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Transcriptomic Analysis of Pediococcus pentosaceus Reveals Carbohydrate Metabolic Dynamics Under Lactic Acid Stress

Stress physiology of lactic acid bacteria (LAB) is crucial to their ecological fitness and applicational implications. As a self-imposed stress, lactic acid is the major final metabolic product of LAB and its accumulation can be detrimental to bacterial cells. However, the relationship between LAB c...

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Autores principales: Han, Dong, Yan, Qiaojuan, Liu, Jun, Jiang, Zhengqiang, Yang, Shaoqing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8481956/
https://www.ncbi.nlm.nih.gov/pubmed/34603267
http://dx.doi.org/10.3389/fmicb.2021.736411
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author Han, Dong
Yan, Qiaojuan
Liu, Jun
Jiang, Zhengqiang
Yang, Shaoqing
author_facet Han, Dong
Yan, Qiaojuan
Liu, Jun
Jiang, Zhengqiang
Yang, Shaoqing
author_sort Han, Dong
collection PubMed
description Stress physiology of lactic acid bacteria (LAB) is crucial to their ecological fitness and applicational implications. As a self-imposed stress, lactic acid is the major final metabolic product of LAB and its accumulation can be detrimental to bacterial cells. However, the relationship between LAB carbohydrate metabolism, the primary energy supplying bioactivities, and lactic acid stress responses is not fully understood. Pediococcus pentosaceus has been recognized as an important cell factory and demonstrated probiotic activities. This study investigated behavior of P. pentosaceus under lactic and acetic acid stresses, particularly with supplementations of metabolizable carbohydrates. Lactic and acetic acid retain similar growth stagnation effect, and both resulted in cell death in P. pentosaceus. All metabolizable carbohydrates improved bacterial survival compared to lactic acid control, while xylooligosaccharides (XOS) exerted the highest viability protective efficacy, 0.82 log CFU/mL higher population survived than other carbohydrates after 30 h of incubation. RNA-seq pipeline showcased the intensive global transcriptional responses of P. pentosaceus to lactic acid, which caused significant regulations (more than 2 Log(2) fold) of 16.5% of total mRNA coding genes. Glucose mainly led to gene suppressions (83 genes) while XOS led to gene up-regulations (19 genes) under lactic acid stress. RT-qPCR study found that RNA polymerase-centered transcriptional regulation is the primary regulatory approach in evaluated culture conditions. The synergy between lactic acid stress and carbohydrate metabolism should be attentively contemplated in future studies and applications.
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spelling pubmed-84819562021-10-01 Transcriptomic Analysis of Pediococcus pentosaceus Reveals Carbohydrate Metabolic Dynamics Under Lactic Acid Stress Han, Dong Yan, Qiaojuan Liu, Jun Jiang, Zhengqiang Yang, Shaoqing Front Microbiol Microbiology Stress physiology of lactic acid bacteria (LAB) is crucial to their ecological fitness and applicational implications. As a self-imposed stress, lactic acid is the major final metabolic product of LAB and its accumulation can be detrimental to bacterial cells. However, the relationship between LAB carbohydrate metabolism, the primary energy supplying bioactivities, and lactic acid stress responses is not fully understood. Pediococcus pentosaceus has been recognized as an important cell factory and demonstrated probiotic activities. This study investigated behavior of P. pentosaceus under lactic and acetic acid stresses, particularly with supplementations of metabolizable carbohydrates. Lactic and acetic acid retain similar growth stagnation effect, and both resulted in cell death in P. pentosaceus. All metabolizable carbohydrates improved bacterial survival compared to lactic acid control, while xylooligosaccharides (XOS) exerted the highest viability protective efficacy, 0.82 log CFU/mL higher population survived than other carbohydrates after 30 h of incubation. RNA-seq pipeline showcased the intensive global transcriptional responses of P. pentosaceus to lactic acid, which caused significant regulations (more than 2 Log(2) fold) of 16.5% of total mRNA coding genes. Glucose mainly led to gene suppressions (83 genes) while XOS led to gene up-regulations (19 genes) under lactic acid stress. RT-qPCR study found that RNA polymerase-centered transcriptional regulation is the primary regulatory approach in evaluated culture conditions. The synergy between lactic acid stress and carbohydrate metabolism should be attentively contemplated in future studies and applications. Frontiers Media S.A. 2021-09-16 /pmc/articles/PMC8481956/ /pubmed/34603267 http://dx.doi.org/10.3389/fmicb.2021.736411 Text en Copyright © 2021 Han, Yan, Liu, Jiang and Yang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Han, Dong
Yan, Qiaojuan
Liu, Jun
Jiang, Zhengqiang
Yang, Shaoqing
Transcriptomic Analysis of Pediococcus pentosaceus Reveals Carbohydrate Metabolic Dynamics Under Lactic Acid Stress
title Transcriptomic Analysis of Pediococcus pentosaceus Reveals Carbohydrate Metabolic Dynamics Under Lactic Acid Stress
title_full Transcriptomic Analysis of Pediococcus pentosaceus Reveals Carbohydrate Metabolic Dynamics Under Lactic Acid Stress
title_fullStr Transcriptomic Analysis of Pediococcus pentosaceus Reveals Carbohydrate Metabolic Dynamics Under Lactic Acid Stress
title_full_unstemmed Transcriptomic Analysis of Pediococcus pentosaceus Reveals Carbohydrate Metabolic Dynamics Under Lactic Acid Stress
title_short Transcriptomic Analysis of Pediococcus pentosaceus Reveals Carbohydrate Metabolic Dynamics Under Lactic Acid Stress
title_sort transcriptomic analysis of pediococcus pentosaceus reveals carbohydrate metabolic dynamics under lactic acid stress
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8481956/
https://www.ncbi.nlm.nih.gov/pubmed/34603267
http://dx.doi.org/10.3389/fmicb.2021.736411
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