Unexplored microbial diversity from 2,500 food metagenomes and links with the human microbiome.

food food microbiome human microbiome large-scale microbiome analysis metagenomic assembly metagenomics strain-level genomics unexplored microbial diversity

Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
16 Aug 2024
Historique:
received: 12 01 2024
revised: 17 05 2024
accepted: 23 07 2024
medline: 31 8 2024
pubmed: 31 8 2024
entrez: 30 8 2024
Statut: aheadofprint

Résumé

Complex microbiomes are part of the food we eat and influence our own microbiome, but their diversity remains largely unexplored. Here, we generated the open access curatedFoodMetagenomicData (cFMD) resource by integrating 1,950 newly sequenced and 583 public food metagenomes. We produced 10,899 metagenome-assembled genomes spanning 1,036 prokaryotic and 108 eukaryotic species-level genome bins (SGBs), including 320 previously undescribed taxa. Food SGBs displayed significant microbial diversity within and between food categories. Extension to >20,000 human metagenomes revealed that food SGBs accounted on average for 3% of the adult gut microbiome. Strain-level analysis highlighted potential instances of food-to-gut transmission and intestinal colonization (e.g., Lacticaseibacillus paracasei) as well as SGBs with divergent genomic structures in food and humans (e.g., Streptococcus gallolyticus and Limosilactobabillus mucosae). The cFMD expands our knowledge on food microbiomes, their role in shaping the human microbiome, and supports future uses of metagenomics for food quality, safety, and authentication.

Identifiants

DOI: 10.1016/j.cell.2024.07.039 PMID: 39214080
pubmed: 39214080
pii: S0092-8674(24)00833-X
doi: 10.1016/j.cell.2024.07.039
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Investigateurs

