Maintenance of translational elongation rate underlies the survival of Escherichia coli during oxidative stress
Abstract To cope with harsh circumstances, bacterial cells must initiate cellular stress response programs, which demands the de novo synthesis of many stress defense proteins. Reactive oxygen species (ROS) is a universal environmental stressor for both prokaryotic cells and eukaryotic cells. Howeve...
Gespeichert in:
Veröffentlicht in: | Nucleic acids research 2019-08, Vol.47 (14), p.7592-7604 |
---|---|
Hauptverfasser: | , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 7604 |
---|---|
container_issue | 14 |
container_start_page | 7592 |
container_title | Nucleic acids research |
container_volume | 47 |
creator | Zhu, Manlu Dai, Xiongfeng |
description | Abstract
To cope with harsh circumstances, bacterial cells must initiate cellular stress response programs, which demands the de novo synthesis of many stress defense proteins. Reactive oxygen species (ROS) is a universal environmental stressor for both prokaryotic cells and eukaryotic cells. However, the physiological burden that limits the survival of bacterial cells during oxidative stress remains elusive. Here we quantitatively characterize the cell growth and translational elongation rate of Escherichia coli cells treated with different doses of hydrogen peroxide. Cell growth is immediately arrested by low to moderate levels of hydrogen peroxide, but completely recovers after a certain lag time. The lag time depends positively on the dose of hydrogen peroxide. During the lag time, translational elongation rate drops by as much as ∼90% at initial stage and recovers to its normal state later, a phenomenon resulting from the dramatic alteration in cellular tRNA pools during oxidative stress. However, translational elongation is completely stalled at a certain threshold-level of hydrogen peroxide, at which cells ultimately fail to resume growth. Although the mRNA transcription of oxidative defense genes in oxyR regulon is dramatically induced upon hydrogen peroxide treatment, the extreme slow-down of translational elongation during high levels of hydrogen peroxide has severely compromised the timely synthesis of those oxidative defense proteins. Our study demonstrates that the tRNA-limited translational elongation is a key physiological bottleneck that the bacteria must overcome to counteract ROS, and the maintenance of translational elongation rate for timely synthesis of stress defense proteins is crucial for cells to smoothly get over the oxidative stress. |
doi_str_mv | 10.1093/nar/gkz467 |
format | Article |
fullrecord | <record><control><sourceid>oup_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6698664</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><oup_id>10.1093/nar/gkz467</oup_id><sourcerecordid>10.1093/nar/gkz467</sourcerecordid><originalsourceid>FETCH-LOGICAL-c408t-1e3a4722ae71cb87629a83d2dff403c8559fff42688dedd82f0fe7975a6fb9693</originalsourceid><addsrcrecordid>eNp9kE1PAyEQhonR2Ppx8QcYLl5MVmFhWfZiYhq_khovet5QGFp0hQZ2G_XXi1aNXjwxZJ55JvMidEDJCSUNO_Uqns6f3rioN9CYMlEWvBHlJhoTRqqCEi5HaCelR0IopxXfRiNGKcs1G6Nwq5zvwSuvAQeL-6h86lTvglcdhi74-ecHR9UDHryB2DlIuF8ATkNcuVXG8txF0guITi-cwjp0DpshOj_H4cWZLFhluo-Q0h7asqpLsP_17qKHy4v7yXUxvbu6mZxPC82J7AsKTPG6LBXUVM9kLcpGSWZKYy0nTMuqamwuSyGlAWNkaYmFuqkrJeysEQ3bRWdr73KYPYPR4PNlXbuM7lnF1zYo1_7teLdo52HVCtFIIXgWHK8FOoaUItifWUraj9jbHHu7jj3Dh7-3_aDfOWfgaA2EYfmf6B3sSJBY</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype></control><display><type>article</type><title>Maintenance of translational elongation rate underlies the survival of Escherichia coli during oxidative stress</title><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>Oxford Journals Open Access Collection</source><source>PubMed Central</source><source>Free Full-Text Journals in Chemistry</source><creator>Zhu, Manlu ; Dai, Xiongfeng</creator><creatorcontrib>Zhu, Manlu ; Dai, Xiongfeng</creatorcontrib><description>Abstract
