A previously uncharacterized divisome-associated lipoprotein, DalA, is needed for normal cell division in Rhodobacterales

Alberge, François; Lakey, Bryan D.; Schaub, Ryan E.; Dohnalkova, Alice C.; Lemmer, Kimberley C.; Dillard, Joseph P.; Noguera, Daniel R.; Donohue, Timothy J.; Søgaard-Andersen, ed., Lotte

doi:10.1128/mbio.01203-23

A previously uncharacterized divisome-associated lipoprotein, DalA, is needed for normal cell division in Rhodobacterales

Journal Article · Fri Jun 30 00:00:00 EDT 2023 · mBio (Online)

DOI:https://doi.org/10.1128/mbio.01203-23· OSTI ID:1987925

^[1]; Lakey, Bryan D. ^[2]; Schaub, Ryan E. ^[3]; Dohnalkova, Alice C. ^[4]; Lemmer, Kimberley C. ^[5]; ^[3]; Noguera, Daniel R. ^[6]; ^[7]; Søgaard-Andersen, ed., Lotte

1 Wisconsin Energy Institute, Great Lakes Bioenergy Research Center, University of Wisconsin-Madison , Madison, Wisconsin, USA
1 Wisconsin Energy Institute, Great Lakes Bioenergy Research Center, University of Wisconsin-Madison , Madison, Wisconsin, USA, Laboratory of Genetics, University of Wisconsin-Madison , Madison, Wisconsin, USA
Department of Medical Microbiology and Immunology, University of Wisconsin-Madison , Madison, Wisconsin, USA
Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory , Richland, Washington, USA
National Renewable Energy Laboratory , Golden, Colorado, USA
1 Wisconsin Energy Institute, Great Lakes Bioenergy Research Center, University of Wisconsin-Madison , Madison, Wisconsin, USA, Department of Civil and Environmental Engineering, University of Wisconsin-Madison , Madison, Wisconsin, USA
1 Wisconsin Energy Institute, Great Lakes Bioenergy Research Center, University of Wisconsin-Madison , Madison, Wisconsin, USA, Department of Bacteriology, University of Wisconsin-Madison , Madison, Wisconsin, USA

ABSTRACT

The bacterial cell envelope is a key subcellular compartment with important roles in antibiotic resistance, nutrient acquisition, and cell morphology. We seek to gain a better understanding of proteins that contribute to the function of the cell envelope in Alphaproteobacteria . Using Rhodobacter sphaeroides , we show that a previously uncharacterized protein, RSP_1200, is an outer membrane (OM) lipoprotein that non-covalently binds peptidoglycan (PG). Using a fluorescently tagged version of this protein, we find that RSP_1200 undergoes a dynamic repositioning during the cell cycle and is enriched at the septum during cell division. We show that the position of RSP_1200 mirrors the location of FtsZ rings, leading us to propose that RSP_1200 is a newly identified component of the R. sphaeroides ’ divisome. Additional support for this hypothesis includes the co-precipitation of RSP_1200 with FtsZ, the Pal protein, and several predicted PG L,D-transpeptidases. We also find that a ∆ RSP_1200 mutation leads to defects in cell division, sensitivity to PG-active antibiotics, and results in the formation of OM protrusions at the septum during cell division. Based on these results, we propose to name RSP_1200 DalA (for division-associated lipoprotein A) and postulate that DalA serves as a scaffold to position or modulate the activity of PG transpeptidases that are needed to form envelope invaginations during cell division. We find that DalA homologs are present in members of the Rhodobacterales order within Alphaproteobacteria . Therefore, we propose that further analysis of this and related proteins will increase our understanding of the macromolecular machinery and proteins that participate in cell division in Gram-negative bacteria.

