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Cited by 375Probiotics and Fermented FoodsGut microbiota and healthGenomics and Phylogenetic Studies

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Large-scale genome-wide analysis links lactic acid bacteria from food with the gut microbiome

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Pasolli, Edoardo, De Filippis, Francesca, Mauriello, Italia E., Cumbo, Fabio, Walsh, Aaron M., Leech, John, Cotter, Paul D., Segata, Nicola, Ercolini, Danilo·2020·Nature Communications
DOI 10.1038/s41467-020-16438-8PMC PMC7248083
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Abstract

Lactic acid bacteria (LAB) are fundamental in the production of fermented foods and several strains are regarded as probiotics. Large quantities of live LAB are consumed within fermented foods, but it is not yet known to what extent the LAB we ingest become members of the gut microbiome. By analysis of 9445 metagenomes from human samples, we demonstrate that the prevalence and abundance of LAB species in stool samples is generally low and linked to age, lifestyle, and geography, with Streptococcus thermophilus and Lactococcus lactis being most prevalent. Moreover, we identify genome-based differences between food and gut microbes by considering 666 metagenome-assembled genomes (MAGs) newly reconstructed from fermented food microbiomes along with 154,723 human MAGs and 193,078 reference genomes. Our large-scale genome-wide analysis demonstrates that closely related LAB strains occur in both food and gut environments and provides unprecedented evidence that fermented foods can be indeed regarded as a possible source of LAB for the gut microbiome.

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Fig. 1 Average prevalence of LAB species from human and food microbiomes. We report the 30 LAB species having a prevalence >0.1% in the human gut. Values are obtained from 9445 publicly available human metagenomes and stratified by multiple host conditions (i.e., body site, age category, westernized lifestyle, and continent). Age category, westernized lifestyle, and continent statistics refer to stool samples only. Food results are obtained from 303 food metagenomes. Numbers and p-values (Fisher’s test, false discovery rate correction) in Supplementary Figs. 1–4 and Supplementary Data 4. Relative abundances in Supplementary Data 2 and 3.
Fig. 1 Average prevalence of LAB species from human and food microbiomes. We report the 30 LAB species having a prevalence >0.1% in the human gut. Values are obtained from 9445 publicly available human metagenomes and stratified by multiple host conditions (i.e., body site, age category, westernized lifestyle, and continent). Age category, westernized lifestyle, and continent statistics refer to stool samples only. Food results are obtained from 303 food metagenomes. Numbers and p-values (Fisher’s test, false discovery rate correction) in Supplementary Figs. 1–4 and Supplementary Data 4. Relative abundances in Supplementary Data 2 and 3.CC BY · PubMed Central
Fig. 2 Microbial genomes reconstructed from food metagenomes. a Most prevalent species-level genome bins (SGBs) in 666 MAGs reconstructed from 303 food metagenomes and overlapping with human MAGs (i.e., found in at least one of the 154,723 human MAGs). Numbers in parenthesis represent the SGB IDs. b Most prevalent food SGBs not overlapping with human MAGs. kSGBs denote SGBs with at least one reference microbial genome, whereas fSGBs identify newly assembled SGBs from food metagenomes only. X-axes for a and b are in logarithmic scale. c Fraction of reference genomes per source type for the 30 selected LAB species and grouped by genera (the same plot at species-level is reported in Supplementary Fig. 6). Raw data in Supplementary Data 6 and 7.
Fig. 2 Microbial genomes reconstructed from food metagenomes. a Most prevalent species-level genome bins (SGBs) in 666 MAGs reconstructed from 303 food metagenomes and overlapping with human MAGs (i.e., found in at least one of the 154,723 human MAGs). Numbers in parenthesis represent the SGB IDs. b Most prevalent food SGBs not overlapping with human MAGs. kSGBs denote SGBs with at least one reference microbial genome, whereas fSGBs identify newly assembled SGBs from food metagenomes only. X-axes for a and b are in logarithmic scale. c Fraction of reference genomes per source type for the 30 selected LAB species and grouped by genera (the same plot at species-level is reported in Supplementary Fig. 6). Raw data in Supplementary Data 6 and 7.CC BY · PubMed Central
Fig. 3 Comparative genomic analysis of the two most prevalent LAB identified in the human gut microbiome. a S. thermophilus is a genetically diverse species both in food and human sources with MAGs reconstructed from Asian gut metagenomes enriched in Clade A (p < 1e − 10). b Lc. lactis subsp. lactis is formed by three main clusters: Cluster 1 exhibits an overall low diversity and includes mostly food genomes related to cheese and dairy fermentation; Cluster 2 is dominated by environmental and raw vegetable products and more diverse human MAGs; Cluster 3 includes only two MAGs from nunu. Phylogenetic trees were built on species-specific marker genes and report five different metadata. Multidimensional scaling (MDS) on average nucleotide identity (ANI) distance is coloured with source information.
Fig. 3 Comparative genomic analysis of the two most prevalent LAB identified in the human gut microbiome. a S. thermophilus is a genetically diverse species both in food and human sources with MAGs reconstructed from Asian gut metagenomes enriched in Clade A (p < 1e − 10). b Lc. lactis subsp. lactis is formed by three main clusters: Cluster 1 exhibits an overall low diversity and includes mostly food genomes related to cheese and dairy fermentation; Cluster 2 is dominated by environmental and raw vegetable products and more diverse human MAGs; Cluster 3 includes only two MAGs from nunu. Phylogenetic trees were built on species-specific marker genes and report five different metadata. Multidimensional scaling (MDS) on average nucleotide identity (ANI) distance is coloured with source information.CC BY · PubMed Central
Fig. 4 Comparative genomic analysis of relevant lactobacilli found in both food and human microbiomes. a Lb. delbrueckii is not prevalent in the gut, and the only two subspecies found in both food and human samples are subsps. lactis and. bulgaricus. Subsps. delbrueckii, sunkii, and jakobsenii are found in food, but never reconstructed from the gut. b Lb. rhamnosus exhibits the greatest number of genomes from human isolates but is scarcely reconstructed from metagenomes. A specific cluster identifies the LGG strain. c Lb. casei/paracasei includes reference genomes identified as both Lb. casei and Lb. paracasei. We detect two main clusters both occurring in food and human samples. d Lb. helveticus exhibits three main clusters, with Cluster 1 including all the dietary supplement strains (source in green), while food genomes are predominantly spread across the other two groups. Phylogenetic trees were built on species-specific marker genes and report five different metadata. Multidimensional scaling (MDS) on average nucleotide identity (ANI) distance is coloured with source information.
Fig. 4 Comparative genomic analysis of relevant lactobacilli found in both food and human microbiomes. a Lb. delbrueckii is not prevalent in the gut, and the only two subspecies found in both food and human samples are subsps. lactis and. bulgaricus. Subsps. delbrueckii, sunkii, and jakobsenii are found in food, but never reconstructed from the gut. b Lb. rhamnosus exhibits the greatest number of genomes from human isolates but is scarcely reconstructed from metagenomes. A specific cluster identifies the LGG strain. c Lb. casei/paracasei includes reference genomes identified as both Lb. casei and Lb. paracasei. We detect two main clusters both occurring in food and human samples. d Lb. helveticus exhibits three main clusters, with Cluster 1 including all the dietary supplement strains (source in green), while food genomes are predominantly spread across the other two groups. Phylogenetic trees were built on species-specific marker genes and report five different metadata. Multidimensional scaling (MDS) on average nucleotide identity (ANI) distance is coloured with source information.CC BY · PubMed Central

