(p)ppGpp-mediated stress response induced by defects in outer membrane biogenesis and ATP production promotes survival in Escherichia coli
Cellular growth requires a high level of coordination to ensure that all processes run in concert. The role of the nucleotide alarmone (p)ppGpp has been extensively studied in response to external stresses, such as amino acid starvation, in Escherichia coli , but much less is known about the involve...
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| Veröffentlicht in: | Scientific reports 2019-02, Vol.9 (1), p.2934-2934, Article 2934 |
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| creator | Roghanian, Mohammad Semsey, Szabolcs Løbner-Olesen, Anders Jalalvand, Farshid |
| description | Cellular growth requires a high level of coordination to ensure that all processes run in concert. The role of the nucleotide alarmone (p)ppGpp has been extensively studied in response to external stresses, such as amino acid starvation, in
Escherichia coli
, but much less is known about the involvement of (p)ppGpp in response to perturbations in intracellular processes. We therefore employed CRISPRi to transcriptionally repress essential genes involved in 14 vital processes and investigated whether a (p)ppGpp-mediated response would be induced. We show that (p)ppGpp is produced and required for a pertinent stress response during interference with outer membrane biogenesis and ADP synthesis specifically. When these processes were perturbed via the transcriptional repression of essential genes, wild type
E. coli
MG1655 ceased growing and entered a semi-dormant state, whereas isogenic (p)ppGpp
0
cells continued to grow uncontrollably to the point of lysis. Furthermore,
in vivo
measurements revealed that the ATP levels were intrinsically offset in (p)ppGpp
0
cells, further indicating a role for the alarmone in cellular energy homeostasis. In summary, our investigation suggests that (p)ppGpp acts as a coordinator of cell growth in response to imbalances in outer membrane biogenesis and adenosine ribonucleotide synthesis, elucidating novel roles for (p)ppGpp in bacterial physiology. |
| doi_str_mv | 10.1038/s41598-019-39371-3 |
| format | Article |
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Escherichia coli
, but much less is known about the involvement of (p)ppGpp in response to perturbations in intracellular processes. We therefore employed CRISPRi to transcriptionally repress essential genes involved in 14 vital processes and investigated whether a (p)ppGpp-mediated response would be induced. We show that (p)ppGpp is produced and required for a pertinent stress response during interference with outer membrane biogenesis and ADP synthesis specifically. When these processes were perturbed via the transcriptional repression of essential genes, wild type
E. coli
MG1655 ceased growing and entered a semi-dormant state, whereas isogenic (p)ppGpp
0
cells continued to grow uncontrollably to the point of lysis. Furthermore,
in vivo
measurements revealed that the ATP levels were intrinsically offset in (p)ppGpp
0
cells, further indicating a role for the alarmone in cellular energy homeostasis. In summary, our investigation suggests that (p)ppGpp acts as a coordinator of cell growth in response to imbalances in outer membrane biogenesis and adenosine ribonucleotide synthesis, elucidating novel roles for (p)ppGpp in bacterial physiology.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-019-39371-3</identifier><identifier>PMID: 30814571</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>14 ; 14/35 ; 631/326/1320 ; 631/326/88 ; Adenosine ; Adenosine diphosphate ; Amino acid starvation ; Amino acids ; ATP ; Bacterial physiology ; Biosynthesis ; E coli ; Energy balance ; Escherichia coli ; Gene silencing ; Homeostasis ; Humanities and Social Sciences ; Lysis ; multidisciplinary ; Science ; Science (multidisciplinary) ; Starvation ; Stress response</subject><ispartof>Scientific reports, 2019-02, Vol.9 (1), p.2934-2934, Article 2934</ispartof><rights>The Author(s) 