IMPORTANCE

Multi-protein complexes of the bacterial cell envelope orchestrate key processes like growth, division, biofilm formation, antimicrobial resistance, and production of valuable compounds. The subunits of these protein complexes are well studied in some bacteria, and differences in their composition and function are linked to variations in cell envelope composition, shape, and proliferation. However, some envelope protein complex subunits have no known homologs across the bacterial phylogeny. We find that Rhodobacter sphaeroides RSP_1200 is a newly identified lipoprotein (DalA) and that loss of this protein causes defects in cell division and changes the sensitivity to compounds, affecting cell envelope synthesis and function. We find that DalA forms a complex with proteins needed for cell division, binds the cell envelope polymer peptidoglycan, and colocalizes with enzymes involved in the assembly of this macromolecule. The analysis of DalA provides new information on the cell division machinery in this and possibly other Alphaproteobacteria.

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Research Organization:: Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); National Renewable Energy Laboratory (NREL), Golden, CO (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Sponsoring Organization:: National Institute of Health (NIH); National Science Foundation (NSF); USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-76RL01830; AC36-08GO28308; SC0018409

OSTI ID:: 1987925

Alternate ID(s):: OSTI ID: 1992301

Report Number(s):: NREL/JA--6A20-86957; e01203-23

Journal Information:: mBio (Online), Journal Name: mBio (Online); ISSN 2150-7511

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (95)

