Deep-time phylogenetic inference by paleoproteomic analysis of dental enamel

Alberto J. Taurozzi, Patrick L. Rüther, Ioannis Patramanis, Claire Koenig, Ryan Sinclair Paterson, Palesa P. Madupe, Florian Simon Harking, Frido Welker, Meaghan Mackie, Jazmín Ramos-Madrigal, Jesper V. Olsen, Enrico Cappellini

Published: 2024-04-26 DOI: 10.1038/s41596-024-00975-3

mass spectrometry

paleoproteomics

phylogenetic inference

dental enamel

ancient proteins

AI 解读

Supplementary information

Reporting Summary

Efficient and safe single-cell cloning of human pluripotent stem cells using the CEPT cocktail

Profiling native pulmonary basement membrane stiffness using atomic force microscopy

Genetic circuit design automation with Cello 2.0

Synthesis of siRNA nanoparticles to silence plaque-destabilizing gene in atherosclerotic lesional macrophages

Scalable dual-omics profiling with single-nucleus chromatin accessibility and mRNA expression sequencing 2 (SNARE-seq2)

A practical guide to scanning light-field microscopy with digital adaptive optics

Effective high-throughput isolation of fully human antibodies targeting infectious pathogens

Improved sampling and DNA extraction procedures for microbiome analysis in food-processing environments

MOF-derived nanoporous carbons with diverse tunable nanoarchitectures

Tutorial: a statistical genetics guide to identifying HLA alleles driving complex disease

