Validation of a Non-Targeted LC-MS Approach for Identifying Ancient Proteins: Method Development on Bone to Improve Artifact Residue Analysis
Abstract
Identification of protein residues from prehistoric cooking pottery using mass spectrometry is challenging because proteins are removed from original tissues, are degraded from cooking, may be poorly preserved due to diagenesis, and occur in a palimpsest of exogenous soil proteins. In contrast, bone proteins are abundant and well preserved. This research is part of a larger method-development project for innovation and improvement of liquid chromatography – mass spectrometry analysis of protein residues from cooking pottery; here we validate the potential of our extraction and characterization approach via application to ancient bone proteins. Because of its preservation potential for proteins and given that our approach is destructive, ancient bone identified via skeletal morphology represents an appropriate verification target. Proteins were identified from zooarchaeological turkey (Meleagris gallopavo Linnaeus Phasianidae), rabbit (Lagomorpha), and squirrel (Sciuridae) remains excavated from ancient pueblo archaeological sites in southwestern Colorado using a non-targeted LC-MS/MS approach. The data have been deposited to the ProteomeXchange Consortium with the dataset identifier PXD002440. Improvement of highly sensitive targeted LC-MS/MS approaches is an avenue for future method development related to the study of protein residues from artifacts such as stone tools and pottery.
References
Ascenzi, A., M. Brunori, G. Citro, and R. Zito. 1985. Immunological Detection of Hemoglobin in Bones of Ancient Roman Times and of Iron and Eneolithic Ages. Proceedings of the National Academy of Sciences 82:7170-7172.
Badenhorst, S., and J. C. Driver. 2009. Faunal Changes in Farming Communities from Basketmaker II to Pueblo III (AD 1-1300) in the San Juan Basin of the American Southwest. Journal of Archaeological Science 36:1832-1841. Doi:10.1016/j.jas.2009.04.006.
Barker, A. 2011. Archaeological Protein Residues: New Data for Conservation Science. Ethnobiology Letters 1:58-65.
Barker, A., B. Venables, S. M. Stevens, Jr., K. W. Seeley, P. Wang, and S. Wolverton. 2012. An Optimized Approach for Protein Residue Extraction and identification from Ceramics after Cooking. Journal of Archaeological Method and Theory 19:407-439.
Barnard, H., L. Shoemaker, O. E. Craig, M. Rider, R. E. Parr, M. Q. Sutton, and R. M. Yohe II. 2007. Introduction to the Analysis of Protein Residues in Archaeological Ceramics. In Theory and Practice of Archaeological Residue Analysis, edited by H. Barnard, and J. W. Eerkens, pp. 216-228 Archaeopress, Oxford.
Buckley, M., M. Collins, J. Thomas-Oates, and J. C. Wilson. 2009. Species Identification by Analysis of Bone Collagen Using Matrix-Assisted Laser Desorption/Ionisation Time-of-Flight Mass Spectrometry. Rapid Communications in Mass Spectrometry 23:3843-3854. Doi:10.1002/rcm.4316.
Buckley, M., S. Fraser, J. Herman, N. D. Melton, J. Mulville, and A. H. Pálsdóttir. 2014. Species Identification of Archaeological Marine Mammals Using Collagen Fingerprinting. Journal of Archaeological Science 41:631-641. Doi:http://dx.doi.org/10.1016/j.jas.2013.08.021.
Buckley, M., S. W. Kansa, S. Howard, S. Campbell, J. Thomas-Oates, and M. Collins. 2010. Distinguishing between Archaeological Sheep and Goat Bones Using a Single Collagen Peptide. Journal of Archaeological Science 37:13-20.
Buckley, M. and C. Wadsworth. 2014. Protein Degradation in Ancient Bone: Diagenesis and Phylogenetic Potential. Paleogeography, Palaeoclimatology, Palaeoecology 416:69-79.
Cappellini, E., M. J. Collins, and M. T. P. Gilbert. 2014. Unlocking Ancient Protein Palimpsests. Science 343:1320-1322. Doi:10.1126/science.1249274.
