The oral microbiome plays key roles in human biology, health, and disease, but little is known about the global diversity, variation, or evolution of this microbial community. To better understand the evolution and changing ecology of the human oral microbiome, we analyzed 124 dental biofilm metagenomes from humans, including Neanderthals and Late Pleistocene to present-day modern humans, chimpanzees, and gorillas, as well as New World howler monkeys for comparison. We find that a core microbiome of primarily biofilm structural taxa has been maintained throughout African hominid evolution, and these microbial groups are also shared with howler monkeys, suggesting that they have been important oral members since before the catarrhine-platyrrhine split ca. 40 Mya. However, community structure and individual microbial phylogenies do not closely reflect host relationships, and the dental biofilms of Homo and chimpanzees are distinguished by major taxonomic and functional differences. Reconstructing oral metagenomes from up to 100 thousand years ago, we show that the microbial profiles of both Neanderthals and modern humans are highly similar, sharing functional adaptations in nutrient metabolism. These include an apparent Homo-specific acquisition of salivary amylase-binding capability by oral streptococci, suggesting microbial coadaptation with host diet. We additionally find evidence of shared genetic diversity in the oral bacteria of Neanderthal and Upper Paleolithic modern humans that is not observed in later modern human populations. Differences in the oral microbiomes of African hominids provide insights into human evolution, the ancestral state of the human microbiome, and a temporal framework for understanding microbial health and disease.

Animal Ecology Department of Ecology and Genetics Uppsala University 75236 Uppsala Sweden

Anthropology Program California State University Channel Islands Camarillo CA 93012

Berliner Gesellschaft für Anthropologie Ethnologie und Urgeschichte 10117 Berlin Germany

Centre for Human Evolution Research The Natural History Museum London SW7 5BD United Kingdom

Centre for Palaeogenetics 10691 Stockholm Sweden

Clínica Alboraya 10 46010 València Spain

Clínica Dental Grande Mateu 46004 València Spain

De la Préhistoire à l'Actuel Culture Environnement et Anthropologie CNRS UMR 5199 Université de Bordeaux 33615 Pessac France

Departament de Prehistòria Historia i Arqueología Universitat de València 46010 València Spain

Departamento de Prehistòria y Arqueología Universidad Nacional de Educación 28040 Madrid Spain

Departamento de Zoología y Antropología Física Universidad de Murcia 30100 Murcia Spain

Department of Anthropology California State University Northridge CA 91330

Department of Anthropology Harvard University Cambridge MA 02138

Department of Anthropology Masaryk University 61137 Brno Czech Republic

Department of Anthropology University of New Mexico Albuquerque NM 87131

Department of Anthropology University of Oklahoma Norman OK 73019

Department of Anthropology University of South Florida St Petersburg FL 33701

Department of Anthropology University of Winnipeg Winnipeg MB R3T 3C7 Canada

Department of Anthropology Western University London ON N6A 5C2 Canada

Department of Archaeogenetics Max Planck Institute for Evolutionary Anthropology 04103 Leipzig Germany

Department of Archaeogenetics Max Planck Institute for the Science of Human History 07745 Jena Germany

Department of Archaeology Faculty of Philosophy University of Belgrade 11000 Belgrade Serbia

Department of Archaeology Max Planck Institute for the Science of Human History 07745 Jena Germany

Department of Bioinformatics and Genetics Swedish Museum of Natural History 10405 Stockholm Sweden

Department of Geological Sciences University of Cape Town Rondebosch 7701 South Africa

Department of Human Evolution Max Planck Institute for Evolutionary Anthropology 04103 Leipzig Germany

Department of Human Evolutionary Biology Harvard University Cambridge MA 02138

Department of Humanities University of Ferrara 44121 Ferrara Italy

Department of Microbiology and Plant Biology University of Oklahoma Norman OK 73019

Department of Microbiology Immunology and Genetics University of North Texas Health Science Center Fort Worth TX 76107

Department of Microbiology The Forsyth Institute Cambridge MA 02142

Deutsche Forschungsgemeinschaft Centre for Advanced Studies Words Bones Genes Tools Eberhard Karls University of Tübingen 72070 Tübingen Germany

Division of Clinical Anatomy and Biological Anthropology Department of Human Biology University of Cape Town Cape Town 7925 South Africa

