A genome-scale metabolic network of the aroma bacterium Leuconostoc mesenteroides subsp. cremoris

Emrah Özcan, S. Selvin Selvi, Emrah Nikerel, Bas Teusink, Ebru Toksoy Öner, Tunahan Çakır

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Leuconostoc mesenteroides subsp. cremoris is an obligate heterolactic fermentative lactic acid bacterium that is mostly used in industrial dairy fermentations. The phosphoketolase pathway (PKP) is a unique feature of the obligate heterolactic fermentation, which leads to the production of lactate, ethanol, and/or acetate, and the final product profile of PKP highly depends on the energetics and redox state of the organism. Another characteristic of the L. mesenteroides subsp. cremoris is the production of aroma compounds in dairy fermentation, such as in cheese production, through the utilization of citrate. Considering its importance in dairy fermentation, a detailed metabolic characterization of the organism is necessary for its more efficient use in the industry. To this aim, a genome-scale metabolic model of dairy-origin L. mesenteroides subsp. cremoris ATCC 19254 (iLM.c559) was reconstructed to explain the energetics and redox state mechanisms of the organism in full detail. The model includes 559 genes governing 1088 reactions between 1129 metabolites, and the reactions cover citrate utilization and citrate-related flavor metabolism. The model was validated by simulating co-metabolism of glucose and citrate and comparing the in silico results to our experimental results. Model simulations further showed that, in co-metabolism of citrate and glucose, no flavor compounds were produced when citrate could stimulate the formation of biomass. Significant amounts of flavor metabolites (e.g., diacetyl and acetoin) were only produced when citrate could not enhance growth, which suggests that flavor formation only occurs under carbon and ATP excess. The effects of aerobic conditions and different carbon sources on product profiles and growth were also investigated using the reconstructed model. The analyses provided further insights for the growth stimulation and flavor formation mechanisms of the organism.

Original languageEnglish
JournalApplied Microbiology and Biotechnology
DOIs
Publication statusPublished - 1 Jan 2019

Fingerprint

Metabolic Networks and Pathways
Citric Acid
Genome
Bacteria
phosphoketolase
Fermentation
Oxidation-Reduction
Lactic Acid
Carbon
Growth
Acetoin
Diacetyl
Glucose
Cheese
Leuconostoc mesenteroides
Computer Simulation
Biomass
Industry
Acetates
Ethanol

Keywords

  • Flavor metabolism
  • Flux balance analysis
  • Genome-scale metabolic model
  • Heterolactic fermentation
  • Lactic acid bacteria
  • Leuconostoc mesenteroides subsp. cremoris

Cite this

@article{7a12c8044c104aef99efb72df2c365f4,
title = "A genome-scale metabolic network of the aroma bacterium Leuconostoc mesenteroides subsp. cremoris",
abstract = "Leuconostoc mesenteroides subsp. cremoris is an obligate heterolactic fermentative lactic acid bacterium that is mostly used in industrial dairy fermentations. The phosphoketolase pathway (PKP) is a unique feature of the obligate heterolactic fermentation, which leads to the production of lactate, ethanol, and/or acetate, and the final product profile of PKP highly depends on the energetics and redox state of the organism. Another characteristic of the L. mesenteroides subsp. cremoris is the production of aroma compounds in dairy fermentation, such as in cheese production, through the utilization of citrate. Considering its importance in dairy fermentation, a detailed metabolic characterization of the organism is necessary for its more efficient use in the industry. To this aim, a genome-scale metabolic model of dairy-origin L. mesenteroides subsp. cremoris ATCC 19254 (iLM.c559) was reconstructed to explain the energetics and redox state mechanisms of the organism in full detail. The model includes 559 genes governing 1088 reactions between 1129 metabolites, and the reactions cover citrate utilization and citrate-related flavor metabolism. The model was validated by simulating co-metabolism of glucose and citrate and comparing the in silico results to our experimental results. Model simulations further showed that, in co-metabolism of citrate and glucose, no flavor compounds were produced when citrate could stimulate the formation of biomass. Significant amounts of flavor metabolites (e.g., diacetyl and acetoin) were only produced when citrate could not enhance growth, which suggests that flavor formation only occurs under carbon and ATP excess. The effects of aerobic conditions and different carbon sources on product profiles and growth were also investigated using the reconstructed model. The analyses provided further insights for the growth stimulation and flavor formation mechanisms of the organism.",
keywords = "Flavor metabolism, Flux balance analysis, Genome-scale metabolic model, Heterolactic fermentation, Lactic acid bacteria, Leuconostoc mesenteroides subsp. cremoris",
author = "Emrah {\"O}zcan and Selvi, {S. Selvin} and Emrah Nikerel and Bas Teusink and {Toksoy {\"O}ner}, Ebru and Tunahan {\cC}akır",
year = "2019",
month = "1",
day = "1",
doi = "10.1007/s00253-019-09630-4",
language = "English",
journal = "Applied Microbiology and Biotechnology",
issn = "0175-7598",
publisher = "Springer Verlag",

}

A genome-scale metabolic network of the aroma bacterium Leuconostoc mesenteroides subsp. cremoris. / Özcan, Emrah; Selvi, S. Selvin; Nikerel, Emrah; Teusink, Bas; Toksoy Öner, Ebru; Çakır, Tunahan.

