Proteomic and in silico analyses of dextran synthesis influence on Leuconostoc lactis AV1n adaptation to temperature change

Leuconostoc lactis is found in vegetables, fruits, and meat and is used by the food industry in the preparation of dairy products, wines, and sugars. We have previously demonstrated that the dextransucrase of Lc. lactis (DsrLL) AV1n produces a high-molecular-weight dextran from sucrose, indicating i...

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Main Authors: Norhane Besrour-Aouam, Vivian de Los Rios, Annel M. Hernández-Alcántara, Mᵃ Luz Mohedano, Afef Najjari, Paloma López, Hadda-Imene Ouzari
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-01-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.1077375/full
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author Norhane Besrour-Aouam
Norhane Besrour-Aouam
Vivian de Los Rios
Annel M. Hernández-Alcántara
Mᵃ Luz Mohedano
Afef Najjari
Paloma López
Hadda-Imene Ouzari
author_facet Norhane Besrour-Aouam
Norhane Besrour-Aouam
Vivian de Los Rios
Annel M. Hernández-Alcántara
Mᵃ Luz Mohedano
Afef Najjari
Paloma López
Hadda-Imene Ouzari
author_sort Norhane Besrour-Aouam
collection DOAJ
description Leuconostoc lactis is found in vegetables, fruits, and meat and is used by the food industry in the preparation of dairy products, wines, and sugars. We have previously demonstrated that the dextransucrase of Lc. lactis (DsrLL) AV1n produces a high-molecular-weight dextran from sucrose, indicating its potential use as a dextran-forming starter culture. We have also shown that this bacterium was able to produce 10-fold higher levels of dextran at 20°C than at 37°C, at the former temperature accompanied by an increase in dsrLL gene expression. However, the general physiological response of Lc. lactis AV1n to cold temperature in the presence of sucrose, leading to increased production of dextran, has not been yet investigated. Therefore, we have used a quantitative proteomics approach to investigate the cold temperature-induced changes in the proteomic profile of this strain in comparison to its proteomic response at 37°C. In total, 337 proteins were found to be differentially expressed at the applied significance criteria (adjusted p-value ≤ 0.05, FDR 5%, and with a fold-change ≥ 1.5 or ≤ 0.67) with 204 proteins overexpressed, among which 13% were involved in protein as well as cell wall, and envelope component biosynthesis including DsrLL. Proteins implicated in cold stress were expressed at a high level at 20°C and possibly play a role in the upregulation of DsrLL, allowing the efficient synthesis of the protein essential for its adaptation to cold. Post-transcriptional regulation of DsrLL expression also seems to take place through the interplay of exonucleases and endonucleases overexpressed at 20°C, which would influence the half-life of the dsrLL transcript. Furthermore, the mechanism of cold resistance of Lc. lactis AV1n seems to be also based on energy saving through a decrease in growth rate mediated by a decrease in carbohydrate metabolism and its orientation toward the production pathways for storage molecules. Thus, this better understanding of the responses to low temperature and mechanisms for environmental adaptation of Lc. lactis could be exploited for industrial use of strains belonging to this species.