2019</rights><rights>This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c577t-a0ed7f9a96712b3fa85dc46e54802888cb4a7f518e8981b6b340bfffe4a50cbf3</citedby><cites>FETCH-LOGICAL-c577t-a0ed7f9a96712b3fa85dc46e54802888cb4a7f518e8981b6b340bfffe4a50cbf3</cites><orcidid>0000-0001-7920-8530</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/PMC6393671/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6393671/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27903,27904,41099,42168,51554,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30814571$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Roghanian, Mohammad</creatorcontrib><creatorcontrib>Semsey, Szabolcs</creatorcontrib><creatorcontrib>Løbner-Olesen, Anders</creatorcontrib><creatorcontrib>Jalalvand, Farshid</creatorcontrib><title>(p)ppGpp-mediated stress response induced by defects in outer membrane biogenesis and ATP production promotes survival in Escherichia coli</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>Cellular growth requires a high level of coordination to ensure that all processes run in concert. The role of the nucleotide alarmone (p)ppGpp has been extensively studied in response to external stresses, such as amino acid starvation, in
Escherichia coli
, but much less is known about the involvement of (p)ppGpp in response to perturbations in intracellular processes. We therefore employed CRISPRi to transcriptionally repress essential genes involved in 14 vital processes and investigated whether a (p)ppGpp-mediated response would be induced. We show that (p)ppGpp is produced and required for a pertinent stress response during interference with outer membrane biogenesis and ADP synthesis specifically. When these processes were perturbed via the transcriptional repression of essential genes, wild type
E. coli
MG1655 ceased growing and entered a semi-dormant state, whereas isogenic (p)ppGpp
0
cells continued to grow uncontrollably to the point of lysis. Furthermore,
in vivo
measurements revealed that the ATP levels were intrinsically offset in (p)ppGpp
0
cells, further indicating a role for the alarmone in cellular energy homeostasis. In summary, our investigation suggests that (p)ppGpp acts as a coordinator of cell growth in response to imbalances in outer membrane biogenesis and adenosine ribonucleotide synthesis, elucidating novel roles for (p)ppGpp in bacterial physiology.</description><subject>14</subject><subject>14/35</subject><subject>631/326/1320</subject><subject>631/326/88</subject><subject>Adenosine</subject><subject>Adenosine diphosphate</subject><subject>Amino acid starvation</subject><subject>Amino acids</subject><subject>ATP</subject><subject>Bacterial physiology</subject><subject>Biosynthesis</subject><subject>E coli</subject><subject>Energy balance</subject><subject>Escherichia coli</subject><subject>Gene silencing</subject><subject>Homeostasis</subject><subject>Humanities and Social Sciences</subject><subject>Lysis</subject><subject>multidisciplinary</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Starvation</subject><subject>Stress response</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>BENPR</sourceid><recordid>eNp9UU1v1DAQjRCIVqV_gAOyxKUcAv5IYueCVFWlIFWCQzlbtjPedZXYwZOs1L_QX42XLaVwwJI9o5k3bzzzquo1o-8ZFeoDNqztVU1ZX4teSFaLZ9Uxp01bc8H58yf-UXWKeEvLaXnfsP5ldSSoYk0r2XF1fza_m-erea4nGIJZYCC4ZEAk5ZlTRCAhDqsrcXtHBvDgFiwhktYFMplgstlEIDakDUTAgMTEgZzffCNzTqVwCSnu3SktgATXvAs7M-4ZLtFtIQe3DYa4NIZX1QtvRoTTB3tSff90eXPxub7-evXl4vy6dq2US20oDNL3pu8k41Z4o9rBNR20jaJcKeVsY6RvmQLVK2Y7KxpqvffQmJY668VJ9fHAO6-2DO0gLtmMes5hMvlOJxP035kYtnqTdroriy5NC8HZA0FOP1bARU8BHYxjWURaUXOmJOV9uQX69h_obVpzLOPtUZ1UQsmuoPgB5XJCzOAfP8Oo3qutD2rrorb-pbYWpejN0zEeS35rWwDiAMCSihvIf3r_h_YnUoO4yA</recordid><startdate>20190227</startdate><enddate>20190227</enddate><creator>Roghanian, Mohammad</creator><creator>Semsey, Szabolcs</creator><creator>Løbner-Olesen, Anders</creator><creator>Jalalvand, Farshid</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7920-8530</orcidid></search><sort><creationdate>20190227</creationdate><title>(p)ppGpp-mediated stress