查看全部

Sections

Figures

References

Supplementary information

Madupe, P. P. et al. Enamel proteins reveal biological sex and genetic variability within southern African Paranthropus. Preprint at bioRxiv http://doi.org/10.1101/2023.07.03.547326 (2023).
Higuchi, R., Bowman, B., Freiberger, M., Ryder, O. A. & Wilson, A. C. DNA sequences from the quagga, an extinct member of the horse family. Nature 312, 282–284 (1984).
Pääbo, S., Gifford, J. A. & Wilson, A. C. Mitochondrial DNA sequences from a 7000-year old brain. Nucleic Acids Res. 16, 9775–9787 (1988).
Hagelberg, E. & Clegg, J. B. Isolation and characterization of DNA from archaeological bone. Proc. Biol. Sci. 244, 45–50 (1991).
Poinar, H. N. et al. Metagenomics to paleogenomics: large-scale sequencing of mammoth DNA. Science 311, 392–394 (2006).
Willerslev, E. et al. Ancient biomolecules from deep ice cores reveal a forested southern Greenland. Science 317, 111–114 (2007).
Rasmussen, M. et al. Ancient human genome sequence of an extinct Palaeo-Eskimo. Nature 463, 757–762 (2010).
Green, R. E. et al. A draft sequence of the Neandertal genome. Science 328, 710–722 (2010).
Orlando, L. et al. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 499, 74–78 (2013).
van der Valk, T. et al. Million-year-old DNA sheds light on the genomic history of mammoths. Nature 591, 265–269 (2021).
Meyer, M. et al. A mitochondrial genome sequence of a hominin from Sima de los Huesos. Nature 505, 403–406 (2014).
Lipson, M. et al. Ancient DNA and deep population structure in sub-Saharan African foragers. Nature 603, 290–296 (2022).
Cappellini, E. et al. Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny. Nature 574, 103–107 (2019).
Welker, F. et al. Enamel proteome shows that Gigantopithecus was an early diverging pongine. Nature 576, 262–265 (2019).
Welker, F. et al. The dental proteome of Homo antecessor. Nature 580, 235–238 (2020).
Warinner, C., Korzow Richter, K. & Collins, M. J. Paleoproteomics. Chem. Rev. 122, 13401–13446 (2022).
Olsen, J. V., Ong, S.-E. & Mann, M. Trypsin cleaves exclusively C-terminal to arginine and lysine residues. Mol. Cell. Proteom. 3, 608–614 (2004).
Stewart, N. A., Gerlach, R. F., Gowland, R. L., Gron, K. J. & Montgomery, J. Sex determination of human remains from peptides in tooth enamel. Proc. Natl Acad. Sci. USA 114, 13649–13654 (2017).
Cappellini, E. et al. Proteomic analysis of a pleistocene mammoth femur reveals more than one hundred ancient bone proteins. J. Proteome Res. 11, 917–926 (2012).
Mackie, M. et al. Palaeoproteomic profiling of conservation layers on a 14th century Italian wall painting. Angew. Chem. 57, 7369–7374 (2018).
Rappsilber, J., Mann, M. & Ishihama, Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896–1906 (2007).
Parker, G. J. et al. Sex estimation using sexually dimorphic amelogenin protein fragments in human enamel. J. Archaeol. Sci. 101, 169–180 (2019).
Rappsilber, J., Ishihama, Y. & Mann, M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663–670 (2003).
Peng, W., Pronker, M. F. & Snijder, J. Mass spectrometry-based de novo sequencing of monoclonal antibodies using multiple proteases and a dual fragmentation scheme. J. Proteome Res. 20, 3559–3566 (2021).
Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367–1372 (2008).
Cox, J. et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794–1805 (2011).
Zhang, J. et al. PEAKS DB: de novo sequencing assisted database search for sensitive and accurate peptide identification. Mol. Cell. Proteom. 11, M111.010587 (2012).
Orlando, L. et al. Ancient DNA analysis. Nat. Rev. Methods Prim. 1, 1–26 (2021).
Renaud, G., Schubert, M., Sawyer, S. & Orlando, L. Authentication and assessment of contamination in ancient DNA. Methods Mol. Biol. 1963, 163–194 (2019).
Radzicka, A. & Wolfenden, R. Rates of uncatalyzed peptide bond hydrolysis in neutral solution and the transition state affinities of proteases. J. Am. Chem. Soc. 118, 6105–6109 (1996).
Iwata, T. et al. Processing of ameloblastin by MMP-20. J. Dent. Res. 86, 153–157 (2007).
Yamakoshi, Y., Hu, J. C.-C., Fukae, M., Yamakoshi, F. & Simmer, J. P. How do enamelysin and kallikrein 4 process the 32-kDa enamelin? Eur. J. Oral. Sci. 114, 45–51 (2006). 379–80.
van Doorn, N. L., Wilson, J., Hollund, H., Soressi, M. & Collins, M. J. Site-specific deamidation of glutamine: a new marker of bone collagen deterioration. Rapid Commun. Mass Spectrom. 26, 2319–2327 (2012).
Schroeter, E. R. & Cleland, T. P. Glutamine deamidation: an indicator of antiquity, or preservational quality? Rapid Commun. Mass Spectrom. 30, 251–255 (2016).
Ramsøe, A. et al. DeamiDATE 1.0: site-specific deamidation as a tool to assess authenticity of members of ancient proteomes. J. Archaeol. Sci. 115, 105080 (2020).
Tagliabracci, V. S. et al. Secreted kinase phosphorylates extracellular proteins that regulate biomineralization. Science 336, 1150–1153 (2012).
Penkman, K. E. H., Kaufman, D. S., Maddy, D. & Collins, M. J. Closed-system behaviour of the intra-crystalline fraction of amino acids in mollusc shells. Quat. Geochronol. 3, 2–25 (2008).
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
