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Microbial Interaction between Lactiplantibacillus plantarum and Saccharomyces cerevisiae: Transcriptome Level Mechanism of Cell-Cell Antagonism

Lactiplantibacillus plantarum and Saccharomyces cerevisiae are frequently co-isolated in food, although playing different roles. This study aimed at investigating the microbial interaction between L. plantarum and S. cerevisiae, especially cell-cell direct interaction and their mechanism. Cell-cell...

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Autores principales: Liu, Junyan, Huang, Teng-Yi, Liu, Gongliang, Ye, Yanrui, Soteyome, Thanapop, Seneviratne, Gamini, Xiao, Gengsheng, Xu, Zhenbo, Kjellerup, Birthe V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9604076/
https://www.ncbi.nlm.nih.gov/pubmed/35980205
http://dx.doi.org/10.1128/spectrum.01433-22
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author Liu, Junyan
Huang, Teng-Yi
Liu, Gongliang
Ye, Yanrui
Soteyome, Thanapop
Seneviratne, Gamini
Xiao, Gengsheng
Xu, Zhenbo
Kjellerup, Birthe V.
author_facet Liu, Junyan
Huang, Teng-Yi
Liu, Gongliang
Ye, Yanrui
Soteyome, Thanapop
Seneviratne, Gamini
Xiao, Gengsheng
Xu, Zhenbo
Kjellerup, Birthe V.
author_sort Liu, Junyan
collection PubMed
description Lactiplantibacillus plantarum and Saccharomyces cerevisiae are frequently co-isolated in food, although playing different roles. This study aimed at investigating the microbial interaction between L. plantarum and S. cerevisiae, especially cell-cell direct interaction and their mechanism. Cell-cell and supernatant-cell coculture models were set up, with CFU counting, OD(600) measurement, optical and atomic force microscopy performed to examine the growth and morphology of L. plantarum and S. cerevisiae cells. In cell-cell coculture model, L. plantarum cells inhibited S. cerevisiae growth (inhibition rate ~80%) with its own growth pattern unaffected. Cell-cell aggregation happened during coculture with surface roughness changed and partial S. cerevisiae cell lysis. Mature (24 h) L. plantarum cell-free culture supernatant showed inhibition (35%-75%) on S. cerevisiae growth independent of pH level, while supernatant from L. plantarum-S. cerevisiae coculture showed relatively stronger inhibition. Upon transcriptomics analysis, hypothesis on the mechanism of microbial interaction between L. plantarum and S. cerevisiae was demonstrated. When L. plantarum cell density reached threshold at 24 h, all genes in lamBDCA quorum sensing (QS) system was upregulated to potentially increase adhesion capability, leading to the aggregation to S. cerevisiae cell. The downregulation of whole basic physiological activity from DNA to RNA to protein, cell cycle, meiosis, and mitogen-activated protein kinase (MAPK) signaling pathways, as well as growth maintenance essential genes ari1, skg6, and kex2/gas1 might induce the decreased growth and proliferation rate and partial death of S. cerevisiae cells in coculture. IMPORTANCE L. plantarum and S. cerevisiae are frequently co-isolated in food, although playing different roles. The co-existence of L. plantarum and S. cerevisiae could result in variable effects, raising economic benefits and safety concerns in food industry. Previous research has reported the microbial interaction between L. plantarum and S. cerevisiae mainly rely on the signaling through extracellular metabolites. However, cell-cell aggregation has been observed with mechanism remain unknown. In the current study, the microbial interaction between L. plantarum and S. cerevisiae was investigated with emphasis on cell-cell direct interaction and further in-depth transcriptome level study showed the key role of lamBDCA quorum sensing system in L. plantarum. The results yield from this study demonstrated the antagonistic effect between L. plantarum and S. cerevisiae.