In Situ Probing of Newly Synthesized Peptidoglycan in Live Bacteria with Fluorescent D -Amino Acids Kuru, Erkin; Hughes, H. Velocity; Brown, Pamela J. Angewandte Chemie International Edition, Vol. 51, Issue 50 https://doi.org/10.1002/anie.201206749	journal	October 2012
Agrobacterium Biology: From Basic Science to Biotechnology Gelvin, Stanton B. Current Topics in Microbiology and Immunology https://doi.org/10.1007/978-3-030-03257-9	book	January 2018
Cell Cycle Regulation and Development in Alphaproteobacteria Biondi, Emanuele https://doi.org/10.1007/978-3-030-90621-4	book	January 2022
ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
The Prokaryotes: Alphaproteobacteria and Betaproteobacteria Rosenberg, Eugene; DeLong, Edward F.; Lory, Stephen https://doi.org/10.1007/978-3-642-30197-1	book	January 2014
Electron Partitioning During Light- and Nutrient-Powered Hydrogen Production by Rhodobacter sphaeroides Yilmaz, Luftu Safak; Kontur, Wayne S.; Sanders, Alison P. BioEnergy Research, Vol. 3, Issue 1 https://doi.org/10.1007/s12155-009-9072-8	journal	January 2010
A single amino acid determinant of the membrane localization of lipoproteins in E. coli Yamaguchi, Kyoji; Yu, Fujio; Inouye, Masayori Cell, Vol. 53, Issue 3 https://doi.org/10.1016/0092-8674(88)90162-6	journal	May 1988
Braun’s Lipoprotein Facilitates OmpA Interaction with the Escherichia coli Cell Wall Samsudin, Firdaus; Boags, Alister; Piggot, Thomas J. Biophysical Journal, Vol. 113, Issue 7 https://doi.org/10.1016/j.bpj.2017.08.011	journal	October 2017
Lipoprotein Cofactors Located in the Outer Membrane Activate Bacterial Cell Wall Polymerases Paradis-Bleau, Catherine; Markovski, Monica; Uehara, Tsuyoshi Cell, Vol. 143, Issue 7 https://doi.org/10.1016/j.cell.2010.11.037	journal	December 2010
Beta-Lactam Antibiotics Induce a Lethal Malfunctioning of the Bacterial Cell Wall Synthesis Machinery Cho, Hongbaek; Uehara, Tsuyoshi; Bernhardt, Thomas G. Cell, Vol. 159, Issue 6 https://doi.org/10.1016/j.cell.2014.11.017	journal	December 2014
Tol Energy-Driven Localization of Pal and Anchoring to the Peptidoglycan Promote Outer-Membrane Constriction Petiti, Mélissa; Serrano, Bastien; Faure, Laura Journal of Molecular Biology, Vol. 431, Issue 17 https://doi.org/10.1016/j.jmb.2019.05.039	journal	August 2019
Timing of TolA and TolQ Recruitment at the Septum Depends on the Functionality of the Tol-Pal System Baccelli, Pauline; Rachedi, Raphaël; Serrano, Bastien Journal of Molecular Biology, Vol. 434, Issue 7 https://doi.org/10.1016/j.jmb.2022.167519	journal	April 2022
Modes of cell wall growth differentiation in rod-shaped bacteria Cava, Felipe; Kuru, Erkin; Brun, Yves V. Current Opinion in Microbiology, Vol. 16, Issue 6 https://doi.org/10.1016/j.mib.2013.09.004	journal	December 2013
Robust peptidoglycan growth by dynamic and variable multi-protein complexes Pazos, Manuel; Peters, Katharina; Vollmer, Waldemar Current Opinion in Microbiology, Vol. 36 https://doi.org/10.1016/j.mib.2017.01.006	journal	April 2017
Recent progress in our understanding of peptidoglycan assembly in Firmicutes Ducret, Adrien; Grangeasse, Christophe Current Opinion in Microbiology, Vol. 60 https://doi.org/10.1016/j.mib.2021.01.011	journal	April 2021
Lipoproteins in Gram-negative bacteria: new insights into their biogenesis, subcellular targeting and functional roles El Rayes, Jessica; Rodríguez-Alonso, Raquel; Collet, Jean-François Current Opinion in Microbiology, Vol. 61 https://doi.org/10.1016/j.mib.2021.02.003	journal	June 2021
Polarity and the diversity of growth mechanisms in bacteria Brown, Pamela J. B.; Kysela, David T.; Brun, Yves V. Seminars in Cell & Developmental Biology, Vol. 22, Issue 8 https://doi.org/10.1016/j.semcdb.2011.06.006	journal	October 2011
