{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T22:09:59Z","timestamp":1790806199048,"version":"4.1.0"},"reference-count":62,"publisher":"American Society for Microbiology","issue":"3","license":[{"start":{"date-parts":[[2016,6,21]],"date-time":"2016-06-21T00:00:00Z","timestamp":1466467200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2016,7,6]],"date-time":"2016-07-06T00:00:00Z","timestamp":1467763200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"funder":[{"DOI":"10.13039\/100004440","name":"Wellcome Trust","doi-asserted-by":"publisher","award":["101824\/Z\/13\/Z"],"award-info":[{"award-number":["101824\/Z\/13\/Z"]}],"id":[{"id":"10.13039\/100004440","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","award":["BB\/J015016\/1"],"award-info":[{"award-number":["BB\/J015016\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000052","name":"HHS | NIH | NIH Office of the Director","doi-asserted-by":"publisher","award":["R01-GM061019"],"award-info":[{"award-number":["R01-GM061019"]}],"id":[{"id":"10.13039\/100000052","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["mBio"],"published-print":{"date-parts":[[2016,7,6]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    Peptidoglycan (PG) is an essential structural component of the bacterial cell wall and maintains the integrity and shape of the cell by forming a continuous layer around the cytoplasmic membrane. The thin PG layer of\n                    <jats:named-content content-type=\"genus-species\">Escherichia coli<\/jats:named-content>\n                    resides in the periplasm, a unique compartment whose composition and pH can vary depending on the local environment of the cell. Hence, the growth of the PG layer must be sufficiently robust to allow cell growth and division under different conditions. We have analyzed the PG composition of 28 mutants lacking multiple PG enzymes (penicillin-binding proteins [PBPs]) after growth in acidic or near-neutral-pH media. Statistical analysis of the muropeptide profiles identified\n                    <jats:sc>dd<\/jats:sc>\n                    -carboxypeptidases (DD-CPases) that were more active in cells grown at acidic pH. In particular, the absence of the DD-CPase PBP6b caused a significant increase in the pentapeptide content of PG as well as morphological defects when the cells were grown at acidic pH. Other DD-CPases (PBP4, PBP4b, PBP5, PBP6a, PBP7, and AmpH) and the PG synthase PBP1B made a smaller or null contribution to the pentapeptide-trimming activity at acidic pH. We solved the crystal structure of PBP6b and also demonstrated that the enzyme is more stable and has a lower\n                    <jats:italic>\n                      K\n                      <jats:sub>m<\/jats:sub>\n                    <\/jats:italic>\n                    at acidic pH, explaining why PBP6b is more active at low pH. Hence, PBP6b is a specialized DD-CPase that contributes to cell shape maintenance at low pH, and\n                    <jats:named-content content-type=\"genus-species\">E. coli<\/jats:named-content>\n                    appears to utilize redundant DD-CPases for normal growth under different conditions.\n                  <\/jats:p>\n                  <jats:p>\n                    <jats:bold>IMPORTANCE<\/jats:bold>\n                    <jats:named-content content-type=\"genus-species\">Escherichia coli<\/jats:named-content>\n                    requires peptidoglycan\n                    <jats:sc>dd<\/jats:sc>\n                    -carboxypeptidases to maintain cell shape by controlling the amount of pentapeptide substrates available to the peptidoglycan synthetic transpeptidases. Why\n                    <jats:named-content content-type=\"genus-species\">E. coli<\/jats:named-content>\n                    has eight, seemingly redundant\n                    <jats:sc>dd<\/jats:sc>\n                    -carboxypeptidases has remained unknown. We now show that one of these\n                    <jats:sc>dd<\/jats:sc>\n                    -carboxypeptidases, PBP6b, is important for cell shape maintenance in acidic growth medium, consistent with the higher activity and stability of the enzyme at low pH. Hence, the presence of multiple\n                    <jats:sc>dd<\/jats:sc>\n                    -carboxypeptidases with different enzymatic properties may allow\n                    <jats:named-content content-type=\"genus-species\">E. coli<\/jats:named-content>\n                    to maintain a normal cell shape under various growth conditions.