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

Niccolò Carlino; Aitor Blanco-Míguez; Michal Punčochář; Claudia Mengoni; Federica Pinto; Alessia Tatti; Paolo Manghi; Federica Armanini; Michele Avagliano; Coral Barcenilla; Samuel Breselge; Raul Cabrera-Rubio; Inés Calvete-Torre; Mairéad Coakley; José F. Cobo-Díaz; Francesca De Filippis; Hrituraj Dey; John Leech; Eline S. Klaassens; Stephen Knobloch; Dominic O'Neil; Narciso M. Quijada; Carlos Sabater; Sigurlaug Skírnisdóttir; Vincenzo Valentino; Liam Walsh; Avelino Alvarez-Ordóñez; Pablo Alvarez; Livio Antonielli; Elke Arendt; Aurelie Aubry; Jacob Baelum; Alejandro Belanche; Yaiza Benavent-Gil; Tony Blake; Radhika Bongoni; Mickael Boyer; Fiona Brennan; Helgi Briem; Derek Butler; Omar Cristobal Carballo; Mireille Cardinal; Chris Creevey; Rongcai Huang; Sharon Huws; Steven McLoughlin; Steven Morrison; Francesco Rubino; Fernanda Godoy Santos; Tianhai Yan; MASTER EU Consortium

doi:10.1016/j.cell.2024.07.039

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

Niccolò Carlino, Aitor Blanco-Míguez, Michal Punčochář, Claudia Mengoni, Federica Pinto, Alessia Tatti, Paolo Manghi, Federica Armanini, Michele Avagliano, Coral Barcenilla, Samuel Breselge, Raul Cabrera-Rubio, Inés Calvete-Torre, Mairéad Coakley, José F. Cobo-Díaz, Francesca De Filippis, Hrituraj Dey, John Leech, Eline S. Klaassens, Stephen KnoblochDominic O'Neil, Narciso M. Quijada, Carlos Sabater, Sigurlaug Skírnisdóttir, Vincenzo Valentino, Liam Walsh, Avelino Alvarez-Ordóñez, Pablo Alvarez, Livio Antonielli, Elke Arendt, Aurelie Aubry, Jacob Baelum, Alejandro Belanche, Yaiza Benavent-Gil, Tony Blake, Radhika Bongoni, Mickael Boyer, Fiona Brennan, Helgi Briem, Derek Butler, Omar Cristobal Carballo, Mireille Cardinal, Chris Creevey, Rongcai Huang, Sharon Huws, Steven McLoughlin, Steven Morrison, Francesco Rubino, Fernanda Godoy Santos, Tianhai Yan, MASTER EU Consortium

School of Biological Sciences

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Abstract

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.

Original language	English
Pages (from-to)	5775-5795.e15
Journal	Cell
Volume	187
Issue number	20
DOIs	https://doi.org/10.1016/j.cell.2024.07.039
Publication status	Published - 03 Oct 2024

Bibliographical note

Publisher Copyright:
© 2024 The Author(s)

Keywords

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

ASJC Scopus subject areas

General Biochemistry,Genetics and Molecular Biology

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10.1016/j.cell.2024.07.039Licence: CC BY-NC-ND

Unexplored microbial diversity from 2,500 food metagenomes and links with the human microbiome
Copyright 2024 the authors. This is an open access article published under a Creative Commons Attribution-NonCommercial-NoDerivs License (https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits distribution and reproduction for non-commercial purposes, provided the author and source are cited.
Final published version, 16.6 MBLicence: CC BY-NC-ND

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Carlino, N., Blanco-Míguez, A., Punčochář, M., Mengoni, C., Pinto, F., Tatti, A., Manghi, P., Armanini, F., Avagliano, M., Barcenilla, C., Breselge, S., Cabrera-Rubio, R., Calvete-Torre, I., Coakley, M., Cobo-Díaz, J. F., De Filippis, F., Dey, H., Leech, J., Klaassens, E. S., ... MASTER EU Consortium (2024). Unexplored microbial diversity from 2,500 food metagenomes and links with the human microbiome. Cell, 187(20), 5775-5795.e15. https://doi.org/10.1016/j.cell.2024.07.039