To cope with harsh circumstances, bacterial cells must initiate cellular stress response programs, which demands the de novo synthesis of many stress defense proteins. Reactive oxygen species (ROS) is a universal environmental stressor for both prokaryotic cells and eukaryotic cells. However, the physiological burden that limits the survival of bacterial cells during oxidative stress remains elusive. Here we quantitatively characterize the cell growth and translational elongation rate of Escherichia coli cells treated with different doses of hydrogen peroxide. Cell growth is immediately arrested by low to moderate levels of hydrogen peroxide, but completely recovers after a certain lag time. The lag time depends positively on the dose of hydrogen peroxide. During the lag time, translational elongation rate drops by as much as ∼90% at initial stage and recovers to its normal state later, a phenomenon resulting from the dramatic alteration in cellular tRNA pools during oxidative stress. However, translational elongation is completely stalled at a certain threshold-level of hydrogen peroxide, at which cells ultimately fail to resume growth. Although the mRNA transcription of oxidative defense genes in oxyR regulon is dramatically induced upon hydrogen peroxide treatment, the extreme slow-down of translational elongation during high levels of hydrogen peroxide has severely compromised the timely synthesis of those oxidative defense proteins. Our study demonstrates that the tRNA-limited translational elongation is a key physiological bottleneck that the bacteria must overcome to counteract ROS, and the maintenance of translational elongation rate for timely synthesis of stress defense proteins is crucial for cells to smoothly get over the oxidative stress.</description><identifier>ISSN: 0305-1048</identifier><identifier>EISSN: 1362-4962</identifier><identifier>DOI: 10.1093/nar/gkz467</identifier><identifier>PMID: 31131413</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Adaptation, Physiological - drug effects ; Adaptation, Physiological - genetics ; Dose-Response Relationship, Drug ; Escherichia coli - drug effects ; Escherichia coli - genetics ; Escherichia coli - metabolism ; Escherichia coli Proteins - genetics ; Escherichia coli Proteins - metabolism ; Hydrogen Peroxide - pharmacology ; Microbial Viability - drug effects ; Microbial Viability - genetics ; Models, Genetic ; Oxidants - pharmacology ; Oxidative Stress ; Protein Biosynthesis - drug effects ; Reactive Oxygen Species - metabolism ; RNA and RNA-protein complexes ; Time Factors</subject><ispartof>Nucleic acids research, 2019-08, Vol.47 (14), p.7592-7604</ispartof><rights>The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research. 2019</rights><rights>The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c408t-1e3a4722ae71cb87629a83d2dff403c8559fff42688dedd82f0fe7975a6fb9693</citedby><cites>FETCH-LOGICAL-c408t-1e3a4722ae71cb87629a83d2dff403c8559fff42688dedd82f0fe7975a6fb9693</cites><orcidid>0000-0002-8225-1799</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6698664/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6698664/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,1605,27926,27927,53793,53795</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31131413$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhu, Manlu</creatorcontrib><creatorcontrib>Dai, Xiongfeng</creatorcontrib><title>Maintenance of translational elongation rate underlies the survival of Escherichia coli during oxidative stress</title><title>Nucleic acids research</title><addtitle>Nucleic Acids Res</addtitle><description>Abstract
To cope with harsh circumstances, bacterial cells must initiate cellular stress response programs, which demands the de novo synthesis of many stress defense proteins. Reactive oxygen species (ROS) is a universal environmental stressor for both prokaryotic cells and eukaryotic cells. However, the physiological burden that limits the survival of bacterial cells during oxidative stress remains elusive. Here we quantitatively characterize the cell growth and translational elongation rate of Escherichia coli cells treated with different doses of hydrogen peroxide. Cell growth is immediately arrested by low to moderate levels of hydrogen peroxide, but completely recovers after a