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Enamel Proteome Shows That Gigantopithecus Was an Early Enamel proteome shows that Gigantopithecus was an early diverging pongine Frido Welker, Jazmín Ramos-Madrigal, Martin Kuhlwilm, Wei Liao, Petra Gutenbrunner, Marc de Manuel, Diana Samodova, Meaghan Mackie, Morten Allentoft, Anne-Marie Bacon, et al. To cite this version: Frido Welker, Jazmín Ramos-Madrigal, Martin Kuhlwilm, Wei Liao, Petra Gutenbrunner, et al.. Enamel proteome shows that Gigantopithecus was an early diverging pongine. Nature, Nature Pub- lishing Group, 2019, 576, pp.262-265. 10.1038/s41586-019-1728-8. hal-03021856 HAL Id: hal-03021856 https://hal.archives-ouvertes.fr/hal-03021856 Submitted on 24 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Article Enamel proteome shows that Gigantopithecus was an early diverging pongine https://doi.org/10.1038/s41586-019-1728-8 Frido Welker1*, Jazmín Ramos-Madrigal1, Martin Kuhlwilm2, Wei Liao3,4, Petra Gutenbrunner5, Marc de Manuel2, Diana Samodova6, Meaghan Mackie1,6, Morten E. Allentoft7, Received: 21 June 2019 Anne-Marie Bacon8, Matthew J. Collins1,9, Jürgen Cox5, Carles Lalueza-Fox2, Jesper V. Olsen6, Accepted: 3 October 2019 Fabrice Demeter7,10, Wei Wang11*, Tomas Marques-Bonet2,12,13,14* & Enrico Cappellini1* Published online: 13 November 2019 Gigantopithecus blacki was a giant hominid that inhabited densely forested environments of Southeast Asia during the Pleistocene epoch1. Its evolutionary relationships to other great ape species, and the divergence of these species during the Middle and Late Miocene epoch (16–5.3 million years ago), remain unclear2,3. Hypotheses regarding the relationships between Gigantopithecus and extinct and extant hominids are wide ranging but difficult to substantiate because of its highly derived dentognathic morphology, the absence of cranial and post-cranial remains1,3–6, and the lack of independent molecular validation. We retrieved dental enamel proteome sequences from a 1.9-million-year-old G. blacki molar found in Chuifeng Cave, China7,8. The thermal age of these protein sequences is approximately five times greater than that of any previously published mammalian proteome or genome. We demonstrate that Gigantopithecus is a sister clade to orangutans (genus Pongo) with a common ancestor about 12–10 million years ago, implying that the divergence of Gigantopithecus from Pongo forms part of the Miocene radiation of great apes. In addition, we hypothesize that the expression of alpha-2-HS- glycoprotein, which has not been previously observed in enamel proteomes, had a role in the biomineralization of the thick enamel crowns that characterize the large molars in Gigantopithecus9,10. The survival of an Early Pleistocene dental enamel proteome in the subtropics further expands the scope of palaeoproteomic analysis into geographical areas and time periods previously considered incompatible with the preservation of substantial amounts of genetic information. G. blacki is an extinct, potentially giant hominid species that once inhab- To address the evolutionary relationships between Gigantopithecus ited Asia. It was first discovered and identified by von Koenigswald in 1935, and extant hominoids, we performed protein extractions on dentine when he described an isolated tooth that he found in a Hong Kong drug- and enamel samples of a single molar (CF-B-16) found in Chuifeng Cave, store11. The entire G. blacki fossil record, dated between the Early Pleis- China (Extended Data Figs. 1, 2), that has been morphologically assigned tocene (about 2 million years ago (Ma)) and the late Middle Pleistocene to G. blacki7,8. The site has been dated, using multiple approaches, to (about 0.3 Ma)12, includes thousands of teeth and four partial mandibles 1.9 ± 0.2 Ma. We processed enamel and dentine samples using recently from subtropical Southeast Asia1,13,14. All the locations at which G. blacki established digestion-free protocols that were optimized for extremely remains have been found are in or near southern China, stretching from degraded ancient proteomes17 (see Methods). Enamel deminerali- Longgupo Cave, just south of the Yangtze River, to the Xinchong Cave zation was replicated using two acids, trifluoroacetic acid (TFA) and on Hainan Island and, possibly, into northern Vietnam and Thailand15,16. hydrochloric acid (HCl). 1Evolutionary Genomics Section, Globe Institute, University of Copenhagen, Copenhagen, Denmark. 2Institute of Evolutionary Biology (UPF-CSIC), University Pompeu Fabra, Barcelona, Spain. 