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; Francesco Asnicar; Gloria Fackelmann; Vitor Heidrich; Abelardo Margolles; Viggó Thór Marteinsson; Omar Rota Stabelli; Martin Wagner; Danilo Ercolini; Paul D Cotter; Nicola Segata; Edoardo Pasolli; Angela Sessitsch; Tanja Kostic; Johanna Maria Ley; Milica Pastar; Livio Antonielli

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 Knobloch, Dominic O'Neil, Narciso M Quijada, Carlos Sabater, Sigurlaug Skírnisdóttir, Vincenzo Valentino, Liam Walsh, Avelino Alvarez-Ordóñez, Francesco Asnicar, Gloria Fackelmann, Vitor Heidrich, Abelardo Margolles, Viggó Thór Marteinsson, Omar Rota Stabelli, Martin Wagner, Danilo Ercolini, Paul D Cotter, Nicola Segata, Edoardo Pasolli, Angela Sessitsch, Tanja Kostic, Johanna Maria Ley, Milica Pastar, Livio Antonielli

Bioresources

University of Trento
University of Natural Resources and Life Sciences Vienna (BOKU)
University of Naples Federico II
University of León
University College Cork
Teagasc Food Research Centre
Institute of Agrochemistry and Food Technology (IATA)
University of Oviedo
Netherlands Organisation for Applied Scientific Research (TNO)
Reykjavík University
Pontifical University of Salamanca
Instituto de Productos Lácteos de Asturias, Consejo Superior de Investigaciones Científicas (IPLA-CSIC)
University of Iceland
FFoQSI GmbH - Austrian Competence Centre for Feed and Food Quality, Safety and Innovation
University of Veterinary Medicine Vienna

Research output: Contribution to journal › Article › peer-review

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
Number of pages	37
Journal	Cell
Volume	187
Issue number	20
Early online date	16 Aug 2024
DOIs	https://doi.org/10.1016/j.cell.2024.07.039
Publication status	Published - Oct 2024

Research Field

Exploration of Biological Resources

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10.1016/j.cell.2024.07.039Licence: 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., ... Antonielli, L. (2024). Unexplored microbial diversity from 2,500 food metagenomes and links with the human microbiome. Cell, 187(20). https://doi.org/10.1016/j.cell.2024.07.039

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

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.",

author = "Niccol{\`o} Carlino and Aitor Blanco-M{\'i}guez and Michal Pun{\v c}och{\'a}{\v r} and Claudia Mengoni and Federica Pinto and Alessia Tatti and Paolo Manghi and Federica Armanini and Michele Avagliano and Coral Barcenilla and Samuel Breselge and Raul Cabrera-Rubio and In{\'e}s Calvete-Torre and Mair{\'e}ad Coakley and Cobo-D{\'i}az, \{Jos{\'e} F\} and \{De Filippis\}, Francesca and Hrituraj Dey and John Leech and Klaassens, \{Eline S\} and Stephen Knobloch and Dominic O'Neil and Quijada, \{Narciso M\} and Carlos Sabater and Sigurlaug Sk{\'i}rnisd{\'o}ttir and Vincenzo Valentino and Liam Walsh and Avelino Alvarez-Ord{\'o}{\~n}ez and Francesco Asnicar and Gloria Fackelmann and Vitor Heidrich and Abelardo Margolles and Marteinsson, \{Vigg{\'o} Th{\'o}r\} and \{Rota Stabelli\}, Omar and Martin Wagner and Danilo Ercolini and Cotter, \{Paul D\} and Nicola Segata and Edoardo Pasolli and Angela Sessitsch and Tanja Kostic and Ley, \{Johanna Maria\} and Milica Pastar and Livio Antonielli",

year = "2024",

month = oct,

doi = "10.1016/j.cell.2024.07.039",

language = "English",

volume = "187",

journal = "Cell",

issn = "0092-8674",

publisher = "Elsevier BV",

number = "20",

}

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, Asnicar, F, Fackelmann, G, Heidrich, V, Margolles, A, Marteinsson, VT, Rota Stabelli, O, Wagner, M, Ercolini, D, Cotter, PD, Segata, N, Pasolli, E, Sessitsch, A , Kostic, T , Ley, JM & Pastar, M & Antonielli, L 2024, 'Unexplored microbial diversity from 2,500 food metagenomes and links with the human microbiome', Cell, vol. 187, no. 20. 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 - Asnicar, Francesco

AU - Fackelmann, Gloria

AU - Heidrich, Vitor

AU - Margolles, Abelardo

AU - Marteinsson, Viggó Thór

AU - Rota Stabelli, Omar

AU - Wagner, Martin

AU - Ercolini, Danilo

AU - Cotter, Paul D

AU - Segata, Nicola

AU - Pasolli, Edoardo

AU - Sessitsch, Angela

AU - Kostic, Tanja

AU - Ley, Johanna Maria

AU - Pastar, Milica

AU - Antonielli, Livio

PY - 2024/10

Y1 - 2024/10

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.

UR - https://www.mendeley.com/catalogue/20de5dbc-fcfc-3ddb-b2dc-af0e1ff8f6d8/

U2 - 10.1016/j.cell.2024.07.039

DO - 10.1016/j.cell.2024.07.039

M3 - Article

C2 - 39214080

SN - 0092-8674

VL - 187

JO - Cell

JF - Cell

IS - 20

ER -

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

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