Cappellini, E., M. T. P. Gilbert, F. Geuna, G. Fiorentino, A. Hall, J. Thomas-Oates, P. D. Ashton, D. A. Ashford, P. Arthur, P. F. Campos, J. Kool, E. Willerslev, and M. J. Collins. 2010. A Multidisciplinary Study of Archaeological Grape Seeds. Naturwissenschaften 97:205-217. Doi:10.1007/s00114-009-0629-3.
Cappellini, E., L. J. Jensen, D. Szklarczyk, A. Ginolhac, R. A. R. da Fonseca, T. W. Stafford, S. R. Holen, M. J. Collins, L. Orlando, E. Willerslev, M. T. P. Gilbert, and J. V. Olsen. 2012. Proteomic Analysis of a Pleistocene Mammoth Femur Reveals More Than One Hundred Ancient Bone Proteins. Journal of Proteome Research 11:917-926.
Carpenter, Meredith L., Jason D. Buenrostro, C. Valdiosera, H. Schroeder, Morten E. Allentoft, M. Sikora, M. Rasmussen, S. Gravel, S. Guillén, G. Nekhrizov, K. Leshtakov, D. Dimitrova, N. Theodossiev, D. Pettener, D. Luiselli, K. Sandoval, A. Moreno-Estrada, Y. Li, J. Wang, M. Thomas P. Gilbert, E. Willerslev, William J. Greenleaf, and Carlos D. Bustamante. 2013. Pulling out the 1%: Whole-Genome Capture for the Targeted Enrichment of Ancient DNA Sequencing Libraries. The American Journal of Human Genetics 93:852-864. Doi:http://dx.doi.org/10.1016/j.ajhg.2013.10.002.
Child, A. M. 1995. Towards and Understanding of the Microbial Decomposition of Archaeological Bone in the Burial Environment. Journal of Archaeological Science 22:165-174. Doi:http://dx.doi.org/10.1006/jasc.1995.0018.
Collins, M. J., C. M. Nielsen–Marsh, J. Hiller, C. I. Smith, J. P. Roberts, R. V. Prigodich, T. J. Wess, J. Csapo, A. R. Millard, and G. Turner–Walker. 2002. The Survival of Organic Matter in Bone: A Review. Archaeometry 44:383-394.
Dobberstein, R. C., M. J. Collins, O. E. Craig, G. Taylor, K. E. H. Penkman, and S. Ritz-Timme. 2009. Archaeological Collagen: Why Worry About Collagen Diagenesis? Archaeological and Anthropological Sciences 1:31-42. Doi:10.1007/s12520-009-0002-7.
Driver, J. C. 1992. Crow Canyon Archaeological Center Manual for Description of Vertebrate Remains. Crow Canyon Archaeological Center, Cortez, CO.
Driver, J. C. 2011. Identification, Classification and Zooarchaeology (Featured Reprint and Invited Comments). Ethnobiology Letters 1:19-39.
Fogel, M. L., and N. Tuross. 1999. Transformation of Plant Biochemicals to Geological Macromolecules During Early Diagenesis. Oecologia 120:336-346. Doi:10.1007/s004420050867.
Fritz, D. L., P. Vogel, D. R. Brown, D. Deshazer and D. M. Waag. 2000. Mouse Model of Sublethal and Lethal Intraperitoneal Glanders (Burkholderia mallei). Veterinary Pathology 37:626-636. Doi: 10.1354/vp.37-6-626.
Graves, H. C. B. 1988. The Effect of Surface Charge on Non-Specific Binding of Rabbit Immunoglobulin G in Solid-Phase Immunoassays. Journal of Immunological Methods 111:157-166. Doi:http://dx.doi.org/10.1016/0022-1759(88)90123-8.
Grupe, G., A. Balzer, and S. Turban-Just. 2000. Modeling Protein Diagenesis in Ancient Bone: Towards a Validation of Stable Isotope Data. In Biogeochemical Approaches to Paleodietary Analysis edited by S. H. Ambrose and M. A. Katzenburg, pp. 173-187. Kluwer Academic, New York.