3School of Earth Sciences, China University of Geosciences, Wuhan, China. 4Anthropology Museum of Guangxi, Nanning, China. 5Computational Systems Biochemistry, Max Planck Institute of Biochemistry, Martinsried, Germany. 6Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, Copenhagen, Denmark. 7Lundbeck Foundation GeoGenetics Centre, Globe Institute, University of Copenhagen, Copenhagen, Denmark. 8CNRS FRE 2029 BABEL, Université Paris Descartes, Faculté de Chirurgie Dentaire, Paris, France. 9Department of Archaeology, University of Cambridge, Cambridge, UK. 10UMR7206 Eco-anthropologie, Muséum national d’Histoire naturelle, Musée de l’Homme, Paris, France. 11Institute of Cultural Heritage, Shandong University, Qingdao, China. 12Catalan Institution of Research and Advanced Studies (ICREA), Barcelona, Spain. 13Centre for Genomic Regulation (CNAG-CRG), Barcelona Institute of Science and Technology, Barcelona, Spain. 14Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Barcelona, Spain. *e-mail: [email protected]; [email protected]; [email protected]; [email protected] Nature | www.nature.com | 1 Article Ellesmere Island 30 Happisburgh Thistle Creek Dmanisi Sima de Olduvai los Huesos Chuifeng Cave Olduvai & Laetoli Chuifeng Cave 20 Laetoli Dmanisi 10 Sima de los Huesos Happisburgh 0 Thistle Creek Mean annual temperature (ºC) –10 Collagen DNA Eggshell Enamel Ellesmere Island –20 100 1,000 10,000 100,0001,000,00010,000,000 100,000,000 Age (years) Fig. 1 | Thermal age of Chuifeng Cave, China, in the subtropics of Southeast intervals based on a chronological age of 1.7 and 2.1 Ma, respectively. Inset, Asia. Chronological (circles) and thermal (coloured wedges, @10 °C) ages of geographical location of Chuifeng Cave in the subtropics of Southeast Asia (red other Cenozoic ancient genomes and proteomes are given for comparison. For asterisk). Base map was generated using public domain data from http://www. Chuifeng Cave, dark red shading indicates thermal age calculated at a naturalearthdata.com/. The red asterisk also encloses the entire known chronological age of 1.9 Ma and lighter shading indicates 95% confidence geographical range of G. blacki fossils. We identified no endogenous proteins from the dentine, but belonged to a female Gigantopithecus. Alternatively, male-diagnostic instead recovered an ancient enamel proteome composed of 409 AMELY-specific peptides were not observed due to their degradation unique peptides matching 6 endogenous proteins: amelogenin X beyond the limit of detection of the instrument. The endogenous (AMELX), ameloblastin (AMBN), amelotin (AMTN), enamelin (ENAM), enamel proteome sequence coverage of 456 amino acids is lower than matrix metalloproteinase-20 (MMP20) and alpha-2-HS-glycoprotein the previously recovered sequence coverage for a Dmanisi Stepha- (AHSG, also known as FETUA; Extended Data Table 1). This observa- norhinus specimen (875 amino acids17; Supplementary Table 1). This tion extends the survival of ancient mammalian proteins to a thermal observation is consistent with the older thermal age for Chuifeng Cave, age, obtained by normalizing the chronological age to a constant tem- compared to Dmanisi17. perature of 10 °C, of approximately 11.8 million years (Myr)@10 °C We replicated enamel demineralization using two acids (TFA and (Extended Data Table 2). Such a thermal age is well beyond the ther- HCl). The chromatograms of these two extracts showed that different mally oldest DNA (0.25 Myr@10 °C, Sima de los Huesos, Spain18), col- peptide populations were released (Extended Data Fig. 3). Owing to the lagen (0.22 Myr@10 °C, Happisburgh, UK19) and enamel proteome partial acidic hydrolysis22, which potentially occurs alongside deminer- (2.2 Myr@10 °C, Dmanisi, Georgia17) reported to date. The Chuifeng alization, peptide populations with a wider range of acidity (Extended Cave enamel proteome is thus, to our knowledge, the oldest Cenozoic Data Fig. 4a) and hydrophobicity (Extended Data Fig. 4c) are gener- skeletal proteome currently reported (Fig. 1). The survival of a subtropi- ated using TFA. Our TFA-based demineralization returned 127 more cal proteome from approximately 2 Ma suggests that chronologically unique non-overlapping peptide sequences than did the HCl-based older specimens from higher latitudes are likely to contain preserved demineralization (Extended Data Fig. 4e). The TFA extract, therefore, ancient proteomes as well. outperformed the HCl-based extraction, despite being carried out on The content of the recovered enamel proteome
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