Katoh, K., Misawa, K., Kuma, K.-I. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002).
Kearse, M. et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).
Xiao, Y., Vecchi, M. M. & Wen, D. Distinguishing between leucine and isoleucine by integrated LC–MS analysis using an orbitrap fusion mass spectrometer. Anal. Chem. 88, 10757–10766 (2016).
Gabriels, R., Martens, L. & Degroeve, S. Updated MS2PIP web server delivers fast and accurate MS2 peak intensity prediction for multiple fragmentation methods, instruments and labeling techniques. Nucleic Acids Res. 47, W295–W299 (2019).
Tiwary, S. et al. High-quality MS/MS spectrum prediction for data-dependent and data-independent acquisition data analysis. Nat. Methods 16, 519–525 (2019).
Gessulat, S. et al. Prosit: proteome-wide prediction of peptide tandem mass spectra by deep learning. Nat. Methods 16, 509–518 (2019).
Wilhelm, M. et al. Deep learning boosts sensitivity of mass spectrometry-based immunopeptidomics. Nat. Commun. 12, 3346 (2021).
Gilbert, C. et al. Species identification of ivory and bone museum objects using minimally invasive proteomics. Sci. Adv. 10, eadi9028 (2024).
Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).
Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).
Patramanis, I., Ramos-Madrigal, J., Cappellini, E. & Racimo, F. PaleoProPhyler: a reproducible pipeline for phylogenetic inference using ancient proteins. Peer Community J. 3, e112 (2023).
Pamilo, P. & Nei, M. Relationships between gene trees and species trees. Mol. Biol. Evol. http://doi.org/10.1093/oxfordjournals.molbev.a040517 (1988).
Takahata, N. Gene genealogy in three related populations: consistency probability between gene and population trees. Genetics 122, 957–966 (1989).
Maddison, W. P. Gene trees in species trees. Syst. Biol. 46, 523–536 (1997).
Nichols, R. Gene trees and species trees are not the same. Trends Ecol. Evol. 16, 358–364 (2001).
Hobolth, A., Dutheil, J. Y., Hawks, J., Schierup, M. H. & Mailund, T. Incomplete lineage sorting patterns among human, chimpanzee, and orangutan suggest recent orangutan speciation and widespread selection. Genome Res. 21, 349–356 (2011).
Mailund, T., Munch, K. & Schierup, M. H. Lineage sorting in apes. Annu. Rev. Genet. 48, 519–535 (2014).
Sousa, F., Bertrand, Y. J. K., Doyle, J. J., Oxelman, B. & Pfeil, B. E. Using genomic and coalescent simulation to investigate gene tree discordance in Medicago L. Syst. Biol. 66, 934–949 (2017).
Scally, A. et al. Insights into hominid evolution from the gorilla genome sequence. Nature 483, 169–175 (2012).
Huerta-Sánchez, E. et al. Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA. Nature 512, 194–197 (2014).
Lanier, H. C., Huang, H. & Knowles, L. L. How low can you go? The effects of mutation rate on the accuracy of species-tree estimation. Mol. Phylogenet. Evol. 70, 112–119 (2014).
Yu, Y., Yu, Y., Smith, M. & Pieper, R. A spinnable and automatable StageTip for high throughput peptide desalting and proteomics. Protoc. Exch. http://doi.org/10.1038/protex.2014.033 (2014).
Prüfer, K. et al. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505, 43–49 (2014).
UniProt: the universal protein knowledgebase. Nucleic Acids Res. 45, D158–D169 (2017).
O’Leary, N. A. et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 44, D733–D745 (2016).
Hall, T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95–98 (1999).
Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).
Posada, D. & Crandall, K. A. MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818 (1998).
Demarchi, B. et al. Protein sequences bound to mineral surfaces persist into deep time. eLife 5, e17092 (2016).
Lacruz, R. S., Habelitz, S., Wright, J. T. & Paine, M. L. Dental enamel formation and implications for oral health and disease. Physiol. Rev. 97, 939–993 (2017).
Blausen.com staff. Medical gallery of Blausen Medical 2014. WikiJournal Med. http://doi.org/10.15347/wjm/2014.010 (2014).
Ahmadi, S. & Winter, D. Identification of poly(ethylene glycol) and poly(ethylene glycol)-based detergents using peptide search engines. Anal. Chem. 90, 6594–6600 (2018).
Bartlett, J. D. Dental enamel development: proteinases and their enamel matrix substrates. ISRN Dent. 2013, 684607 (2013).
Lu, Y. et al. Functions of KLK4 and MMP-20 in dental enamel formation. Biol. Chem. 389, 695–700 (2008).
The UniProt Consortium. UniProt: the Universal Protein Knowledgebase in 2023. Nucleic Acids Res. 51, D523–D531 (2023).
Sayers, E. W. et al. Database resources of the national center for biotechnology information. Nucleic Acids Res. 50, D20–D26 (2022).
Clark, K., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. & Sayers, E. W. GenBank. Nucleic Acids Res. 44, D67–D72 (2016).
The NCBI C++ Toolkit. National Center for Biotechnology Information (2003).
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
Prüfer, K. et al. Computational challenges in the analysis of ancient DNA. Genome Biol. 11, R47 (2010).
Hendy, J. et al. A guide to ancient protein studies. Nat. Ecol. Evol. 2, 791–799 (2018).

Deep-time phylogenetic inference by paleoproteomic analysis of dental enamel

Supplementary information

Reporting Summary

推荐阅读