Heaton, K., C. Solazzo, M. J. Collins, J. Thomas-Oates, and E. T. Bergström. 2009. Towards the Application of Desorption Electrospray Ionisation Mass Spectrometry (Desi-Ms) to the Analysis of Ancient Proteins from Artefacts. Journal of Archaeological Science 36:2145-2154. Doi:http://dx.doi.org/10.1016/j.jas.2009.05.016.
Keller, A., A. I. Nesvizhskii, E. Kolker, and R. Aebersold. 2002. Empirical Statistical Model to Estimate the Accuracy of Peptide Identifications Made by Ms/Ms and Database Search. Analytical Chemistry 74:5383-5392. Doi:10.1021/ac025747h.
Kooyman, B., M. E. Newman, C. Cluney, M. Lobb, S. Tolman, P. McNeil, and L.V. Hills. 2001. Identification of Horse Exploitation by Clovis Hunters Based on Protein Analysis. American Antiquity 66:686-691.
Lowenstein, J. M., J. D. Reuther, D. G. Hood, G. Scheuenstuhl, S. C. Gerlach, and D. H. Ubelaker. 2006. Identification of Animal Species by Protein Radioimmunoassay of Bone Fragments and Bloodstained Stone Tools. Forensic Science International 159:182-188.
Marlar, R. A., B. L. Banks, B. R. Billman, P. Lambert and J. E. Marlar. 2000. Biochemical Evidence of Cannibalism in a Prehistoric Pueblo Site in Southwestern Colorado. Nature 407:73-8. Doi:10.1038/35024064
Mikšík, I., P. Sedláková, S. Pataridis, F. Bortolotti, R. Gottardo, and F. Tagliaro. 2014. Prince Cangrande’s Collagen: Study of Protein Modification on the Mummy of the Lord of Verona, Italy (1291–1329 Ad). Chromatographia 77:1503-1510. Doi:10.1007/s10337-014-2710-0.
Moore, L. W., and G. Warren. 1979. Agrobacterium radiobacter Strain 84 and Biological Control of Crown Gall. Annual Review of Phytopathology 17:163-179.
Muir, R. J., and J. C. Driver. 2002. Scale of Analysis and Zooarchaeological Interpretation: Pueblo III Faunal Variation in the Northern San Juan Region. Journal of Anthropological Archaeology 21:165-199. Doi:10.1006/jaar.2001.0392.
Nesvizhskii, A. I., A. Keller, E. Kolker, and R. Aebersold. 2003. A Statistical Model for Identifying Proteins by Tandem Mass Spectrometry. Analytical Chemistry 75:4646-4658. Doi:10.1021/ac0341261.
Nielsen-Marsh, C. M., M. P. Richards, P. V. Hauschka, J. E. Thomas-Oates, E. Trinkaus, P. B. Pettitt, I. Karavanić, H. Poinar, and M. J. Collins. 2005. Osteocalcin Protein Sequences of Neanderthals and Modern Primates. Proceedings of the National Academy of Sciences of the United States of America 102:4409-4413. Doi:10.1073/pnas.0500450102.
San Antonio, J. D., M. H. Schweitzer, S. T. Jensen, R. Kalluri, M. Buckley, and J. P. R. O. Orgel. 2011. Dinosaur Peptides Suggest Mechanisms of Protein Survival. PLoS ONE 6:e20381. Doi:10.1371/journal.pone.0020381.
Smith, P. R., and M. T. Wilson. 1990. Detection of Haemoglobin in Human Skeletal Remains by Elisa. Journal of Archaeological Science 17:255-268. Doi:http://dx.doi.org/10.1016/0305-4403(90)90023-X.
Solazzo, C., W. W. Fitzhugh, C. Rolando, and C. Tokarski. 2008. Identification of Protein Remains in Archaeological Potsherds by Proteomics. Analytical Chemistry 80:4590-4597. Doi:10.1021/ac800515v.
Stevens, S. M., Jr., S. Wolverton, B. Venables, A. Barker, K. W. Seeley, and P. Adhikari. 2010. Evaluation of Microwave-Assisted Enzymatic Digestion and Tandem Mass Spectrometry for the Identification of Protein Residues from an Inorganic Solid Matrix: Implications in Archaeological Research. Analytical and Bioanalytical Chemistry 396:1491-1499. Doi:10.1007/s00216-009-3341-4.