Escribano Escrivá Clínica Dental 38003 Santa Cruz de Tenerife Spain

Faculty of Archaeology Leiden University 2333CC Leiden The Netherlands

Grupo de Investigación en Prehistòria IT 1223 19 Ikerbasque Basque Foundation for Science 01006 Vitoria Gasteiz Spain

Institut für Ur und Frühgeschichte und Archäologie des Mittelalters Eberhard Karls University of Tübingen 72074 Tübingen Germany

Institute for Archaeological Sciences Eberhard Karls University of Tübingen 72070 Tübingen Germany

Institute for Pre and Protohistoric Archaeology and Archaeology of the Roman Provinces Ludwig Maximilians University Münich 80539 Münich Germany

Institute of Archaeology at Brno Czech Academy of Sciences 60200 Brno Czech Republic

Institute of Environmental Geology and Geoengineering National Research Council Milano Lombardia 20126 Italy

Instituto Internacional de Investigaciones Prehistóricas de Cantabria Universidad de Cantabria Gobierno de Cantabria Banco 39071 Santander Spain

Laboratoire Chronoenvironnement CNRS UMR 6249 25030 Besançon France

Laboratories of Molecular Anthropology and Microbiome Research University of Oklahoma Norman OK 73019

Landesamt für Denkmalpflege im Regierungspräsidium Stuttgart 78467 Konstanz Germany

McDonald Institute for Archaeological Research University of Cambridge Cambridge CB2 3ER United Kingdom

Museum für Vor und Frühgeschichte Berlin Stiftung Preussischer Kulturbesitz 10117 Berlin Germany

Natural History Museum University of Oslo 0562 Oslo Norway

Oral Medicine Infection and Immunity Harvard School of Dental Medicine Boston MA 02115

Palaeobiology Biogeology Department of Geosciences Eberhard Karls University of Tübingen 72074 Tübingen Germany

Paleoanthropology Institute of Archaeological Sciences Eberhard Karls University of Tübingen 72070 Tübingen Germany

Prehistoria Departamento de Historia Geografía y Comunicación Universidad de Burgos 09001 Burgos Spain

School of Human Evolution and Social Change Arizona State University Tempe AZ 85287

Science for Life Laboratory 75237 Uppsala Sweden

Senckenberg Centre for Human Evolution and Palaeoenviroment Eberhard Karls University of Tübingen 72074 Tübingen Germany

Service Régional d'Archéologie de Bourgogne Franche Comté Direction Régionale des Affaires Culturelles Bourgogne Franche Comté 25043 Besançon France

Sonderforschungsbereiche 1070 Ressourcen Kulturen Eberhard Karls University of Tübingen 72074 Tübingen Germany

000      

00000naa a2200000 a 4500

001      

bmc22004338

003      

CZ-PrNML

005      

20220127145330.0

007      

ta

008      

220113s2021 xxu f 000 0|eng||

009      

AR

024    7_

$a 10.1073/pnas.2021655118 $2 doi

035    __

$a (PubMed)33972424

040    __

$a ABA008 $b cze $d ABA008 $e AACR2

041    0_

$a eng

044    __

$a xxu

100    1_

$a Fellows Yates, James A $u Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07745 Jena, Germany; fellows@shh.mpg.de warinner@shh.mpg.de $u Institute for Pre- and Protohistoric Archaeology and Archaeology of the Roman Provinces, Ludwig-Maximilians-University Münich, 80539 Münich, Germany

245    14

$a The evolution and changing ecology of the African hominid oral microbiome / $c JA. Fellows Yates, IM. Velsko, F. Aron, C. Posth, CA. Hofman, RM. Austin, CE. Parker, AE. Mann, K. Nägele, KW. Arthur, JW. Arthur, CC. Bauer, I. Crevecoeur, C. Cupillard, MC. Curtis, L. Dalén, M. Díaz-Zorita Bonilla, JC. Díez Fernández-Lomana, DG. Drucker, E. Escribano Escrivá, M. Francken, VE. Gibbon, MR. González Morales, A. Grande Mateu, K. Harvati, AG. Henry, L. Humphrey, M. Menéndez, D. Mihailović, M. Peresani, S. Rodríguez Moroder, M. Roksandic, H. Rougier, S. Sázelová, JT. Stock, LG. Straus, J. Svoboda, B. Teßmann, MJ. Walker, RC. Power, CM. Lewis, K. Sankaranarayanan, K. Guschanski, RW. Wrangham, FE. Dewhirst, DC. Salazar-García, J. Krause, A. Herbig, C. Warinner

