences. 282 (1806): 20142671. doi:10.1098/rspb.2014.2671. ISSN 0962-8452. PMC 4426609. PMID 25833851.
  11. ^ Rodriguez-Pascual, Fernando; Slatter, David Anthony (December 2016). "Collagen cross-linking: insights on the evolution of metazoan extracellular matrix". Scientific Reports. 6 (1): 37374. Bibcode:2016NatSR...637374R. doi:10.1038/srep37374. ISSN 2045-2322. PMC 5120351. PMID 27876853.
  12. ^ a b c Wadsworth, Caroline; Buckley, Mike (2014-03-30). "Proteome degradation in fossils: investigating the longevity of protein survival in ancient bone: Proteome degradation in fossils". Rapid Communications in Mass Spectrometry. 28 (6): 605–615. doi:10.1002/rcm.6821. PMC 4282581. PMID 24519823.
  13. ^ Buckley, Michael; Harvey, Virginia L; Orihuela, Johanset; Mychajliw, Alexis M; Keating, Joseph N; Milan, Juan N Almonte; Lawless, Craig; Chamberlain, Andrew T; Egerton, Victoria M; Manning, Phillip L (2020-10-01). Teeling, Emma (ed.). "Collagen Sequence Analysis Reveals Evolutionary History of Extinct West Indies Nesophontes (Island-Shrews)". Molecular Biology and Evolution. 37 (10): 2931–2943. doi:10.1093/molbev/msaa137. ISSN 0737-4038. PMC 7530613. PMID 32497204.
  14. ^ Solazzo, Caroline; Wadsley, Marc; Dyer, Jolon M.; Clerens, Stefan; Collins, Matthew J.; Plowman, Jeffrey (2013-12-15). "Characterisation of novel α-keratin peptide markers for species identification in keratinous tissues using mass spectrometry: Novel α-keratin peptide markers for species identification". Rapid Communications in Mass Spectrometry. 27 (23): 2685–2698. doi:10.1002/rcm.6730. PMID 24591030.
  15. ^ Hollemeyer, Klaus; Altmeyer, Wolfgang; Heinzle, Elmar; Pitra, Christian (2008-09-30). "Species identification of Oetzi's clothing with matrix-assisted laser desorption/ionization time-of-flight mass spectrometry based on peptide pattern similarities of hair digests". Rapid Communications in Mass Spectrometry. 22 (18): 2751–2767. Bibcode:2008RCMS...22.2751H. doi:10.1002/rcm.3679. PMID 18720427.
  16. ^ Cappellini, E.; Collins, M. J.; Gilbert, M. T. P. (2014-03-20). "Unlocking Ancient Protein Palimpsests". Science. 343 (6177): 1320–1322. Bibcode:2014Sci...343.1320C. doi:10.1126/science.1249274. ISSN 0036-8075. S2CID 32042460.
  17. ^ Schweitzer, M. H.; Suo, Z.; Avci, R.; Asara, J. M.; Allen, M. A.; Arce, F. T.; Horner, J. R. (2007-04-13). "Analyses of Soft Tissue from Tyrannosaurus rex Suggest the Presence of Protein". Science. 316 (5822): 277–280. Bibcode:2007Sci...316..277S. doi:10.1126/science.1138709. ISSN 0036-8075. PMID 17431179. S2CID 42153727.
  18. ^ Schweitzer, M. H.; Zheng, W.; Organ, C. L.; Avci, R.; Suo, Z.; Freimark, L. M.; Lebleu, V. S.; Duncan, M. B.; Vander Heiden, M. G.; Neveu, J. M.; Lane, W. S. (2009-04-30). "Biomolecular Characterization and Protein Sequences of the Campanian Hadrosaur B. canadensis". Science. 324 (5927): 626–631. Bibcode:2009Sci...324..626S. doi:10.1126/science.1165069. ISSN 0036-8075. PMID 19407199. S2CID 5358680.
  19. ^ Bern, Marshall; Phinney, Brett S.; Goldberg, David (2009-09-04). "Reanalysis of Tyrannosaurus rex Mass Spectra". Journal of Proteome Research. 8 (9): 4328–4332. doi:10.1021/pr900349r. ISSN 1535-3893. PMC 2738754. PMID 19603827.
  20. ^ Manning, Phillip L.; Morris, Peter M.; McMahon, Adam; Jones, Emrys; Gize, Andy; Macquaker, Joe H. S.; Wolff, George; Thompson, Anu; Marshall, Jim; Taylor, Kevin G.; Lyson, Tyler (2009-10-07). "Mineralized soft-tissue structure and chemistry in a mummified hadrosaur from the Hell Creek Formation, North Dakota (USA)". Proceedings of the Royal Society B: Biological Sciences. 276 (1672): 3429–3437. doi:10.1098/rspb.2009.0812. ISSN 0962-8452. PMC 2817188. PMID 19570788.
  21. ^ a b Buckley, Michael; Warwood, Stacey; van Dongen, Bart; Kitchener, Andrew C.; Manning, Phillip L. (2017-05-31). "A fossil protein chimera; difficulties in discriminating dinosaur peptide sequences from modern cross-contamination". Proceedings of the Royal Society B: Biological Sciences. 284 (1855): 20170544. doi:10.1098/rspb.2017.0544. ISSN 0962-8452. PMC 5454271. PMID 28566488.
  22. ^ Lendaro, Eugenio; Ippoliti, Rodolfo; Bellelli, Andrea; Brunori, Maurizio; Zito, Romano; Citro, Gennaro; Ascenzi, Antonio (November 1991). "On the problem of immunological detection of antigens in skeletal remains". American Journal of Physical Anthropology. 86 (3): 429–432. doi:10.1002/ajpa.1330860308. ISSN 0002-9483. PMID 1746647.
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