The essential features and modes of bacterial polar growth Cameron, Todd A.; Zupan, John R.; Zambryski, Patricia C. Trends in Microbiology, Vol. 23, Issue 6 https://doi.org/10.1016/j.tim.2015.01.003	journal	June 2015
A Statistical Model for Identifying Proteins by Tandem Mass Spectrometry Nesvizhskii, Alexey I.; Keller, Andrew; Kolker, Eugene Analytical Chemistry, Vol. 75, Issue 17 https://doi.org/10.1021/ac0341261	journal	September 2003
Mechanisms of Incorporation for D -Amino Acid Probes That Target Peptidoglycan Biosynthesis Kuru, Erkin; Radkov, Atanas; Meng, Xin ACS Chemical Biology, Vol. 14, Issue 12 https://doi.org/10.1021/acschembio.9b00664	journal	November 2019
Chemometric Analysis of Bacterial Peptidoglycan Reveals Atypical Modifications That Empower the Cell Wall against Predatory Enzymes and Fly Innate Immunity Espaillat, Akbar; Forsmo, Oskar; El Biari, Khouzaima Journal of the American Chemical Society, Vol. 138, Issue 29 https://doi.org/10.1021/jacs.6b04430	journal	July 2016
Daughter cell separation is controlled by cytokinetic ring-activated cell wall hydrolysis Uehara, Tsuyoshi; Parzych, Katherine R.; Dinh, Thuy The EMBO Journal, Vol. 29, Issue 8 https://doi.org/10.1038/emboj.2010.36	journal	March 2010
A Broad Host Range Mobilization System for In Vivo Genetic Engineering Transposon Mutagenesis in Gram Negative Bacteria Simon, R.; Priefer, U.; Pühler, A. Bio/Technology, Vol. 1, Issue 9, p. 784-791 https://doi.org/10.1038/nbt1183-784	journal	November 1983
Fiji: an open-source platform for biological-image analysis Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2019	journal	June 2012
ClearVolume: open-source live 3D visualization for light-sheet microscopy Royer, Loic A.; Weigert, Martin; Günther, Ulrik Nature Methods, Vol. 12, Issue 6 https://doi.org/10.1038/nmeth.3372	journal	May 2015
MicrobeJ, a tool for high throughput bacterial cell detection and quantitative analysis Ducret, Adrien; Quardokus, Ellen M.; Brun, Yves V. Nature Microbiology, Vol. 1, Issue 7 https://doi.org/10.1038/nmicrobiol.2016.77	journal	June 2016
From the regulation of peptidoglycan synthesis to bacterial growth and morphology Typas, Athanasios; Banzhaf, Manuel; Gross, Carol A. Nature Reviews Microbiology, Vol. 10, Issue 2 https://doi.org/10.1038/nrmicro2677	journal	December 2011
Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions Schwechheimer, Carmen; Kuehn, Meta J. Nature Reviews Microbiology, Vol. 13, Issue 10 https://doi.org/10.1038/nrmicro3525	journal	September 2015
Z-ring membrane anchors associate with cell wall synthases to initiate bacterial cell division Pazos, Manuel; Peters, Katharina; Casanova, Mercedes Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07559-2	journal	November 2018
The lipoprotein Pal stabilises the bacterial outer membrane during constriction by a mobilisation-and-capture mechanism Szczepaniak, Joanna; Holmes, Peter; Rajasekar, Karthik Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15083-5	journal	March 2020
Lipoprotein Lpp regulates the mechanical properties of the E. coli cell envelope Mathelié-Guinlet, Marion; Asmar, Abir T.; Collet, Jean-François Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15489-1	journal	April 2020
β-Barrel proteins tether the outer membrane in many Gram-negative bacteria Sandoz, Kelsi M.; Moore, Roger A.; Beare, Paul A. Nature Microbiology, Vol. 6, Issue 1 https://doi.org/10.1038/s41564-020-00798-4	journal	November 2020
β-Barrels covalently link peptidoglycan and the outer membrane in the α-proteobacterium Brucella abortus Godessart, Pierre; Lannoy, Adélie; Dieu, Marc Nature Microbiology, Vol. 6, Issue 1 https://doi.org/10.1038/s41564-020-00799-3	journal	November 2020
Regulation of peptidoglycan synthesis and remodelling Egan, Alexander J. F.; Errington, Jeff; Vollmer, Waldemar Nature Reviews Microbiology, Vol. 18, Issue 8 https://doi.org/10.1038/s41579-020-0366-3	journal	May 2020