Avelino Alvarez-Ordóñez (A)
Pablo Alvarez (P)
Livio Antonielli (L)
Elke Arendt (E)
Federica Armanini (F)
Aurelie Aubry (A)
Jacob Baelum (J)
Coral Barcenilla (C)
Alejandro Belanche (A)
Yaiza Benavent-Gil (Y)
Tony Blake (T)
Aitor Blanco-Míguez (A)
Radhika Bongoni (R)
Mickael Boyer (M)
Fiona Brennan (F)
Samuel Breselge (S)
Helgi Briem (H)
Derek Butler (D)
Inés Calvete-Torre (I)
Omar Cristobal Carballo (OC)
Mireille Cardinal (M)
Niccolò Carlino (N)
Christian Chervaux (C)
Christine Chopin (C)
Natallia Clotaire (N)
Mairead Coakley (M)
José Francisco Cobo-Díaz (JF)
Jim Codd (J)
Stephen Conroy (S)
Karla Fabiola Corral-Jara (KF)
Karla-Fabiola Corral-Jara (KF)
Paul D Cotter (PD)
Gerard Coyne (G)
Gerard Coyne (G)
Chris Creevey (C)
Patricia D Cuevas (PD)
Brendan Curran (B)
Susana Delgado (S)
Liesbeth Derde (L)
Muriel Derrien (M)
Danilo Ercolini (D)
Ruth Gomez Exposito (RG)
María Mercedes López Fernández (MM)
Francesca De Filippis (F)
Daniel Fordham (D)
Hubert Galy (H)
Asimenia Gavriilidou (A)
Oddur Gunnarsson (O)
Buck Hanson (B)
Gerben Hermes (G)
Rongcai Huang (R)
Sharon Huws (S)
Israel Ikoyi (I)
Alice Jaeger (A)
Ian Jeffery (I)
Marc Jérôme (M)
Pierre-Alexandre Juan (PA)
David Kenny (D)
Annelies Kers (A)
Karim-Franck Khinouche (KF)
Stuart Kirwan (S)
Eline S Klaassens (ES)
Stephen Knobloch (S)
Kristinn Kolbeinsson (K)
Laetitia Kolypczuk (L)
Tanja Kostic (T)
Fabio Ledda (F)
John Leech (J)
Doerte Lehmann (D)
Françoise Leroi (F)
Eva Lewis (E)
Johanna Ley (J)
Eva Lucic (E)
Kieran Lynch (K)
Sabrina Mace (S)
Iain MacLaren-Lee (I)
Lisa Mahler de Sanchez (L)
Juergen Marchart (J)
Abelardo Margolles (A)
Viggó Thór Marteinsson (VT)
Giulia Masetti (G)
Fiona McGovern (F)
Noirin McHugh (N)
Steven McLoughlin (S)
Dara Meehan (D)
Lars Mølbak (L)
Thomas Monin (T)
Javier Moreno (J)
Diego Morgavi (D)
Steven Morrison (S)
Steffen Müench (S)
Ana Rute Ramos Neves (AR)
Emma Neylon (E)
Laura Nyhan (L)
Rhona O'Kelly (R)
Dominic O'Neil (D)
Paul O'Toole (P)
Abimael Ortiz-Chura (A)
Juan Manuel Palma (JM)
Edoardo Pasolli (E)
Delphine Passerini (D)
Milica Pastar (M)
Federica Pinto (F)
Walter Pirovano (W)
Olga Plans (O)
Marion Policht (M)
Aurel Pop (A)
Bianca Pop (B)
Milka Popova (M)
Miguel Prieto (M)
Narciso M Quijada (NM)
Antje Reiss (A)
Pedro Romero (P)
Patricia Ruas-Madiedo (P)
Francesco Rubino (F)
Raul Cabrera Rubio (RC)
Lorena Ruiz (L)
Angela Ryan (A)
Clodagh Ryan (C)
Carlos Sabater (C)
Aylin Sahin (A)
Cecile Salaun (C)
Fernanda Godoy Santos (FG)
Carolin Schneider (C)
Nicola Segata (N)
Evelyne Selberherr (E)
Angela Sessitsch (A)
Sigurlaug Skírnisdóttir (S)
Hauke Smidt (H)
Paul Smith (P)
Markus Sprenger-Haussels (M)
Ilma Tapio (I)
Julien Tap (J)
Vincenzo Valentino (V)
Martin Wagner (M)
Aaron Walsh (A)
Liam Walsh (L)
Sinead M Waters (SM)
Spike Willcocks (S)
David R Yáñez-Ruiz (DR)
Tianhai Yan (T)
Min Yap (M)
Emanuele Zannini (E)
Véronique Zuliani (V)

Informations de copyright

Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests D.O. is an employee of QIAGEN GmbH. E.S.K. is an employee of BaseClear B.V.

Auteurs

Niccolò Carlino (N)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.

Aitor Blanco-Míguez (A)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.

Michal Punčochář (M)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.

Claudia Mengoni (C)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.

Federica Pinto (F)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.

Alessia Tatti (A)

Scuola Universitaria Superiore IUSS Pavia, Pavia, Italy; Centre for Agriculture Food Environment, University of Trento, Trento, Italy; Research and Innovation Centre, Fondazione Edmund Mach, San Michele All'Adige, Italy.

Paolo Manghi (P)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.

Federica Armanini (F)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.

Michele Avagliano (M)

Department of Agricultural Sciences, Division of Microbiology, University of Naples Federico II, Portici, Italy.

Coral Barcenilla (C)

Department of Food Hygiene and Technology, Universidad de León, León, Spain.

Samuel Breselge (S)

Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland; APC Microbiome Ireland, University College Cork, Cork, Ireland.

Raul Cabrera-Rubio (R)

Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland; Department of Biotechnology, Institute of Agrochemistry and Food Technology - National Research Council (IATA-CSIC), Paterna, Valencia, Spain.

Inés Calvete-Torre (I)

Department of Microbiology and Biochemistry of Dairy Products, Instituto de Productos Lácteos de Asturias - Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Villaviciosa, Spain; Microhealth Group, Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Oviedo, Spain.

