Finding functional differences between species in a microbial community: Case studies in wine fermentation and Kefir culture

Chrats Melkonian, Willi Gottstein, Sonja Blasche, Yongkyu Kim, Martin Abel-Kistrup, Hentie Swiegers, Sofie Saerens, Nathalia Edwards, Kiran R. Patil, Bas Teusink, Douwe Molenaar

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Microbial life usually takes place in a community where individuals interact, by competition for nutrients, cross-feeding, inhibition by end-products, but also by their spatial distribution. Lactic acid bacteria are prominent members of microbial communities responsible for food fermentations. Their niche in a community depends on their own properties as well as those of the other species. Here, we apply a computational approach, which uses only genomic and metagenomic information and functional annotation of genes, to find properties that distinguish a species from others in the community, as well as to follow individual species in a community. We analyzed isolated and sequenced strains from a kefir community, and metagenomes from wine fermentations. We demonstrate how the distinguishing properties of an organism lead to experimentally testable hypotheses concerning the niche and the interactions with other species. We observe, for example, that L. kefiranofaciens, a dominant organism in kefir, stands out among the Lactobacilli because it potentially has more amino acid auxotrophies. Using metagenomic analysis of industrial wine fermentations we investigate the role of an inoculated L. plantarum in malolactic fermentation. We observed that L. plantarum thrives better on white than on red wine fermentations and has the largest number of phosphotransferase system among the bacteria observed in the wine communities. Also, L. plantarum together with Pantoea, Erwinia, Asaia, Gluconobacter, and Komagataeibacter genera had the highest number of genes involved in biosynthesis of amino acids.

Original languageEnglish
Article number01347
Pages (from-to)1-14
Number of pages14
JournalFrontiers in Microbiology
Volume10
Issue numberJUNE
DOIs
Publication statusPublished - 25 Jun 2019

Fingerprint

Wine
Fermentation
Metagenomics
Gluconobacter
Pantoea
Metagenome
Erwinia
Bacteria
Molecular Sequence Annotation
Amino Acids
Food
Lactobacillus
Lactic Acid
Phosphotransferases
Kefir
Genes

Keywords

  • Computational biology
  • Genomes
  • Kefir
  • Lactic acid bacteria
  • Metagenomics
  • Microbial communities
  • Wine

Cite this

Melkonian, Chrats ; Gottstein, Willi ; Blasche, Sonja ; Kim, Yongkyu ; Abel-Kistrup, Martin ; Swiegers, Hentie ; Saerens, Sofie ; Edwards, Nathalia ; Patil, Kiran R. ; Teusink, Bas ; Molenaar, Douwe. / Finding functional differences between species in a microbial community : Case studies in wine fermentation and Kefir culture. In: Frontiers in Microbiology. 2019 ; Vol. 10, No. JUNE. pp. 1-14.
@article{a99766ff180846fe81f2e631505c7f06,
title = "Finding functional differences between species in a microbial community: Case studies in wine fermentation and Kefir culture",
abstract = "Microbial life usually takes place in a community where individuals interact, by competition for nutrients, cross-feeding, inhibition by end-products, but also by their spatial distribution. Lactic acid bacteria are prominent members of microbial communities responsible for food fermentations. Their niche in a community depends on their own properties as well as those of the other species. Here, we apply a computational approach, which uses only genomic and metagenomic information and functional annotation of genes, to find properties that distinguish a species from others in the community, as well as to follow individual species in a community. We analyzed isolated and sequenced strains from a kefir community, and metagenomes from wine fermentations. We demonstrate how the distinguishing properties of an organism lead to experimentally testable hypotheses concerning the niche and the interactions with other species. We observe, for example, that L. kefiranofaciens, a dominant organism in kefir, stands out among the Lactobacilli because it potentially has more amino acid auxotrophies. Using metagenomic analysis of industrial wine fermentations we investigate the role of an inoculated L. plantarum in malolactic fermentation. We observed that L. plantarum thrives better on white than on red wine fermentations and has the largest number of phosphotransferase system among the bacteria observed in the wine communities. Also, L. plantarum together with Pantoea, Erwinia, Asaia, Gluconobacter, and Komagataeibacter genera had the highest number of genes involved in biosynthesis of amino acids.",
keywords = "Computational biology, Genomes, Kefir, Lactic acid bacteria, Metagenomics, Microbial communities, Wine",
author = "Chrats Melkonian and Willi Gottstein and Sonja Blasche and Yongkyu Kim and Martin Abel-Kistrup and Hentie Swiegers and Sofie Saerens and Nathalia Edwards and Patil, {Kiran R.} and Bas Teusink and Douwe Molenaar",
year = "2019",
month = "6",
day = "25",
doi = "10.3389/fmicb.2019.01347",
language = "English",
volume = "10",
pages = "1--14",
journal = "Frontiers in Microbiology",
issn = "1664-302X",
publisher = "Frontiers Media S.A.",
number = "JUNE",