\n                  <\/jats:p>","DOI":"10.1128\/mbio.00819-16","type":"journal-article","created":{"date-parts":[[2016,6,23]],"date-time":"2016-06-23T13:13:59Z","timestamp":1466687639000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":103,"title":["The Redundancy of Peptidoglycan Carboxypeptidases Ensures Robust Cell Shape Maintenance in Escherichia coli"],"prefix":"10.1128","volume":"7","author":[{"given":"Katharina","family":"Peters","sequence":"first","affiliation":[{"name":"Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Suresh","family":"Kannan","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of Arkansas for Medical Sciences, Little Rock, Arkansas, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vincenzo A.","family":"Rao","sequence":"additional","affiliation":[{"name":"Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacob","family":"Biboy","sequence":"additional","affiliation":[{"name":"Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniela","family":"Vollmer","sequence":"additional","affiliation":[{"name":"Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephen W.","family":"Erickson","sequence":"additional","affiliation":[{"name":"Department of Biostatistics, University of Arkansas for Medical Sciences, Little Rock, Arkansas, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard J.","family":"Lewis","sequence":"additional","affiliation":[{"name":"Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kevin D.","family":"Young","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of Arkansas for Medical Sciences, Little Rock, Arkansas, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Waldemar","family":"Vollmer","sequence":"additional","affiliation":[{"name":"Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_3_2_2","first-page":"1570","volume-title":"Escherichia coli and Salmonella: cellular and molecular biology","author":"Ingraham JL","year":"1996","unstructured":"Ingraham JL, Marr AG. 1996. Effect of temperature, pressure, pH, and osmotic stress on growth, p 1570\u20131578. In Neidhardt FC, Curtiss R, III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (ed), Escherichia coli and Salmonella: cellular and molecular biology, vol 2. ASM Press, Washington, DC."},{"key":"e_1_3_3_3_2","first-page":"167","article-title":"Structural and functional properties of porin channels in E. coli outer membranes","volume":"46","author":"Rosenbusch JP","year":"1990","unstructured":"Rosenbusch JP. 1990. Structural and functional properties of porin channels in E. coli outer membranes. Experientia 46:167\u2013173.","journal-title":"Experientia"},{"key":"e_1_3_3_4_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6976.2007.00094.x"},{"key":"e_1_3_3_5_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrmicro2677"},{"key":"e_1_3_3_6_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6976.2008.00105.x"},{"key":"e_1_3_3_7_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6976.2006.00024.x"},{"key":"e_1_3_3_8_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.2012.08103.x"},{"key":"e_1_3_3_9_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.2006.05280.x"},{"key":"e_1_3_3_10_2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.07118"},{"key":"e_1_3_3_11_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M706390200"},{"key":"e_1_3_3_12_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2010.11.037"},{"key":"e_1_3_3_13_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2010.11.038"},{"key":"e_1_3_3_14_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6976.2007.00090.x"},{"key":"e_1_3_3_15_2","doi-asserted-by":"publisher","DOI":"10.1128\/MMBR.62.1.181-203.1998"},{"key":"e_1_3_3_16_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M508646200"},{"key":"e_1_3_3_17_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M604083200"},{"key":"e_1_3_3_18_2","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2015.0031"},{"key":"e_1_3_3_19_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.1991.tb00739.x"},{"key":"e_1_3_3_20_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00203-005-0057-5"},{"key":"e_1_3_3_21_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/16.4.1617"},{"key":"e_1_3_3_22_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.182.6.1714-1721.2000"},{"key":"e_1_3_3_23_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.183.10.3055-3064.2001"},{"key":"e_1_3_3_24_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.178.24.7106-7111.1996"},{"key":"e_1_3_3_25_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1432-1033.1994.00597.x"},{"key":"e_1_3_3_26_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.179.19.6112-6121.1997"},{"