certain lag time. The lag time depends positively on the dose of hydrogen peroxide. During the lag time, translational elongation rate drops by as much as ∼90% at initial stage and recovers to its normal state later, a phenomenon resulting from the dramatic alteration in cellular tRNA pools during oxidative stress. However, translational elongation is completely stalled at a certain threshold-level of hydrogen peroxide, at which cells ultimately fail to resume growth. Although the mRNA transcription of oxidative defense genes in oxyR regulon is dramatically induced upon hydrogen peroxide treatment, the extreme slow-down of translational elongation during high levels of hydrogen peroxide has severely compromised the timely synthesis of those oxidative defense proteins. Our study demonstrates that the tRNA-limited translational elongation is a key physiological bottleneck that the bacteria must overcome to counteract ROS, and the maintenance of translational elongation rate for timely synthesis of stress defense proteins is crucial for cells to smoothly get over the oxidative stress.</description><subject>Adaptation, Physiological - drug effects</subject><subject>Adaptation, Physiological - genetics</subject><subject>Dose-Response Relationship, Drug</subject><subject>Escherichia coli - drug effects</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - metabolism</subject><subject>Escherichia coli Proteins - genetics</subject><subject>Escherichia coli Proteins - metabolism</subject><subject>Hydrogen Peroxide - pharmacology</subject><subject>Microbial Viability - drug effects</subject><subject>Microbial Viability - genetics</subject><subject>Models, Genetic</subject><subject>Oxidants - pharmacology</subject><subject>Oxidative Stress</subject><subject>Protein Biosynthesis - drug effects</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>RNA and RNA-protein complexes</subject><subject>Time Factors</subject><issn>0305-1048</issn><issn>1362-4962</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNp9kE1PAyEQhonR2Ppx8QcYLl5MVmFhWfZiYhq_khovet5QGFp0hQZ2G_XXi1aNXjwxZJ55JvMidEDJCSUNO_Uqns6f3rioN9CYMlEWvBHlJhoTRqqCEi5HaCelR0IopxXfRiNGKcs1G6Nwq5zvwSuvAQeL-6h86lTvglcdhi74-ecHR9UDHryB2DlIuF8ATkNcuVXG8txF0guITi-cwjp0DpshOj_H4cWZLFhluo-Q0h7asqpLsP_17qKHy4v7yXUxvbu6mZxPC82J7AsKTPG6LBXUVM9kLcpGSWZKYy0nTMuqamwuSyGlAWNkaYmFuqkrJeysEQ3bRWdr73KYPYPR4PNlXbuM7lnF1zYo1_7teLdo52HVCtFIIXgWHK8FOoaUItifWUraj9jbHHu7jj3Dh7-3_aDfOWfgaA2EYfmf6B3sSJBY</recordid><startdate>20190822</startdate><enddate>20190822</enddate><creator>Zhu, Manlu</creator><creator>Dai, Xiongfeng</creator><general>Oxford University Press</general><scope>TOX</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-8225-1799</orcidid></search><sort><creationdate>20190822</creationdate><title>Maintenance of translational elongation rate underlies the survival of Escherichia coli during oxidative stress</title><author>Zhu, Manlu ; Dai, Xiongfeng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c408t-1e3a4722ae71cb87629a83d2dff403c8559fff42688dedd82f0fe7975a6fb9693</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Adaptation, Physiological - drug effects</topic><topic>Adaptation, Physiological - genetics</topic><topic>Dose-Response Relationship, Drug</topic><topic>Escherichia coli - drug effects</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli - metabolism</topic><topic>Escherichia coli Proteins - genetics</topic><topic>Escherichia coli Proteins - metabolism</topic><topic>Hydrogen Peroxide - pharmacology</topic><topic>Microbial Viability - drug effects</topic><topic>Microbial Viability - genetics</topic><topic>Models, Genetic</topic><topic>Oxidants - pharmacology</topic><topic>Oxidative Stress</topic><topic>Protein Biosynthesis - drug effects</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>RNA and RNA-protein complexes</topic><topic>Time Factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhu, Manlu</creatorcontrib><creatorcontrib>Dai, Xiongfeng</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nucleic acids research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhu, Manlu</au><au>Dai, Xiongfeng</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Maintenance of translational elongation rate underlies the survival of Escherichia coli during oxidative stress</atitle><jtitle>Nucleic acids research</jtitle><addtitle>Nucleic Acids Res</addtitle><date>2019-08-22</date><risdate>2019</risdate><volume>47</volume><issue>14</issue><spage>7592</spage><epage>7604</epage><pages>7592-7604</pages><issn>0305-1048</issn><eissn>1362-4962</eissn><abstract>Abstract