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spelling doaj.art-779bfd92176a430991340b750bbbaba82023-01-11T05:49:39ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-01-011310.3389/fmicb.2022.10773751077375Proteomic and in silico analyses of dextran synthesis influence on Leuconostoc lactis AV1n adaptation to temperature changeNorhane Besrour-Aouam0Norhane Besrour-Aouam1Vivian de Los Rios2Annel M. Hernández-Alcántara3Mᵃ Luz Mohedano4Afef Najjari5Paloma López6Hadda-Imene Ouzari7Centro de Investigaciones Biológicas Margarita Salas, CIB-CSIC, Madrid, SpainLaboratoire Microorganismes et Biomolécules Actives (LR03ES03), Faculté des Sciences de Tunis, Université Tunis El Manar, Tunis, TunisiaCentro de Investigaciones Biológicas Margarita Salas, CIB-CSIC, Madrid, SpainCentro de Investigaciones Biológicas Margarita Salas, CIB-CSIC, Madrid, SpainCentro de Investigaciones Biológicas Margarita Salas, CIB-CSIC, Madrid, SpainLaboratoire Microorganismes et Biomolécules Actives (LR03ES03), Faculté des Sciences de Tunis, Université Tunis El Manar, Tunis, TunisiaCentro de Investigaciones Biológicas Margarita Salas, CIB-CSIC, Madrid, SpainLaboratoire Microorganismes et Biomolécules Actives (LR03ES03), Faculté des Sciences de Tunis, Université Tunis El Manar, Tunis, TunisiaLeuconostoc lactis is found in vegetables, fruits, and meat and is used by the food industry in the preparation of dairy products, wines, and sugars. We have previously demonstrated that the dextransucrase of Lc. lactis (DsrLL) AV1n produces a high-molecular-weight dextran from sucrose, indicating its potential use as a dextran-forming starter culture. We have also shown that this bacterium was able to produce 10-fold higher levels of dextran at 20°C than at 37°C, at the former temperature accompanied by an increase in dsrLL gene expression. However, the general physiological response of Lc. lactis AV1n to cold temperature in the presence of sucrose, leading to increased production of dextran, has not been yet investigated. Therefore, we have used a quantitative proteomics approach to investigate the cold temperature-induced changes in the proteomic profile of this strain in comparison to its proteomic response at 37°C. In total, 337 proteins were found to be differentially expressed at the applied significance criteria (adjusted p-value ≤ 0.05, FDR 5%, and with a fold-change ≥ 1.5 or ≤ 0.67) with 204 proteins overexpressed, among which 13% were involved in protein as well as cell wall, and envelope component biosynthesis including DsrLL. Proteins implicated in cold stress were expressed at a high level at 20°C and possibly play a role in the upregulation of DsrLL, allowing the efficient synthesis of the protein essential for its adaptation to cold. Post-transcriptional regulation of DsrLL expression also seems to take place through the interplay of exonucleases and endonucleases overexpressed at 20°C, which would influence the half-life of the dsrLL transcript. Furthermore, the mechanism of cold resistance of Lc. lactis AV1n seems to be also based on energy saving through a decrease in growth rate mediated by a decrease in carbohydrate metabolism and its orientation toward the production pathways for storage molecules. Thus, this better understanding of the responses to low temperature and mechanisms for environmental adaptation of Lc. lactis could be exploited for industrial use of strains belonging to this species.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1077375/fullLeuconostocdextranexopolysaccharideslactic acid bacteriaproteomic
spellingShingle Norhane Besrour-Aouam
Norhane Besrour-Aouam
Vivian de Los Rios
Annel M. Hernández-Alcántara
Mᵃ Luz Mohedano
Afef Najjari
Paloma López
Hadda-Imene Ouzari
Proteomic and in silico analyses of dextran synthesis influence on Leuconostoc lactis AV1n adaptation to temperature change
Frontiers in Microbiology
Leuconostoc
dextran
exopolysaccharides
lactic acid bacteria
proteomic
title Proteomic and in silico analyses of dextran synthesis influence on Leuconostoc lactis AV1n adaptation to temperature change
title_full Proteomic and in silico analyses of dextran synthesis influence on Leuconostoc lactis AV1n adaptation to temperature change
title_fullStr Proteomic and in silico analyses of dextran synthesis influence on Leuconostoc lactis AV1n adaptation to temperature change
title_full_unstemmed Proteomic and in silico analyses of dextran synthesis influence on Leuconostoc lactis AV1n adaptation to temperature change
title_short Proteomic and in silico analyses of dextran synthesis influence on Leuconostoc lactis AV1n adaptation to temperature change
title_sort proteomic and in silico analyses of dextran synthesis influence on leuconostoc lactis av1n adaptation to temperature change
topic Leuconostoc
dextran
exopolysaccharides
lactic acid bacteria
proteomic
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.1077375/full
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