key":"e_1_3_3_27_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.05764-11"},{"key":"e_1_3_3_28_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tim.2008.04.006"},{"key":"e_1_3_3_29_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.181.13.3981-3993.1999"},{"key":"e_1_3_3_30_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.185.7.2178-2186.2003"},{"key":"e_1_3_3_31_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.151.1.491-494.1982"},{"key":"e_1_3_3_32_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.2002.03131.x"},{"key":"e_1_3_3_33_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2014.02.033"},{"key":"e_1_3_3_34_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.184.13.3630-3639.2002"},{"key":"e_1_3_3_35_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.2010.07205.x"},{"key":"e_1_3_3_36_2","doi-asserted-by":"publisher","DOI":"10.1021\/ja903773f"},{"key":"e_1_3_3_37_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M004471200"},{"key":"e_1_3_3_38_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M310177200"},{"key":"e_1_3_3_39_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6968.2009.01863.x"},{"key":"e_1_3_3_40_2","doi-asserted-by":"publisher","DOI":"10.1128\/AAC.05150-14"},{"key":"e_1_3_3_41_2","doi-asserted-by":"publisher","DOI":"10.1128\/AAC.01224-13"},{"key":"e_1_3_3_42_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.178.21.6110-6115.1996"},{"key":"e_1_3_3_43_2","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.1500263"},{"key":"e_1_3_3_44_2","doi-asserted-by":"publisher","DOI":"10.1111\/1574-6968.12009"},{"key":"e_1_3_3_45_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.2012.08023.x"},{"key":"e_1_3_3_46_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2014.02.033"},{"key":"e_1_3_3_47_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6976.2007.00099.x"},{"key":"e_1_3_3_48_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.00025-08"},{"key":"e_1_3_3_49_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.00084-07"},{"key":"e_1_3_3_50_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.184.22.6093-6099.2002"},{"key":"e_1_3_3_51_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.179.17.5465-5470.1997"},{"key":"e_1_3_3_52_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0021-9258(17)30613-0"},{"key":"e_1_3_3_53_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0021-9258(19)81481-3"},{"key":"e_1_3_3_54_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.183.20.6148-6149.2001"},{"key":"e_1_3_3_55_2","doi-asserted-by":"publisher","DOI":"10.1107\/S0907444909047337"},{"key":"e_1_3_3_56_2","doi-asserted-by":"publisher","DOI":"10.1107\/S0907444913000061"},{"key":"e_1_3_3_57_2","doi-asserted-by":"publisher","DOI":"10.1107\/S0021889807021206"},{"key":"e_1_3_3_58_2","doi-asserted-by":"publisher","DOI":"10.1107\/S0907444911001314"},{"key":"e_1_3_3_59_2","doi-asserted-by":"publisher","DOI":"10.1107\/S0907444910007493"},{"key":"e_1_3_3_60_2","doi-asserted-by":"publisher","DOI":"10.1089\/108705701753364922"},{"key":"e_1_3_3_61_2","doi-asserted-by":"publisher","DOI":"10.1128\/AAC.43.5.1124"},{"key":"e_1_3_3_62_2","doi-asserted-by":"publisher","DOI":"10.1016\/0003-2697(88)90468-X"},{"key":"e_1_3_3_63_2","doi-asserted-by":"publisher","DOI":"10.1021\/bi801993x"}],"container-title":["mBio"],"original-title":[],"contributor":[{"given":"William","family":"Margolin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"reviewer"}]},{"given":"David","family":"Popham","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"reviewer"}]}],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/mBio.00819-16","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/mBio.00819-16","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,3,7]],"date-time":"2022-03-07T21:00:16Z","timestamp":1646686816000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/mBio.00819-16"}},"subtitle":[],"editor":[{"given":"Olaf","family":"Schneewind","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2016,7,6]]},"references-count":62,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2016,7,6]]}},"alternative-id":["10.1128\/mBio.00819-16"],"URL":"https:\/\/doi.org\/10.1128\/mbio.00819-16","relation":{},"ISSN":["2161-2129","2150-7511"],"issn-type":[{"value":"2161-2129","type":"print"},{"value":"2150-7511","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,7,6]]},"assertion":[{"value":"2016-05-10","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2016-05-13","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2016-06-21","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e00819-16"}}