520    9_

$a The oral microbiome plays key roles in human biology, health, and disease, but little is known about the global diversity, variation, or evolution of this microbial community. To better understand the evolution and changing ecology of the human oral microbiome, we analyzed 124 dental biofilm metagenomes from humans, including Neanderthals and Late Pleistocene to present-day modern humans, chimpanzees, and gorillas, as well as New World howler monkeys for comparison. We find that a core microbiome of primarily biofilm structural taxa has been maintained throughout African hominid evolution, and these microbial groups are also shared with howler monkeys, suggesting that they have been important oral members since before the catarrhine-platyrrhine split ca. 40 Mya. However, community structure and individual microbial phylogenies do not closely reflect host relationships, and the dental biofilms of Homo and chimpanzees are distinguished by major taxonomic and functional differences. Reconstructing oral metagenomes from up to 100 thousand years ago, we show that the microbial profiles of both Neanderthals and modern humans are highly similar, sharing functional adaptations in nutrient metabolism. These include an apparent Homo-specific acquisition of salivary amylase-binding capability by oral streptococci, suggesting microbial coadaptation with host diet. We additionally find evidence of shared genetic diversity in the oral bacteria of Neanderthal and Upper Paleolithic modern humans that is not observed in later modern human populations. Differences in the oral microbiomes of African hominids provide insights into human evolution, the ancestral state of the human microbiome, and a temporal framework for understanding microbial health and disease.

650    _2

$a zvířata $7 D000818

650    _2

$a Bacteria $x klasifikace $x genetika $7 D001419

650    _2

$a biofilmy $7 D018441

650    12

$a biologická evoluce $7 D005075

650    _2

$a zubní plak $x mikrobiologie $7 D003773

650    _2

$a ekologie $x metody $7 D004463

650    _2

$a zeměpis $7 D005843

650    _2

$a Gorilla gorilla $x mikrobiologie $7 D006071

650    _2

$a Hominidae $x klasifikace $x mikrobiologie $7 D015186

650    _2

$a lidé $7 D006801

650    _2

$a metagenom $x genetika $7 D054892

650    _2

$a mikrobiota $x genetika $7 D064307

650    _2

$a ústa $x mikrobiologie $7 D009055

650    _2

$a Pan troglodytes $x mikrobiologie $7 D002679

650    _2

$a fylogeneze $7 D010802

651    _2

$a Afrika $7 D000349

655    _2

$a časopisecké články $7 D016428

655    _2

$a práce podpořená grantem $7 D013485

700    1_

$a Velsko, Irina M $u Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07745 Jena, Germany

700    1_

$a Aron, Franziska $u Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07745 Jena, Germany

700    1_

$a Posth, Cosimo $u Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07745 Jena, Germany $u Institute for Archaeological Sciences, Eberhard Karls University of Tübingen, 72070 Tübingen, Germany

700    1_

$a Hofman, Courtney A $u Department of Anthropology, University of Oklahoma, Norman, OK 73019 $u Laboratories of Molecular Anthropology and Microbiome Research, University of Oklahoma, Norman, OK 73019

700    1_

$a Austin, Rita M $u Department of Anthropology, University of Oklahoma, Norman, OK 73019 $u Laboratories of Molecular Anthropology and Microbiome Research, University of Oklahoma, Norman, OK 73019 $u Natural History Museum, University of Oslo, 0562 Oslo, Norway

700    1_

$a Parker, Cody E $u Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07745 Jena, Germany $u School of Human Evolution and Social Change, Arizona State University, Tempe, AZ 85287

700    1_

$a Mann, Allison E $u Department of Microbiology, Immunology and Genetics, University of North Texas Health Science Center, Fort Worth, TX 76107

700    1_

$a Nägele, Kathrin $u Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07745 Jena, Germany

700    1_

$a Arthur, Kathryn Weedman $u Department of Anthropology, University of South Florida, St. Petersburg, FL 33701

700    1_

$a Arthur, John W $u Department of Anthropology, University of South Florida, St. Petersburg, FL 33701

700    1_

$a Bauer, Catherine C $u Palaeobiology, Biogeology, Department of Geosciences, Eberhard Karls University of Tübingen, 72074 Tübingen, Germany