The bacterial actin MreB rotates, and rotation depends on cell-wall assembly van Teeffelen, Sven; Wang, Siyuan; Furchtgott, Leon Proceedings of the National Academy of Sciences, Vol. 108, Issue 38 https://doi.org/10.1073/pnas.1108999108	journal	September 2011
Polar growth in the Alphaproteobacterial order Rhizobiales Brown, P. J. B.; de Pedro, M. A.; Kysela, D. T. Proceedings of the National Academy of Sciences, Vol. 109, Issue 5 https://doi.org/10.1073/pnas.1114476109	journal	January 2012
Rod-like bacterial shape is maintained by feedback between cell curvature and cytoskeletal localization Ursell, Tristan S.; Nguyen, Jeffrey; Monds, Russell D. Proceedings of the National Academy of Sciences, Vol. 111, Issue 11 https://doi.org/10.1073/pnas.1317174111	journal	February 2014
Outer-membrane lipoprotein LpoB spans the periplasm to stimulate the peptidoglycan synthase PBP1B Egan, A. J. F.; Jean, N. L.; Koumoutsi, A. Proceedings of the National Academy of Sciences, Vol. 111, Issue 22 https://doi.org/10.1073/pnas.1400376111	journal	May 2014
Conserved mechanism of cell-wall synthase regulation revealed by the identification of a new PBP activator in Pseudomonas aeruginosa Greene, Neil G.; Fumeaux, Coralie; Bernhardt, Thomas G. Proceedings of the National Academy of Sciences, Vol. 115, Issue 12 https://doi.org/10.1073/pnas.1717925115	journal	March 2018
Copper inhibits peptidoglycan LD-transpeptidases suppressing β-lactam resistance due to bypass of penicillin-binding proteins Peters, Katharina; Pazos, Manuel; Edoo, Zainab Proceedings of the National Academy of Sciences, Vol. 115, Issue 42 https://doi.org/10.1073/pnas.1809285115	journal	October 2018
The Tol-Pal system is required for peptidoglycan-cleaving enzymes to complete bacterial cell division Yakhnina, Anastasiya A.; Bernhardt, Thomas G. Proceedings of the National Academy of Sciences, Vol. 117, Issue 12 https://doi.org/10.1073/pnas.1919267117	journal	March 2020
The LpoA activator is required to stimulate the peptidoglycan polymerase activity of its cognate cell wall synthase PBP1a Sardis, Marios F.; Bohrhunter, Jessica L.; Greene, Neil G. Proceedings of the National Academy of Sciences, Vol. 118, Issue 35 https://doi.org/10.1073/pnas.2108894118	journal	August 2021
SuperPlots: Communicating reproducibility and variability in cell biology Lord, Samuel J.; Velle, Katrina B.; Mullins, R. Dyche Journal of Cell Biology, Vol. 219, Issue 6 https://doi.org/10.1083/jcb.202001064	journal	April 2020
Lpp, the Braun lipoprotein, turns 50—major achievements and remaining issues Asmar, Abir T.; Collet, Jean-François FEMS Microbiology Letters, Vol. 365, Issue 18 https://doi.org/10.1093/femsle/fny199	journal	August 2018
The multifarious roles of Tol-Pal in Gram-negative bacteria Szczepaniak, Joanna; Press, Cara; Kleanthous, Colin FEMS Microbiology Reviews, Vol. 44, Issue 4 https://doi.org/10.1093/femsre/fuaa018	journal	May 2020
A Requirement for Sodium in the Growth of Rhodopseudomonas spheroides Sistrom, W. R. Journal of General Microbiology, Vol. 22, Issue 3 https://doi.org/10.1099/00221287-22-3-778	journal	June 1960
A pyramid approach to subpixel registration based on intensity Thevenaz, P.; Ruttimann, U. E.; Unser, M. IEEE Transactions on Image Processing, Vol. 7, Issue 1 https://doi.org/10.1109/83.650848	journal	January 1998
Lipoproteins in bacteria: structures and biosynthetic pathways Nakayama, Hiroshi; Kurokawa, Kenji; Lee, Bok Luel FEBS Journal, Vol. 279, Issue 23 https://doi.org/10.1111/febs.12041	journal	November 2012
LD‐transpeptidases: the great unknown among the peptidoglycan cross‐linkers Aliashkevich, Alena; Cava, Felipe The FEBS Journal https://doi.org/10.1111/febs.16066	journal	June 2021
