Identification of Quinone Degradation as a Triggering Event for Intense Pulsed Light-Elicited Metabolic Changes in <i>Escherichia coli</i> by Metabolomic Fingerprinting

Intense pulsed light (IPL) is becoming a new technical platform for disinfecting food against pathogenic bacteria. Metabolic changes are deemed to occur in bacteria as either the causes or the consequences of IPL-elicited bactericidal and bacteriostatic effects. However, little is known about the in...

Full description

Bibliographic Details
Main Authors: Qingqing Mao, Juer Liu, Justin R. Wiertzema, Dongjie Chen, Paul Chen, David J. Baumler, Roger Ruan, Chi Chen
Format: Article
Language:English
Published: MDPI AG 2021-02-01
Series:Metabolites
Subjects:
Online Access:https://www.mdpi.com/2218-1989/11/2/102
_version_ 1797411508252049408
author Qingqing Mao
Juer Liu
Justin R. Wiertzema
Dongjie Chen
Paul Chen
David J. Baumler
Roger Ruan
Chi Chen
author_facet Qingqing Mao
Juer Liu
Justin R. Wiertzema
Dongjie Chen
Paul Chen
David J. Baumler
Roger Ruan
Chi Chen
author_sort Qingqing Mao
collection DOAJ
description Intense pulsed light (IPL) is becoming a new technical platform for disinfecting food against pathogenic bacteria. Metabolic changes are deemed to occur in bacteria as either the causes or the consequences of IPL-elicited bactericidal and bacteriostatic effects. However, little is known about the influences of IPL on bacterial metabolome. In this study, the IPL treatment was applied to <i>E. coli</i> K-12 for 0–20 s, leading to time- and dose-dependent reductions in colony-forming units (CFU) and morphological changes. Both membrane lipids and cytoplasmic metabolites of the control and IPL-treated <i>E. coli</i> were examined by the liquid chromatography-mass spectrometry (LC-MS)-based metabolomic fingerprinting. The results from multivariate modeling and marker identification indicate that the metabolites in electron transport chain (ETC), redox response, glycolysis, amino acid, and nucleotide metabolism were selectively affected by the IPL treatments. The time courses and scales of these metabolic changes, together with the biochemical connections among them, revealed a cascade of events that might be initiated by the degradation of quinone electron carriers and then followed by oxidative stress, disruption of intermediary metabolism, nucleotide degradation, and morphological changes. Therefore, the degradations of membrane quinones, especially the rapid depletion of menaquinone-8 (MK-8), can be considered as a triggering event in the IPL-elicited metabolic changes in <i>E. coli</i>.
first_indexed 2024-03-09T04:47:04Z
format Article
id doaj.art-954e5835d6ff4712ad3c3956bd4f25fd
institution Directory Open Access Journal
issn 2218-1989
language English
last_indexed 2024-03-09T04:47:04Z
publishDate 2021-02-01
publisher MDPI AG
record_format Article
series Metabolites
spelling doaj.art-954e5835d6ff4712ad3c3956bd4f25fd2023-12-03T13:14:54ZengMDPI AGMetabolites2218-19892021-02-0111210210.3390/metabo11020102Identification of Quinone Degradation as a Triggering Event for Intense Pulsed Light-Elicited Metabolic Changes in <i>Escherichia coli</i> by Metabolomic FingerprintingQingqing Mao0Juer Liu1Justin R. Wiertzema2Dongjie Chen3Paul Chen4David J. Baumler5Roger Ruan6Chi Chen7Department of Food Science and Nutrition, University of Minnesota, 1334 Eckles Ave, Saint Paul, MN 55108, USADepartment of Food Science and Nutrition, University of Minnesota, 1334 Eckles Ave, Saint Paul, MN 55108, USADepartment of Food Science and Nutrition, University of Minnesota, 1334 Eckles Ave, Saint Paul, MN 55108, USADepartment of Food Science and Nutrition, University of Minnesota, 1334 Eckles Ave, Saint Paul, MN 55108, USADepartment of Bioproducts and Biosystems Engineering, University of Minnesota, 1390 Eckles Ave., Saint Paul, MN 55108, USADepartment of Food Science and Nutrition, University of Minnesota, 1334 Eckles Ave, Saint Paul, MN 55108, USADepartment of Bioproducts and Biosystems Engineering, University of Minnesota, 1390 Eckles Ave., Saint Paul, MN 55108, USADepartment of Food Science and Nutrition, University of Minnesota, 1334 Eckles Ave, Saint Paul, MN 55108, USAIntense pulsed light (IPL) is becoming a new technical platform for disinfecting food against pathogenic bacteria. Metabolic changes are deemed to occur in bacteria as either the causes or the consequences of IPL-elicited