700    1_

$a Crevecoeur, Isabelle $u De la Préhistoire à l'Actuel: Culture, Environnement et Anthropologie (PACEA), CNRS UMR 5199, Université de Bordeaux, 33615 Pessac, France

700    1_

$a Cupillard, Christophe $u Laboratoire Chronoenvironnement, CNRS UMR 6249, 25030 Besançon, France $u Service Régional d'Archéologie de Bourgogne-Franche-Comté, Direction Régionale des Affaires Culturelles (DRAC) Bourgogne-Franche-Comté, 25043 Besançon, France

700    1_

$a Curtis, Matthew C $u Anthropology Program, California State University Channel Islands, Camarillo, CA 93012

700    1_

$a Dalén, Love $u Centre for Palaeogenetics, 10691 Stockholm, Sweden $u Department of Bioinformatics and Genetics, Swedish Museum of Natural History, 10405 Stockholm, Sweden

700    1_

$a Díaz-Zorita Bonilla, Marta $u Institut für Ur- und Frühgeschichte und Archäologie des Mittelalters, Eberhard Karls University of Tübingen, 72074 Tübingen, Germany $u Sonderforschungsbereiche 1070 Ressourcen Kulturen, Eberhard Karls University of Tübingen, 72074 Tübingen, Germany

700    1_

$a Díez Fernández-Lomana, J Carlos $u Prehistoria, Departamento de Historia, Geografía y Comunicación, Universidad de Burgos, 09001 Burgos, Spain

700    1_

$a Drucker, Dorothée G $u Senckenberg Centre for Human Evolution and Palaeoenviroment, Eberhard Karls University of Tübingen, 72074 Tübingen, Germany

700    1_

$a Escribano Escrivá, Elena $u Escribano Escrivá Clínica Dental, 38003 Santa Cruz de Tenerife, Spain

700    1_

$a Francken, Michael $u Landesamt für Denkmalpflege im Regierungspräsidium Stuttgart, 78467 Konstanz, Germany

700    1_

$a Gibbon, Victoria E $u Division of Clinical Anatomy and Biological Anthropology, Department of Human Biology, University of Cape Town, Cape Town 7925, South Africa

700    1_

$a González Morales, Manuel R $u Instituto Internacional de Investigaciones Prehistóricas de Cantabria, Universidad de Cantabria-Gobierno de Cantabria-Banco, 39071 Santander, Spain

700    1_

$a Grande Mateu, Ana $u Clínica Dental Grande Mateu, 46004 València, Spain

700    1_

$a Harvati, Katerina $u Senckenberg Centre for Human Evolution and Palaeoenviroment, Eberhard Karls University of Tübingen, 72074 Tübingen, Germany $u Paleoanthropology, Institute of Archaeological Sciences, Eberhard Karls University of Tübingen, 72070 Tübingen, Germany $u Deutsche Forschungsgemeinschaft Centre for Advanced Studies "Words, Bones, Genes, Tools," Eberhard Karls University of Tübingen, 72070 Tübingen, Germany

700    1_

$a Henry, Amanda G $u Faculty of Archaeology, Leiden University, 2333CC Leiden, The Netherlands

700    1_

$a Humphrey, Louise $u Centre for Human Evolution Research, The Natural History Museum, London SW7 5BD, United Kingdom

700    1_

$a Menéndez, Mario $u Departamento de Prehistòria y Arqueología, Universidad Nacional de Educación, 28040 Madrid, Spain

700    1_

$a Mihailović, Dušan $u Department of Archaeology, Faculty of Philosophy, University of Belgrade, 11000 Belgrade, Serbia

700    1_

$a Peresani, Marco $u Department of Humanities, University of Ferrara, 44121 Ferrara, Italy $u Institute of Environmental Geology and Geoengineering, National Research Council, Milano, Lombardia, 20126, Italy

700    1_

$a Rodríguez Moroder, Sofía $u Clínica Alboraya 10, 46010 València, Spain

700    1_

$a Roksandic, Mirjana $u Department of Anthropology, University of Winnipeg, Winnipeg, MB R3T 3C7, Canada

700    1_

$a Rougier, Hélène $u Department of Anthropology, California State University, Northridge, CA 91330