Proposal for a peptidoglycan-associating alpha-helical motif in the C-terminal regions of some bacterial cell-surface proteins Koebnik, Ralf Molecular Microbiology, Vol. 16, Issue 6 https://doi.org/10.1111/j.1365-2958.1995.tb02348.x	journal	June 1995
Maturation of the Escherichia coli divisome occurs in two steps : Maturation of the divisome Aarsman, Mirjam E. G.; Piette, André; Fraipont, Claudine Molecular Microbiology, Vol. 55, Issue 6 https://doi.org/10.1111/j.1365-2958.2005.04502.x	journal	January 2005
The trans ‐envelope Tol–Pal complex is part of the cell division machinery and required for proper outer‐membrane invagination during cell constriction in E. coli Gerding, Matthew A.; Ogata, Yasuyuki; Pecora, Nicole D. Molecular Microbiology, Vol. 63, Issue 4 https://doi.org/10.1111/j.1365-2958.2006.05571.x	journal	December 2006
The tubulin homologue FtsZ contributes to cell elongation by guiding cell wall precursor synthesis in Caulobacter crescentus Aaron, Michelle; Charbon, Godefroid; Lam, Hubert Molecular Microbiology, Vol. 64, Issue 4 https://doi.org/10.1111/j.1365-2958.2007.05720.x	journal	May 2007
Assembly of the MreB-associated cytoskeletal ring of Escherichia coli: E. coli MreB-associated cytoskeletal Vats, Purva; Shih, Yu-Ling; Rothfield, Lawrence Molecular Microbiology, Vol. 72, Issue 1 https://doi.org/10.1111/j.1365-2958.2009.06632.x	journal	March 2009
Positioning cell wall synthetic complexes by the bacterial morphogenetic proteins MreB and MreD: Control of cell shape in bacteria White, Courtney L.; Kitich, Aleksandar; Gober, James W. Molecular Microbiology, Vol. 76, Issue 3 https://doi.org/10.1111/j.1365-2958.2010.07108.x	journal	March 2010
The free and bound forms of Lpp occupy distinct subcellular locations in Escherichia coli: Free-form Lpp is surface-exposed in E. coli Cowles, Charles E.; Li, Yongfeng; Semmelhack, Martin F. Molecular Microbiology, Vol. 79, Issue 5 https://doi.org/10.1111/j.1365-2958.2011.07539.x	journal	January 2011
The Covalent Murein-Lipoprotin Structure of the Escherichia coli Cell Wall. The Attachment Site of the Lipoprotein on the Murein Braun, Volkmar; Sieglin, Uta European Journal of Biochemistry, Vol. 13, Issue 2 https://doi.org/10.1111/j.1432-1033.1970.tb00936.x	journal	April 1970
Colocalization and interaction between elongasome and divisome during a preparative cell division phase inEscherichia coli van der Ploeg, René; Verheul, Jolanda; Vischer, Norbert O. E. Molecular Microbiology, Vol. 87, Issue 5 https://doi.org/10.1111/mmi.12150	journal	February 2013
Positioning of chemosensory proteins and FtsZ through theRhodobacter sphaeroidescell cycle Chiu, Sheng-Wen; Roberts, Mark A. J.; Leake, Mark C. Molecular Microbiology https://doi.org/10.1111/mmi.12366	journal	September 2013
Dynamics of the peptidoglycan biosynthetic machinery in the stalked budding bacteriumHyphomonas neptunium Cserti, Emöke; Rosskopf, Sabine; Chang, Yi-Wei Molecular Microbiology, Vol. 103, Issue 5 https://doi.org/10.1111/mmi.13593	journal	January 2017
Assembly and activation of the Escherichia coli divisome: The E. coli divisome Du, Shishen; Lutkenhaus, Joe Molecular Microbiology, Vol. 105, Issue 2 https://doi.org/10.1111/mmi.13696	journal	May 2017
Treadmilling by FtsZ filaments drives peptidoglycan synthesis and bacterial cell division Bisson-Filho, Alexandre W.; Hsu, Yen-Pang; Squyres, Georgia R. Science, Vol. 355, Issue 6326 https://doi.org/10.1126/science.aak9973	journal	February 2017
GTPase activity–coupled treadmilling of the bacterial tubulin FtsZ organizes septal cell wall synthesis Yang, Xinxing; Lyu, Zhixin; Miguel, Amanda Science, Vol. 355, Issue 6326 https://doi.org/10.1126/science.aak9995	journal	February 2017
Profiling of β-Lactam Selectivity for Penicillin-Binding Proteins in Escherichia coli Strain DC2 Kocaoglu, Ozden; Carlson, Erin E. Antimicrobial Agents and Chemotherapy, Vol. 59, Issue 5 https://doi.org/10.1128/AAC.04552-14	journal	May 2015