In: Applied Microbiology and Biotechnology, 01.01.2019.

Research output: Contribution to JournalArticleAcademicpeer-review

TY - JOUR

T1 - A genome-scale metabolic network of the aroma bacterium Leuconostoc mesenteroides subsp. cremoris

AU - Özcan, Emrah

AU - Selvi, S. Selvin

AU - Nikerel, Emrah

AU - Teusink, Bas

AU - Toksoy Öner, Ebru

AU - Çakır, Tunahan

PY - 2019/1/1

Y1 - 2019/1/1

N2 - Leuconostoc mesenteroides subsp. cremoris is an obligate heterolactic fermentative lactic acid bacterium that is mostly used in industrial dairy fermentations. The phosphoketolase pathway (PKP) is a unique feature of the obligate heterolactic fermentation, which leads to the production of lactate, ethanol, and/or acetate, and the final product profile of PKP highly depends on the energetics and redox state of the organism. Another characteristic of the L. mesenteroides subsp. cremoris is the production of aroma compounds in dairy fermentation, such as in cheese production, through the utilization of citrate. Considering its importance in dairy fermentation, a detailed metabolic characterization of the organism is necessary for its more efficient use in the industry. To this aim, a genome-scale metabolic model of dairy-origin L. mesenteroides subsp. cremoris ATCC 19254 (iLM.c559) was reconstructed to explain the energetics and redox state mechanisms of the organism in full detail. The model includes 559 genes governing 1088 reactions between 1129 metabolites, and the reactions cover citrate utilization and citrate-related flavor metabolism. The model was validated by simulating co-metabolism of glucose and citrate and comparing the in silico results to our experimental results. Model simulations further showed that, in co-metabolism of citrate and glucose, no flavor compounds were produced when citrate could stimulate the formation of biomass. Significant amounts of flavor metabolites (e.g., diacetyl and acetoin) were only produced when citrate could not enhance growth, which suggests that flavor formation only occurs under carbon and ATP excess. The effects of aerobic conditions and different carbon sources on product profiles and growth were also investigated using the reconstructed model. The analyses provided further insights for the growth stimulation and flavor formation mechanisms of the organism.

AB - Leuconostoc mesenteroides subsp. cremoris is an obligate heterolactic fermentative lactic acid bacterium that is mostly used in industrial dairy fermentations. The phosphoketolase pathway (PKP) is a unique feature of the obligate heterolactic fermentation, which leads to the production of lactate, ethanol, and/or acetate, and the final product profile of PKP highly depends on the energetics and redox state of the organism. Another characteristic of the L. mesenteroides subsp. cremoris is the production of aroma compounds in dairy fermentation, such as in cheese production, through the utilization of citrate. Considering its importance in dairy fermentation, a detailed metabolic characterization of the organism is necessary for its more efficient use in the industry. To this aim, a genome-scale metabolic model of dairy-origin L. mesenteroides subsp. cremoris ATCC 19254 (iLM.c559) was reconstructed to explain the energetics and redox state mechanisms of the organism in full detail. The model includes 559 genes governing 1088 reactions between 1129 metabolites, and the reactions cover citrate utilization and citrate-related flavor metabolism. The model was validated by simulating co-metabolism of glucose and citrate and comparing the in silico results to our experimental results. Model simulations further showed that, in co-metabolism of citrate and glucose, no flavor compounds were produced when citrate could stimulate the formation of biomass. Significant amounts of flavor metabolites (e.g., diacetyl and acetoin) were only produced when citrate could not enhance growth, which suggests that flavor formation only occurs under carbon and ATP excess. The effects of aerobic conditions and different carbon sources on product profiles and growth were also investigated using the reconstructed model. The analyses provided further insights for the growth stimulation and flavor formation mechanisms of the organism.

KW - Flavor metabolism

KW - Flux balance analysis

KW - Genome-scale metabolic model

KW - Heterolactic fermentation

KW - Lactic acid bacteria

KW - Leuconostoc mesenteroides subsp. cremoris

UR - http://www.scopus.com/inward/record.url?scp=85061002578&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85061002578&partnerID=8YFLogxK

U2 - 10.1007/s00253-019-09630-4

DO - 10.1007/s00253-019-09630-4

M3 - Article

JO - Applied Microbiology and Biotechnology

JF - Applied Microbiology and Biotechnology

SN - 0175-7598

ER -