response induced by defects in outer membrane biogenesis and ATP production promotes survival in Escherichia coli</title><author>Roghanian, Mohammad ; Semsey, Szabolcs ; Løbner-Olesen, Anders ; Jalalvand, Farshid</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c577t-a0ed7f9a96712b3fa85dc46e54802888cb4a7f518e8981b6b340bfffe4a50cbf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>14</topic><topic>14/35</topic><topic>631/326/1320</topic><topic>631/326/88</topic><topic>Adenosine</topic><topic>Adenosine diphosphate</topic><topic>Amino acid starvation</topic><topic>Amino acids</topic><topic>ATP</topic><topic>Bacterial physiology</topic><topic>Biosynthesis</topic><topic>E coli</topic><topic>Energy balance</topic><topic>Escherichia coli</topic><topic>Gene silencing</topic><topic>Homeostasis</topic><topic>Humanities and Social Sciences</topic><topic>Lysis</topic><topic>multidisciplinary</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Starvation</topic><topic>Stress response</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Roghanian, Mohammad</creatorcontrib><creatorcontrib>Semsey, Szabolcs</creatorcontrib><creatorcontrib>Løbner-Olesen, Anders</creatorcontrib><creatorcontrib>Jalalvand, Farshid</creatorcontrib><collection>SpringerOpen</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Scientific reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Roghanian, Mohammad</au><au>Semsey, Szabolcs</au><au>Løbner-Olesen, Anders</au><au>Jalalvand, Farshid</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>(p)ppGpp-mediated stress response induced by defects in outer membrane biogenesis and ATP production promotes survival in Escherichia coli</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2019-02-27</date><risdate>2019</risdate><volume>9</volume><issue>1</issue><spage>2934</spage><epage>2934</epage><pages>2934-2934</pages><artnum>2934</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>Cellular growth requires a high level of coordination to ensure that all processes run in concert. The role of the nucleotide alarmone (p)ppGpp has been extensively studied in response to external stresses, such as amino acid starvation, in
Escherichia coli
, but much less is known about the involvement of (p)ppGpp in response to perturbations in intracellular processes. We therefore employed CRISPRi to transcriptionally repress essential genes involved in 14 vital processes and investigated whether a (p)ppGpp-mediated response would be induced. We show that (p)ppGpp is produced and required for a pertinent stress response during interference with outer membrane biogenesis and ADP synthesis specifically. When these processes were perturbed via the transcriptional repression of essential genes, wild type
E. coli
MG1655 ceased growing and entered a semi-dormant state, whereas isogenic (p)ppGpp
0
cells continued to grow uncontrollably to the point of lysis. Furthermore,
in vivo
measurements revealed that the ATP levels were intrinsically offset in (p)ppGpp
0
cells, further indicating a role for the alarmone in cellular energy homeostasis. In summary, our investigation suggests that (p)ppGpp acts as a coordinator of cell growth in response to imbalances in outer membrane biogenesis and adenosine ribonucleotide synthesis, elucidating novel roles for (p)ppGpp in bacterial physiology.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>30814571</pmid><doi>10.1038/s41598-019-39371-3</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-7920-8530</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | 14 14/35 631/326/1320 631/326/88 Adenosine Adenosine diphosphate Amino acid starvation Amino acids ATP Bacterial physiology Biosynthesis E coli Energy balance Escherichia coli Gene silencing Homeostasis Humanities and Social Sciences Lysis multidisciplinary Science Science (multidisciplinary) Starvation Stress response |
| title | (p)ppGpp-mediated stress response induced by defects in outer membrane biogenesis and ATP production promotes survival in Escherichia coli |
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