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abstract = "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.",

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Carlino, N, Blanco-Míguez, A, Punčochář, M, Mengoni, C, Pinto, F, Tatti, A, Manghi, P, Armanini, F, Avagliano, M, Barcenilla, C, Breselge, S, Cabrera-Rubio, R, Calvete-Torre, I, Coakley, M, Cobo-Díaz, JF, De Filippis, F, Dey, H, Leech, J, Klaassens, ES, Knobloch, S, O'Neil, D, Quijada, NM, Sabater, C, Skírnisdóttir, S, Valentino, V, Walsh, L, Alvarez-Ordóñez, A, Alvarez, P, Antonielli, L, Arendt, E, Aubry, A, Baelum, J, Belanche, A, Benavent-Gil, Y, Blake, T, Bongoni, R, Boyer, M, Brennan, F, Briem, H, Butler, D, Carballo, OC, Cardinal, M, Creevey, C, Huang, R, Huws, S, McLoughlin, S, Morrison, S, Rubino, F, Santos, FG, Yan, T & MASTER EU Consortium 2024, 'Unexplored microbial diversity from 2,500 food metagenomes and links with the human microbiome', Cell, vol. 187, no. 20, pp. 5775-5795.e15. https://doi.org/10.1016/j.cell.2024.07.039

TY - JOUR

T1 - Unexplored microbial diversity from 2,500 food metagenomes and links with the human microbiome

AU - Carlino, Niccolò

AU - Blanco-Míguez, Aitor

AU - Punčochář, Michal

AU - Mengoni, Claudia

AU - Pinto, Federica

AU - Tatti, Alessia

AU - Manghi, Paolo

AU - Armanini, Federica

AU - Avagliano, Michele

AU - Barcenilla, Coral

AU - Breselge, Samuel

AU - Cabrera-Rubio, Raul

AU - Calvete-Torre, Inés

AU - Coakley, Mairéad

AU - Cobo-Díaz, José F.

AU - De Filippis, Francesca

AU - Dey, Hrituraj

AU - Leech, John

AU - Klaassens, Eline S.

AU - Knobloch, Stephen

AU - O'Neil, Dominic

AU - Quijada, Narciso M.

AU - Sabater, Carlos

AU - Skírnisdóttir, Sigurlaug

AU - Valentino, Vincenzo

AU - Walsh, Liam

AU - Alvarez-Ordóñez, Avelino

AU - Alvarez, Pablo

AU - Antonielli, Livio

AU - Arendt, Elke

AU - Aubry, Aurelie

AU - Baelum, Jacob

AU - Belanche, Alejandro

AU - Benavent-Gil, Yaiza

AU - Blake, Tony

AU - Bongoni, Radhika

AU - Boyer, Mickael

AU - Brennan, Fiona

AU - Briem, Helgi

AU - Butler, Derek

AU - Carballo, Omar Cristobal

AU - Cardinal, Mireille

AU - Creevey, Chris

AU - Huang, Rongcai

AU - Huws, Sharon

AU - McLoughlin, Steven

AU - Morrison, Steven

AU - Rubino, Francesco

AU - Santos, Fernanda Godoy

AU - Yan, Tianhai

AU - MASTER EU Consortium

PY - 2024/10/3

Y1 - 2024/10/3

N2 - 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.

AB - 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.

KW - food

KW - food microbiome

KW - human microbiome

KW - large-scale microbiome analysis

KW - metagenomic assembly

KW - metagenomics

KW - strain-level genomics

KW - unexplored microbial diversity

U2 - 10.1016/j.cell.2024.07.039

DO - 10.1016/j.cell.2024.07.039

M3 - Article

C2 - 39214080

AN - SCOPUS:85204442573

SN - 0092-8674

VL - 187

SP - 5775-5795.e15

JO - Cell

JF - Cell

IS - 20

ER -

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

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

Access to Document

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