Relationship Between the Rod Complex and Peptidoglycan Structure in Escherichia Coli

Overview

Journal Microbiologyopen

Specialty Microbiology

Date 2023 Oct 25

PMID 37877652

Authors

Risa Ago

Yuhei O Tahara

Honoka Yamaguchi

Motoya Saito

Wakana Ito

Kaito Yamasaki

Taishi Kasai

Sho Okamoto

Taiki Chikada

Taku Oshima

Issey Osaka

Makoto Miyata

Hironori Niki

Daisuke Shiomi

Affiliations

Soon will be listed here.

Abstract

Peptidoglycan for elongation in Escherichia coli is synthesized by the Rod complex, which includes RodZ. Although various mutant strains of the Rod complex have been isolated, the relationship between the activity of the Rod complex and the overall physical and chemical structures of the peptidoglycan have not been reported. We constructed a RodZ mutant, termed RMR, and analyzed the growth rate, morphology, and other characteristics of cells producing the Rod complexes containing RMR. The growth and morphology of RMR cells were abnormal, and we isolated suppressor mutants from RMR cells. Most of the suppressor mutations were found in components of the Rod complex, suggesting that these suppressor mutations increase the integrity and/or the activity of the Rod complex. We purified peptidoglycan from wild-type, RMR, and suppressor mutant cells and observed their structures in detail. We found that the peptidoglycan purified from RMR cells had many large holes and different compositions of muropeptides from those of WT cells. The Rod complex may be a determinant not only for the whole shape of peptidoglycan but also for its highly dense structure to support the mechanical strength of the cell wall.

Citing Articles

Septal wall synthesis is sufficient to change ameba-like cells into uniform oval-shaped cells in Escherichia coli L-forms.

Hayashi M, Takaoka C, Higashi K, Kurokawa K, Margolin W, Oshima T Commun Biol. 2024; 7(1):1569.

PMID: 39587276 PMC: 11589767. DOI: 10.1038/s42003-024-07279-y.

Budding and explosive membrane vesicle production by hypervesiculating strain Δ.

Ojima Y, Toda K, Sawabe T, Kumazoe Y, Tahara Y, Miyata M Front Microbiol. 2024; 15:1400434.

PMID: 38966389 PMC: 11222570. DOI: 10.3389/fmicb.2024.1400434.

Visualization of Bacillus subtilis spore structure and germination using quick-freeze deep-etch electron microscopy.

Jalil K, Tahara Y, Miyata M Microscopy (Oxf). 2024; 73(6):463-472.

PMID: 38819330 PMC: 11630275. DOI: 10.1093/jmicro/dfae023.

Comprehensive understanding of the mutant 'giant' developed via ultraviolet mutagenesis.

Lee C, Han S, Na H, Kim Z, Ahn J, Oh B Front Plant Sci. 2024; 15:1369976.

PMID: 38567133 PMC: 10985164. DOI: 10.3389/fpls.2024.1369976.

Relationship between the Rod complex and peptidoglycan structure in Escherichia coli.

Ago R, Tahara Y, Yamaguchi H, Saito M, Ito W, Yamasaki K Microbiologyopen. 2023; 12(5):e1385.

PMID: 37877652 PMC: 10561026. DOI: 10.1002/mbo3.1385.

References

Li H, Durbin R . Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25(14):1754-60. PMC: 2705234. DOI: 10.1093/bioinformatics/btp324. View

Rohs P, Bernhardt T . Growth and Division of the Peptidoglycan Matrix. Annu Rev Microbiol. 2021; 75:315-336. DOI: 10.1146/annurev-micro-020518-120056. View

Rohs P, Qiu J, Torres G, Smith M, Fivenson E, Bernhardt T . Identification of potential regulatory domains within the MreC and MreD components of the cell elongation machinery. J Bacteriol. 2021; 203(9). PMC: 8092158. DOI: 10.1128/JB.00493-20. View

Elsbroek L, Amiteye D, Schreiber S, Herrmann F . Molecular Imaging of Isolated DH5α Peptidoglycan Sacculi Identifies the Mechanism of Action of Cell Wall-Inhibiting Antibiotics. ACS Chem Biol. 2023; 18(4):848-860. DOI: 10.1021/acschembio.2c00945. View