In vivo interaction of beta-lactam antibiotics with the penicillin-binding proteins of Streptococcus pneumoniae Williamson, R.; Hakenbeck, R.; Tomasz, A. Antimicrobial Agents and Chemotherapy, Vol. 18, Issue 4 https://doi.org/10.1128/AAC.18.4.629	journal	October 1980
Identification of the L,D-Transpeptidases for Peptidoglycan Cross-Linking in Escherichia coli Magnet, S.; Dubost, L.; Marie, A. Journal of Bacteriology, Vol. 190, Issue 13 https://doi.org/10.1128/JB.00025-08	journal	May 2008
Identification of the l,d-Transpeptidases Responsible for Attachment of the Braun Lipoprotein to Escherichia coli Peptidoglycan Magnet, Sophie; Bellais, Samuel; Dubost, Lionel Journal of Bacteriology, Vol. 189, Issue 10 https://doi.org/10.1128/JB.00084-07	journal	March 2007
The Caulobacter Tol-Pal Complex Is Essential for Outer Membrane Integrity and the Positioning of a Polar Localization Factor Yeh, Yi-Chun; Comolli, Luis R.; Downing, Kenneth H. Journal of Bacteriology, Vol. 192, Issue 19 https://doi.org/10.1128/JB.00607-10	journal	October 2010
FtsA Regulates Z-Ring Morphology and Cell Wall Metabolism in an FtsZ C-Terminal Linker-Dependent Manner in Caulobacter crescentus Barrows, Jordan M.; Sundararajan, Kousik; Bhargava, Anant Journal of Bacteriology, Vol. 202, Issue 7 https://doi.org/10.1128/JB.00693-19	journal	March 2020
In Vitro Characterization of Peptidoglycan-Associated Lipoprotein (PAL)–Peptidoglycan and PAL–TolB Interactions Bouveret, Emmanuelle; Bénédetti, Hélène; Rigal, Alain Journal of Bacteriology, Vol. 181, Issue 20 https://doi.org/10.1128/JB.181.20.6306-6311.1999	journal	October 1999
Pal Lipoprotein of Escherichia coli Plays a Major Role in Outer Membrane Integrity Cascales, Eric; Bernadac, Alain; Gavioli, Marthe Journal of Bacteriology, Vol. 184, Issue 3 https://doi.org/10.1128/JB.184.3.754-759.2002	journal	February 2002
Localization of MreB in Rhodobacter sphaeroides under Conditions Causing Changes in Cell Shape and Membrane Structure Slovak, Peter M.; Wadhams, George H.; Armitage, Judith P. Journal of Bacteriology, Vol. 187, Issue 1 https://doi.org/10.1128/JB.187.1.54-64.2005	journal	January 2005
PBP1A Directly Interacts with the Divisome Complex to Promote Septal Peptidoglycan Synthesis in Acinetobacter baumannii Kang, Katie N.; Boll, Joseph M. Journal of Bacteriology, Vol. 204, Issue 12 https://doi.org/10.1128/jb.00239-22	journal	December 2022
Tol-Pal System and Rgs Proteins Interact to Promote Unipolar Growth and Cell Division in Sinorhizobium meliloti Krol, Elizaveta; Yau, Hamish C. L.; Lechner, Marcus mBio, Vol. 11, Issue 3 https://doi.org/10.1128/mBio.00306-20	journal	June 2020
Mutations That Alter the Bacterial Cell Envelope Increase Lipid Production Lemmer, Kimberly C.; Zhang, Weiping; Langer, Samantha J. mBio, Vol. 8, Issue 3 https://doi.org/10.1128/mBio.00513-17	journal	May 2017
The NtrYX Two-Component System Regulates the Bacterial Cell Envelope Lemmer, Kimberly C.; Alberge, François; Myers, Kevin S. mBio, Vol. 11, Issue 3 https://doi.org/10.1128/mBio.00957-20	journal	May 2020
Peptidoglycan Synthesis Machinery in Agrobacterium tumefaciens During Unipolar Growth and Cell Division Cameron, Todd A.; Anderson-Furgeson, James; Zupan, John R. mBio, Vol. 5, Issue 3 https://doi.org/10.1128/mBio.01219-14	journal	May 2014
Regulation of the Peptidoglycan Polymerase Activity of PBP1b by Antagonist Actions of the Core Divisome Proteins FtsBLQ and FtsN Boes, Adrien; Olatunji, Samir; Breukink, Eefjan mBio, Vol. 10, Issue 1 https://doi.org/10.1128/mBio.01912-18	journal	January 2019
In Vivo Imaging of the Segregation of the 2 Chromosomes and the Cell Division Proteins of Rhodobacter sphaeroides Reveals an Unexpected Role for MipZ Dubarry, Nelly; Willis, Clare R.; Ball, Graeme mBio, Vol. 10, Issue 1 https://doi.org/10.1128/mBio.02515-18	journal	February 2019