}

Finding functional differences between species in a microbial community : Case studies in wine fermentation and Kefir culture. / Melkonian, Chrats; Gottstein, Willi; Blasche, Sonja; Kim, Yongkyu; Abel-Kistrup, Martin; Swiegers, Hentie; Saerens, Sofie; Edwards, Nathalia; Patil, Kiran R.; Teusink, Bas; Molenaar, Douwe.

In: Frontiers in Microbiology, Vol. 10, No. JUNE, 01347, 25.06.2019, p. 1-14.

Research output: Contribution to JournalArticleAcademicpeer-review

TY - JOUR

T1 - Finding functional differences between species in a microbial community

T2 - Case studies in wine fermentation and Kefir culture

AU - Melkonian, Chrats

AU - Gottstein, Willi

AU - Blasche, Sonja

AU - Kim, Yongkyu

AU - Abel-Kistrup, Martin

AU - Swiegers, Hentie

AU - Saerens, Sofie

AU - Edwards, Nathalia

AU - Patil, Kiran R.

AU - Teusink, Bas

AU - Molenaar, Douwe

PY - 2019/6/25

Y1 - 2019/6/25

N2 - Microbial life usually takes place in a community where individuals interact, by competition for nutrients, cross-feeding, inhibition by end-products, but also by their spatial distribution. Lactic acid bacteria are prominent members of microbial communities responsible for food fermentations. Their niche in a community depends on their own properties as well as those of the other species. Here, we apply a computational approach, which uses only genomic and metagenomic information and functional annotation of genes, to find properties that distinguish a species from others in the community, as well as to follow individual species in a community. We analyzed isolated and sequenced strains from a kefir community, and metagenomes from wine fermentations. We demonstrate how the distinguishing properties of an organism lead to experimentally testable hypotheses concerning the niche and the interactions with other species. We observe, for example, that L. kefiranofaciens, a dominant organism in kefir, stands out among the Lactobacilli because it potentially has more amino acid auxotrophies. Using metagenomic analysis of industrial wine fermentations we investigate the role of an inoculated L. plantarum in malolactic fermentation. We observed that L. plantarum thrives better on white than on red wine fermentations and has the largest number of phosphotransferase system among the bacteria observed in the wine communities. Also, L. plantarum together with Pantoea, Erwinia, Asaia, Gluconobacter, and Komagataeibacter genera had the highest number of genes involved in biosynthesis of amino acids.

AB - Microbial life usually takes place in a community where individuals interact, by competition for nutrients, cross-feeding, inhibition by end-products, but also by their spatial distribution. Lactic acid bacteria are prominent members of microbial communities responsible for food fermentations. Their niche in a community depends on their own properties as well as those of the other species. Here, we apply a computational approach, which uses only genomic and metagenomic information and functional annotation of genes, to find properties that distinguish a species from others in the community, as well as to follow individual species in a community. We analyzed isolated and sequenced strains from a kefir community, and metagenomes from wine fermentations. We demonstrate how the distinguishing properties of an organism lead to experimentally testable hypotheses concerning the niche and the interactions with other species. We observe, for example, that L. kefiranofaciens, a dominant organism in kefir, stands out among the Lactobacilli because it potentially has more amino acid auxotrophies. Using metagenomic analysis of industrial wine fermentations we investigate the role of an inoculated L. plantarum in malolactic fermentation. We observed that L. plantarum thrives better on white than on red wine fermentations and has the largest number of phosphotransferase system among the bacteria observed in the wine communities. Also, L. plantarum together with Pantoea, Erwinia, Asaia, Gluconobacter, and Komagataeibacter genera had the highest number of genes involved in biosynthesis of amino acids.

KW - Computational biology

KW - Genomes

KW - Kefir

KW - Lactic acid bacteria

KW - Metagenomics

KW - Microbial communities

KW - Wine

UR - http://www.scopus.com/inward/record.url?scp=85069037071&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85069037071&partnerID=8YFLogxK

U2 - 10.3389/fmicb.2019.01347

DO - 10.3389/fmicb.2019.01347

M3 - Article

VL - 10

SP - 1

EP - 14

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

IS - JUNE

M1 - 01347

ER -