Tuross, N. 1991. Recovery of Bone and Serum Proteins from Human Skeletal Tissue: Igg, Osteonectin, and Albumin. In Human Paleopathology: Current Syntheses and Future Options, edited by D. J. Ortner, and A. C. Aufderheide, pp. 51-54 Smithsonian Institution Press, Washington D.C.
van Doorn, N., H. Hollund, and M. Collins. 2011. A Novel and Non-Destructive Approach for Zooms Analysis: Ammonium Bicarbonate Buffer Extraction. Archaeological and Anthropological Sciences 3:281-289. Doi:10.1007/s12520-011-0067-y.
van Doorn, N. L., J. Wilson, H. Hollund, M. Soressi, and M. J. Collins. 2012. Site-Specific Deamidation of Glutamine: A New Marker of Bone Collagen Deterioration. Rapid Communications in Mass Spectrometry 26:2319-2327. Doi:10.1002/rcm.6351.
Vizcaino, J. A., Cote, R. G., Csordas, A., Dianes, J. A., Fabregat, A., Foster, J. M., et al. (2013). The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. [Research Support, Non-U.S. Gov't]. Nucleic acids research, 41(Database issue), D1063-1069.
Warinner, C., J. F. M. Rodrigues, R. Vyas, C. Trachsel, N. Shved, J. Grossmann, A. Radini, Y. Hancock, R. Y. Tito, S. Fiddyment, C. Speller, J. Hendy, S. Charlton, H. U. Luder, D. C. Salazar-Garcia, E. Eppler, R. Seiler, L. H. Hansen, J. A. S. Castruita, S. Barkow-Oesterreicher, K. Y. Teoh, C. D. Kelstrup, J. V. Olsen, P. Nanni, T. Kawai, E. Willerslev, C. von Mering, C. M. Lewis Jr, M. J. Collins, M. T. P. Gilbert, F. Ruhli, and E. Cappellini. 2014. Pathogens and Host Immunity in the Ancient Human Oral Cavity. Nat Genet 46:336-344. Doi:10.1038/ng.2906
Waterboer, T., P. Sehr, and M. Pawlita. 2006. Suppression of Non-Specific Binding in Serological Luminex Assays. Journal of Immunological Methods 309:200-204. Doi:http://dx.doi.org/10.1016/j.jim.2005.11.008.
Whitlock, G. C., D. M. Estes, and A. G. Torres. 2007. Glanders: Off to the Races with Burkholderia mallei. Microbiology Letters 277:115-122. Doi:http://dx.doi.org/10.1111/j.1574-6968.2007.00949.x.
Wiśniewski, J. R., A. Zougman, N. Nagaraj, and M. Mann. 2009. Universal Sample Preparation Method for Proteome Analysis. Nature Methods 6:359-362. Doi:10.1038/nmeth.1322.
Welker, F., M. J. Collins, J. A. Thomas, M. Wadsley, S. Brace, E. Cappellini, S. T. Turvey, M. Reguero, J. N. Gelfo, A. Kramarz, J. Burger, J. Thomas-Oates, D. A. Ashford, P. D. Ashton, K. Rowsell, D. M. Porter, B. Kessler, R. Fischer, C. Baessmann, S. Kaspar, J. V. Olsen, P. Kiley, J. A. Elliott, C. D. Kelstrup, V. Mullin, M. Hofreiter, E. Willerslev, J. Hublin, L. Orlando, I. Barnes, and R. D. E. MacPhee. 2015. Ancient Proteins Resolve the Evolutionary History of Darwin's South American Ungulates. Nature advance online publication. doi:10.1038/nature14249
Wolverton, S. 2013. Data Quality in Zooarchaeological Faunal Identification. Journal of Archaeological Method and Theory 20:381-396. Doi:10.1007/s10816-012-9161-4.
Wolverton, S., J. Dombrosky, and A. Barker. 2014. Paleoetnobiologia. In Introdução À Etnobiologia, edited by U. P. Albuquerque, pp. 43-51, NUPEEA, Recife.
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