bactericidal and bacteriostatic effects. However, little is known about the influences of IPL on bacterial metabolome. In this study, the IPL treatment was applied to <i>E. coli</i> K-12 for 0–20 s, leading to time- and dose-dependent reductions in colony-forming units (CFU) and morphological changes. Both membrane lipids and cytoplasmic metabolites of the control and IPL-treated <i>E. coli</i> were examined by the liquid chromatography-mass spectrometry (LC-MS)-based metabolomic fingerprinting. The results from multivariate modeling and marker identification indicate that the metabolites in electron transport chain (ETC), redox response, glycolysis, amino acid, and nucleotide metabolism were selectively affected by the IPL treatments. The time courses and scales of these metabolic changes, together with the biochemical connections among them, revealed a cascade of events that might be initiated by the degradation of quinone electron carriers and then followed by oxidative stress, disruption of intermediary metabolism, nucleotide degradation, and morphological changes. Therefore, the degradations of membrane quinones, especially the rapid depletion of menaquinone-8 (MK-8), can be considered as a triggering event in the IPL-elicited metabolic changes in <i>E. coli</i>.https://www.mdpi.com/2218-1989/11/2/102intense pulsed light<i>Escherichia coli</i>bacterial metabolomemembrane quinonesoxidative stressintermediary metabolism
spellingShingle Qingqing Mao
Juer Liu
Justin R. Wiertzema
Dongjie Chen
Paul Chen
David J. Baumler
Roger Ruan
Chi Chen
Identification of Quinone Degradation as a Triggering Event for Intense Pulsed Light-Elicited Metabolic Changes in <i>Escherichia coli</i> by Metabolomic Fingerprinting
Metabolites
intense pulsed light
<i>Escherichia coli</i>
bacterial metabolome
membrane quinones
oxidative stress
intermediary metabolism
title Identification of Quinone Degradation as a Triggering Event for Intense Pulsed Light-Elicited Metabolic Changes in <i>Escherichia coli</i> by Metabolomic Fingerprinting
title_full Identification of Quinone Degradation as a Triggering Event for Intense Pulsed Light-Elicited Metabolic Changes in <i>Escherichia coli</i> by Metabolomic Fingerprinting
title_fullStr Identification of Quinone Degradation as a Triggering Event for Intense Pulsed Light-Elicited Metabolic Changes in <i>Escherichia coli</i> by Metabolomic Fingerprinting
title_full_unstemmed Identification of Quinone Degradation as a Triggering Event for Intense Pulsed Light-Elicited Metabolic Changes in <i>Escherichia coli</i> by Metabolomic Fingerprinting
title_short Identification of Quinone Degradation as a Triggering Event for Intense Pulsed Light-Elicited Metabolic Changes in <i>Escherichia coli</i> by Metabolomic Fingerprinting
title_sort identification of quinone degradation as a triggering event for intense pulsed light elicited metabolic changes in i escherichia coli i by metabolomic fingerprinting
topic intense pulsed light
<i>Escherichia coli</i>
bacterial metabolome
membrane quinones
oxidative stress
intermediary metabolism
url https://www.mdpi.com/2218-1989/11/2/102
work_keys_str_mv AT qingqingmao identificationofquinonedegradationasatriggeringeventforintensepulsedlightelicitedmetabolicchangesiniescherichiacoliibymetabolomicfingerprinting
AT juerliu identificationofquinonedegradationasatriggeringeventforintensepulsedlightelicitedmetabolicchangesiniescherichiacoliibymetabolomicfingerprinting
AT justinrwiertzema identificationofquinonedegradationasatriggeringeventforintensepulsedlightelicitedmetabolicchangesiniescherichiacoliibymetabolomicfingerprinting
AT dongjiechen identificationofquinonedegradationasatriggeringeventforintensepulsedlightelicitedmetabolicchangesiniescherichiacoliibymetabolomicfingerprinting
AT paulchen identificationofquinonedegradationasatriggeringeventforintensepulsedlightelicitedmetabolicchangesiniescherichiacoliibymetabolomicfingerprinting
AT davidjbaumler identificationofquinonedegradationasatriggeringeventforintensepulsedlightelicitedmetabolicchangesiniescherichiacoliibymetabolomicfingerprinting
AT rogerruan identificationofquinonedegradationasatriggeringeventforintensepulsedlightelicitedmetabolicchangesiniescherichiacoliibymetabolomicfingerprinting
AT chichen identificationofquinonedegradationasatriggeringeventforintensepulsedlightelicitedmetabolicchangesiniescherichiacoliibymetabolomicfingerprinting