Mairéad Coakley (M)

Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland.

José F Cobo-Díaz (JF)

Department of Food Hygiene and Technology, Universidad de León, León, Spain.

Francesca De Filippis (F)

Department of Agricultural Sciences, Division of Microbiology, University of Naples Federico II, Portici, Italy; Task Force on Microbiome Studies, University of Naples Federico II, Portici, Italy.

Hrituraj Dey (H)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.

John Leech (J)

Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland.

Eline S Klaassens (ES)

BaseClear B.V., Leiden, the Netherlands.

Stephen Knobloch (S)

Microbiology Research Group, Matís, Reykjavík, Iceland.

Dominic O'Neil (D)

QIAGEN GmbH, Hilden, Germany.

Narciso M Quijada (NM)

Austrian Competence Centre for Feed and Food Quality, Safety, and Innovation, FFoQSI GmbH, Tulln an der Donau, Austria; Unit of Food Microbiology, Institute of Food Safety, Food Technology and Veterinary Public Health, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Vienna, Austria; Institute for Agribiotechnology Research (CIALE), Department of Microbiology and Genetics, University of Salamanca, Salamanca, Spain.

Carlos Sabater (C)

Department of Microbiology and Biochemistry of Dairy Products, Instituto de Productos Lácteos de Asturias - Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Villaviciosa, Spain; Microhealth Group, Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Oviedo, Spain.

Sigurlaug Skírnisdóttir (S)

Microbiology Research Group, Matís, Reykjavík, Iceland.

Vincenzo Valentino (V)

Department of Agricultural Sciences, Division of Microbiology, University of Naples Federico II, Portici, Italy.

Liam Walsh (L)

Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland; APC Microbiome Ireland, University College Cork, Cork, Ireland; School of Microbiology, University College Cork, Cork, Ireland.

Avelino Alvarez-Ordóñez (A)

Department of Food Hygiene and Technology, Universidad de León, León, Spain.

Francesco Asnicar (F)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.

Gloria Fackelmann (G)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.

Vitor Heidrich (V)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.

Abelardo Margolles (A)

Department of Microbiology and Biochemistry of Dairy Products, Instituto de Productos Lácteos de Asturias - Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Villaviciosa, Spain; Microhealth Group, Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Oviedo, Spain.

Viggó Thór Marteinsson (VT)

Microbiology Research Group, Matís, Reykjavík, Iceland; University of Iceland, Faculty of Food Science and Nutrition, Reykjavík, Iceland.

Omar Rota Stabelli (O)

Centre for Agriculture Food Environment, University of Trento, Trento, Italy; Research and Innovation Centre, Fondazione Edmund Mach, San Michele All'Adige, Italy.

Martin Wagner (M)

Austrian Competence Centre for Feed and Food Quality, Safety, and Innovation, FFoQSI GmbH, Tulln an der Donau, Austria; Unit of Food Microbiology, Institute of Food Safety, Food Technology and Veterinary Public Health, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Vienna, Austria.

Danilo Ercolini (D)

Department of Agricultural Sciences, Division of Microbiology, University of Naples Federico II, Portici, Italy; Task Force on Microbiome Studies, University of Naples Federico II, Portici, Italy.

Paul D Cotter (PD)

Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland; APC Microbiome Ireland, University College Cork, Cork, Ireland; VistaMilk SFI Research Centre, Teagasc, Moorepark, Fermoy, Co. Cork, Ireland.

Nicola Segata (N)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy; IEO, Istituto Europeo di Oncologia IRCSS, Milan, Italy; Department of Twins Research and Genetic Epidemiology, King's College London, London, UK. Electronic address: nicola.segata@unitn.it.

Edoardo Pasolli (E)

Department of Agricultural Sciences, Division of Microbiology, University of Naples Federico II, Portici, Italy; Task Force on Microbiome Studies, University of Naples Federico II, Portici, Italy.

Classifications MeSH