To cope with harsh circumstances, bacterial cells must initiate cellular stress response programs, which demands the de novo synthesis of many stress defense proteins. Reactive oxygen species (ROS) is a universal environmental stressor for both prokaryotic cells and eukaryotic cells. However, the physiological burden that limits the survival of bacterial cells during oxidative stress remains elusive. Here we quantitatively characterize the cell growth and translational elongation rate of Escherichia coli cells treated with different doses of hydrogen peroxide. Cell growth is immediately arrested by low to moderate levels of hydrogen peroxide, but completely recovers after a certain lag time. The lag time depends positively on the dose of hydrogen peroxide. During the lag time, translational elongation rate drops by as much as ∼90% at initial stage and recovers to its normal state later, a phenomenon resulting from the dramatic alteration in cellular tRNA pools during oxidative stress. However, translational elongation is completely stalled at a certain threshold-level of hydrogen peroxide, at which cells ultimately fail to resume growth. Although the mRNA transcription of oxidative defense genes in oxyR regulon is dramatically induced upon hydrogen peroxide treatment, the extreme slow-down of translational elongation during high levels of hydrogen peroxide has severely compromised the timely synthesis of those oxidative defense proteins. Our study demonstrates that the tRNA-limited translational elongation is a key physiological bottleneck that the bacteria must overcome to counteract ROS, and the maintenance of translational elongation rate for timely synthesis of stress defense proteins is crucial for cells to smoothly get over the oxidative stress.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>31131413</pmid><doi>10.1093/nar/gkz467</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-8225-1799</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0305-1048 |
ispartof | Nucleic acids research, 2019-08, Vol.47 (14), p.7592-7604 |
issn | 0305-1048 1362-4962 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6698664 |
source | MEDLINE; DOAJ Directory of Open Access Journals; Oxford Journals Open Access Collection; PubMed Central; Free Full-Text Journals in Chemistry |
subjects | Adaptation, Physiological - drug effects Adaptation, Physiological - genetics Dose-Response Relationship, Drug Escherichia coli - drug effects Escherichia coli - genetics Escherichia coli - metabolism Escherichia coli Proteins - genetics Escherichia coli Proteins - metabolism Hydrogen Peroxide - pharmacology Microbial Viability - drug effects Microbial Viability - genetics Models, Genetic Oxidants - pharmacology Oxidative Stress Protein Biosynthesis - drug effects Reactive Oxygen Species - metabolism RNA and RNA-protein complexes Time Factors |
title | Maintenance of translational elongation rate underlies the survival of Escherichia coli during oxidative stress |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-18T05%3A51%3A22IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-oup_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Maintenance%20of%20translational%20elongation%20rate%20underlies%20the%20survival%20of%20Escherichia%20coli%20during%20oxidative%20stress&rft.jtitle=Nucleic%20acids%20research&rft.au=Zhu,%20Manlu&rft.date=2019-08-22&rft.volume=47&rft.issue=14&rft.spage=7592&rft.epage=7604&rft.pages=7592-7604&rft.issn=0305-1048&rft.eissn=1362-4962&rft_id=info:doi/10.1093/nar/gkz467&rft_dat=%3Coup_pubme%3E10.1093/nar/gkz467%3C/oup_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_id=info:pmid/31131413&rft_oup_id=10.1093/nar/gkz467&rfr_iscdi=true |