700    1_

$a Sázelová, Sandra $u Institute of Archaeology at Brno, Czech Academy of Sciences, 60200 Brno, Czech Republic

700    1_

$a Stock, Jay T $u Department of Anthropology, Western University, London, ON N6A 5C2, Canada $u Department of Archaeology, Max Planck Institute for the Science of Human History, 07745 Jena, Germany $u McDonald Institute for Archaeological Research, University of Cambridge, Cambridge CB2 3ER, United Kingdom

700    1_

$a Straus, Lawrence Guy $u Department of Anthropology, University of New Mexico, Albuquerque, NM 87131

700    1_

$a Svoboda, Jiří $u Institute of Archaeology at Brno, Czech Academy of Sciences, 60200 Brno, Czech Republic $u Department of Anthropology, Masaryk University, 61137 Brno, Czech Republic

700    1_

$a Teßmann, Barbara $u Museum für Vor- und Frühgeschichte Berlin, Stiftung Preussischer Kulturbesitz, 10117 Berlin, Germany $u Berliner Gesellschaft für Anthropologie, Ethnologie und Urgeschichte, 10117 Berlin, Germany

700    1_

$a Walker, Michael J $u Departamento de Zoología y Antropología Física, Universidad de Murcia, 30100 Murcia, Spain

700    1_

$a Power, Robert C $u Institute for Pre- and Protohistoric Archaeology and Archaeology of the Roman Provinces, Ludwig-Maximilians-University Münich, 80539 Münich, Germany $u Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany

700    1_

$a Lewis, Cecil M $u Department of Anthropology, University of Oklahoma, Norman, OK 73019

700    1_

$a Sankaranarayanan, Krithivasan $u Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019

700    1_

$a Guschanski, Katerina $u Animal Ecology, Department of Ecology and Genetics, Uppsala University, 75236 Uppsala, Sweden $u Science for Life Laboratory, 75237 Uppsala, Sweden $u Faculty of Archaeology, Leiden University, 2333CC Leiden, The Netherlands

700    1_

$a Wrangham, Richard W $u Department of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138

700    1_

$a Dewhirst, Floyd E $u Department of Microbiology, The Forsyth Institute, Cambridge, MA 02142 $u Oral Medicine, Infection, and Immunity, Harvard School of Dental Medicine, Boston, MA 02115

700    1_

$a Salazar-García, Domingo C $u Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany $u Grupo de Investigación en Prehistòria IT-1223-19 (Universidad del País Vasco-Euskal Herriko Unibertsitatea), Ikerbasque, Basque Foundation for Science, 01006 Vitoria-Gasteiz, Spain $u Departament de Prehistòria, Historia i Arqueología, Universitat de València, 46010 València, Spain $u Department of Geological Sciences, University of Cape Town, Rondebosch 7701, South Africa

700    1_

$a Krause, Johannes $u Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07745 Jena, Germany $u Department of Archaeogenetics, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany

700    1_

$a Herbig, Alexander $u Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07745 Jena, Germany

700    1_

$a Warinner, Christina $u Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07745 Jena, Germany; fellows@shh.mpg.de warinner@shh.mpg.de $u Department of Anthropology, University of Oklahoma, Norman, OK 73019 $u Department of Anthropology, Harvard University, Cambridge, MA 02138

773    0_

$w MED00010472 $t Proceedings of the National Academy of Sciences of the United States of America $x 1091-6490 $g Roč. 118, č. 20 (2021)

856    41

$u https://pubmed.ncbi.nlm.nih.gov/33972424 $y Pubmed

910    __

$a ABA008 $b sig $c sign $y p $z 0

990    __

$a 20220113 $b ABA008

991    __

$a 20220127145326 $b ABA008

999    __

$a ok $b bmc $g 1751714 $s 1155487

BAS    __

$a 3

BAS    __

$a PreBMC

BMC    __

$a 2021 $b 118 $c 20 $e 20210518 $i 1091-6490 $m Proceedings of the National Academy of Sciences of the United States of America $n Proc Natl Acad Sci U S A $x MED00010472

GRA    __

$a R01 DE024468 $p NIDCR NIH HHS $2 United States

GRA    __

$a R01 GM089886 $p NIGMS NIH HHS $2 United States

GRA    __

$a R37 DE016937 $p NIDCR NIH HHS $2 United States

LZP    __

$a Pubmed-20220113