Peptidoglycan Remodeling Enables Escherichia coli To Survive Severe Outer Membrane Assembly Defect Morè, Niccolò; Martorana, Alessandra M.; Biboy, Jacob mBio, Vol. 10, Issue 1 https://doi.org/10.1128/mBio.02729-18	journal	February 2019
The role of CenKR in the coordination of Rhodobacter sphaeroides cell elongation and division Lakey, Bryan D.; Alberge, François; Parrell, Daniel mBio https://doi.org/10.1128/mbio.00631-23	journal	June 2023
Growth and Division of the Peptidoglycan Matrix Rohs, Patricia D. A.; Bernhardt, Thomas G. Annual Review of Microbiology, Vol. 75, Issue 1 https://doi.org/10.1146/annurev-micro-020518-120056	journal	October 2021
Bacterial cell division at a glance Mahone, Christopher R.; Goley, Erin D. Journal of Cell Science, Vol. 133, Issue 7 https://doi.org/10.1242/jcs.237057	journal	April 2020
Communication across the bacterial cell envelope depends on the size of the periplasm Asmar, Abir T.; Ferreira, Josie L.; Cohen, Eli J. PLOS Biology, Vol. 15, Issue 12 https://doi.org/10.1371/journal.pbio.2004303	journal	December 2017
NlpD links cell wall remodeling and outer membrane invagination during cytokinesis in Escherichia coli Tsang, Mary-Jane; Yakhnina, Anastasiya A.; Bernhardt, Thomas G. PLOS Genetics, Vol. 13, Issue 7 https://doi.org/10.1371/journal.pgen.1006888	journal	July 2017
The mecillinam resistome reveals a role for peptidoglycan endopeptidases in stimulating cell wall synthesis in Escherichia coli Lai, Ghee Chuan; Cho, Hongbaek; Bernhardt, Thomas G. PLOS Genetics, Vol. 13, Issue 7 https://doi.org/10.1371/journal.pgen.1006934	journal	July 2017
The essential Rhodobacter sphaeroides CenKR two-component system regulates cell division and envelope biosynthesis Lakey, Bryan D.; Myers, Kevin S.; Alberge, François PLOS Genetics, Vol. 18, Issue 6 https://doi.org/10.1371/journal.pgen.1010270	journal	June 2022
Outer membrane lipoprotein NlpI scaffolds peptidoglycan hydrolases within multi‐enzyme complexes in Escherichia coli Banzhaf, Manuel; Yau, Hamish CL; Verheul, Jolanda The EMBO Journal, Vol. 39, Issue 5 https://doi.org/10.15252/embj.2019102246	journal	February 2020
Digestion of Peptidoglycan and Analysis of Soluble Fragments Schaub, Ryan; Dillard, Joseph BIO-PROTOCOL, Vol. 7, Issue 15 https://doi.org/10.21769/BioProtoc.2438	journal	January 2017
Molecular mechanisms for the evolution of bacterial morphologies and growth modes Randich, Amelia M.; Brun, Yves V. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00580	journal	June 2015
The Fluorescent D-Amino Acid NADA as a Tool to Study the Conditional Activity of Transpeptidases in Escherichia coli Montón Silva, Alejandro; Otten, Christian; Biboy, Jacob Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02101	journal	September 2018
Elongation at Midcell in Preparation of Cell Division Requires FtsZ, but Not MreB nor PBP2 in Caulobacter crescentus van Teeseling, Muriel C. F. Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.732031	journal	August 2021
The Tol-Pal System Plays an Important Role in Maintaining Cell Integrity During Elongation in Escherichia coli Park, Sohee; Cho, Hongbaek Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.891926	journal	May 2022
Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division Gray, Andrew N.; Egan, Alexander JF; van't Veer, Inge L. eLife, Vol. 4 https://doi.org/10.7554/eLife.07118	journal	May 2015
Adaptation of the periplasm to maintain spatial constraints essential for cell envelope processes and cell viability Mandela, Eric; Stubenrauch, Christopher J.; Ryoo, David eLife, Vol. 11 https://doi.org/10.7554/eLife.73516	journal	January 2022

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Journal Article · Tue Jun 06 20:00:00 EDT 2023 · mBio (Online) · OSTI ID:1984122

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