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Metadata

Authors
Pasolli, E., De Filippis, F., Mauriello, I. E., Cumbo, F., Walsh, A. M., Leech, J., Cotter, P. D., Segata, N., & Ercolini, D.
Affiliations
  • University of Naples Federico II (IT)
  • University of Trento (IT)
  • Teagasc - The Irish Agriculture and Food Development Authority (IE)
Corresponding author
Ercolini, Danilo
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2020-05-25
Volume
11
Issue
1
Pages
2610-2610
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-020-16438-8
PMC
PMC7248083
OpenAlex
W3027854790
Cited by
367
References
67
Citations by year
2026: 41 · 2025: 59 · 2024: 49 · 2023: 78 · 2022: 74 · 2021: 51 · 2020: 14
FWCI
4.75
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Arrow@dit (Dublin Institute of Technology) (acceptedVersion)
  • HAL (submittedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Institutional Research Information System (Università degli Studi di Trento) (submittedVersion, cc-by)
  • T-Stór (Teagasc) (submittedVersion, cc-by-nc-sa)
  • Lenus, The Irish Health Repository (Dr Steevens Hospital Library) (submittedVersion)
Funders
  • Joint Programming Initiative A healthy diet for a healthy life
  • European Commission (HORIZON2020, 818368)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
lactic acid bacteria, gut microbiota, fermented foods, probiotics, metagenome-assembled genomes, Streptococcus thermophilus, Lactococcus lactis, human gut metagenome
MeSH terms
Gastrointestinal Microbiome, Fermented Foods, Animals, Food Microbiology, Humans, Life Style, Primates, Lactococcus lactis, Probiotics, Databases, Genetic, Streptococcus thermophilus, Metagenome, Lactobacillales

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