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spelling pubmed-96040762022-10-27 Microbial Interaction between Lactiplantibacillus plantarum and Saccharomyces cerevisiae: Transcriptome Level Mechanism of Cell-Cell Antagonism Liu, Junyan Huang, Teng-Yi Liu, Gongliang Ye, Yanrui Soteyome, Thanapop Seneviratne, Gamini Xiao, Gengsheng Xu, Zhenbo Kjellerup, Birthe V. Microbiol Spectr Research Article Lactiplantibacillus plantarum and Saccharomyces cerevisiae are frequently co-isolated in food, although playing different roles. This study aimed at investigating the microbial interaction between L. plantarum and S. cerevisiae, especially cell-cell direct interaction and their mechanism. Cell-cell and supernatant-cell coculture models were set up, with CFU counting, OD(600) measurement, optical and atomic force microscopy performed to examine the growth and morphology of L. plantarum and S. cerevisiae cells. In cell-cell coculture model, L. plantarum cells inhibited S. cerevisiae growth (inhibition rate ~80%) with its own growth pattern unaffected. Cell-cell aggregation happened during coculture with surface roughness changed and partial S. cerevisiae cell lysis. Mature (24 h) L. plantarum cell-free culture supernatant showed inhibition (35%-75%) on S. cerevisiae growth independent of pH level, while supernatant from L. plantarum-S. cerevisiae coculture showed relatively stronger inhibition. Upon transcriptomics analysis, hypothesis on the mechanism of microbial interaction between L. plantarum and S. cerevisiae was demonstrated. When L. plantarum cell density reached threshold at 24 h, all genes in lamBDCA quorum sensing (QS) system was upregulated to potentially increase adhesion capability, leading to the aggregation to S. cerevisiae cell. The downregulation of whole basic physiological activity from DNA to RNA to protein, cell cycle, meiosis, and mitogen-activated protein kinase (MAPK) signaling pathways, as well as growth maintenance essential genes ari1, skg6, and kex2/gas1 might induce the decreased growth and proliferation rate and partial death of S. cerevisiae cells in coculture. IMPORTANCE L. plantarum and S. cerevisiae are frequently co-isolated in food, although playing different roles. The co-existence of L. plantarum and S. cerevisiae could result in variable effects, raising economic benefits and safety concerns in food industry. Previous research has reported the microbial interaction between L. plantarum and S. cerevisiae mainly rely on the signaling through extracellular metabolites. However, cell-cell aggregation has been observed with mechanism remain unknown. In the current study, the microbial interaction between L. plantarum and S. cerevisiae was investigated with emphasis on cell-cell direct interaction and further in-depth transcriptome level study showed the key role of lamBDCA quorum sensing system in L. plantarum. The results yield from this study demonstrated the antagonistic effect between L. plantarum and S. cerevisiae. American Society for Microbiology 2022-08-18 /pmc/articles/PMC9604076/ /pubmed/35980205 http://dx.doi.org/10.1128/spectrum.01433-22 Text en Copyright © 2022 Liu et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Liu, Junyan
Huang, Teng-Yi
Liu, Gongliang
Ye, Yanrui
Soteyome, Thanapop
Seneviratne, Gamini
Xiao, Gengsheng
Xu, Zhenbo
Kjellerup, Birthe V.
Microbial Interaction between Lactiplantibacillus plantarum and Saccharomyces cerevisiae: Transcriptome Level Mechanism of Cell-Cell Antagonism
title Microbial Interaction between Lactiplantibacillus plantarum and Saccharomyces cerevisiae: Transcriptome Level Mechanism of Cell-Cell Antagonism
title_full Microbial Interaction between Lactiplantibacillus plantarum and Saccharomyces cerevisiae: Transcriptome Level Mechanism of Cell-Cell Antagonism
title_fullStr Microbial Interaction between Lactiplantibacillus plantarum and Saccharomyces cerevisiae: Transcriptome Level Mechanism of Cell-Cell Antagonism
title_full_unstemmed Microbial Interaction between Lactiplantibacillus plantarum and Saccharomyces cerevisiae: Transcriptome Level Mechanism of Cell-Cell Antagonism
title_short Microbial Interaction between Lactiplantibacillus plantarum and Saccharomyces cerevisiae: Transcriptome Level Mechanism of Cell-Cell Antagonism
title_sort microbial interaction between lactiplantibacillus plantarum and saccharomyces cerevisiae: transcriptome level mechanism of cell-cell antagonism
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9604076/
https://www.ncbi.nlm.nih.gov/pubmed/35980205
http://dx.doi.org/10.1128/spectrum.01433-22
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