Ikebe R, Kuwabara Y, Chikada T, Niki H, Shiomi D . The periplasmic disordered domain of RodZ promotes its self-interaction in Escherichia coli. Genes Cells. 2018; 23(4):307-317. DOI: 10.1111/gtc.12572. View

Rohs P, Buss J, Sim S, Squyres G, Srisuknimit V, Smith M . A central role for PBP2 in the activation of peptidoglycan polymerization by the bacterial cell elongation machinery. PLoS Genet. 2018; 14(10):e1007726. PMC: 6207328. DOI: 10.1371/journal.pgen.1007726. View

Garner E, Bernard R, Wang W, Zhuang X, Rudner D, Mitchison T . Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science. 2011; 333(6039):222-5. PMC: 3235694. DOI: 10.1126/science.1203285. View

Turner R, Mesnage S, Hobbs J, Foster S . Molecular imaging of glycan chains couples cell-wall polysaccharide architecture to bacterial cell morphology. Nat Commun. 2018; 9(1):1263. PMC: 5871751. DOI: 10.1038/s41467-018-03551-y. View

Guzman L, Weiss D, Beckwith J . Domain-swapping analysis of FtsI, FtsL, and FtsQ, bitopic membrane proteins essential for cell division in Escherichia coli. J Bacteriol. 1997; 179(16):5094-103. PMC: 179367. DOI: 10.1128/jb.179.16.5094-5103.1997. View

10.

Turner R, Hurd A, Cadby A, Hobbs J, Foster S . Cell wall elongation mode in Gram-negative bacteria is determined by peptidoglycan architecture. Nat Commun. 2013; 4:1496. PMC: 3586723. DOI: 10.1038/ncomms2503. View

11.

Kawazura T, Matsumoto K, Kojima K, Kato F, Kanai T, Niki H . Exclusion of assembled MreB by anionic phospholipids at cell poles confers cell polarity for bidirectional growth. Mol Microbiol. 2017; 104(3):472-486. DOI: 10.1111/mmi.13639. View

12.

van Teeffelen S, Wang S, Furchtgott L, Huang K, Wingreen N, Shaevitz J . The bacterial actin MreB rotates, and rotation depends on cell-wall assembly. Proc Natl Acad Sci U S A. 2011; 108(38):15822-7. PMC: 3179079. DOI: 10.1073/pnas.1108999108. View

13.

Bendezu F, de Boer P . Conditional lethality, division defects, membrane involution, and endocytosis in mre and mrd shape mutants of Escherichia coli. J Bacteriol. 2007; 190(5):1792-811. PMC: 2258658. DOI: 10.1128/JB.01322-07. View

14.

Cho H, Uehara T, Bernhardt T . Beta-lactam antibiotics induce a lethal malfunctioning of the bacterial cell wall synthesis machinery. Cell. 2014; 159(6):1300-11. PMC: 4258230. DOI: 10.1016/j.cell.2014.11.017. View

15.

Salamaga B, Kong L, Pasquina-Lemonche L, Lafage L, von Und Zur Muhlen M, Gibson J . Demonstration of the role of cell wall homeostasis in growth and the action of bactericidal antibiotics. Proc Natl Acad Sci U S A. 2021; 118(44). PMC: 8612353. DOI: 10.1073/pnas.2106022118. View

16.

Dominguez-Escobar J, Chastanet A, Crevenna A, Fromion V, Wedlich-Soldner R, Carballido-Lopez R . Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science. 2011; 333(6039):225-8. DOI: 10.1126/science.1203466. View

17.

Ouzounov N, Nguyen J, Bratton B, Jacobowitz D, Gitai Z, Shaevitz J . MreB Orientation Correlates with Cell Diameter in Escherichia coli. Biophys J. 2016; 111(5):1035-43. PMC: 5018124. DOI: 10.1016/j.bpj.2016.07.017. View

18.

Nagasaki H, Mochizuki T, Kodama Y, Saruhashi S, Morizaki S, Sugawara H . DDBJ read annotation pipeline: a cloud computing-based pipeline for high-throughput analysis of next-generation sequencing data. DNA Res. 2013; 20(4):383-90. PMC: 3738164. DOI: 10.1093/dnares/dst017. View

19.

de Pedro M, Quintela J, Holtje J, Schwarz H . Murein segregation in Escherichia coli. J Bacteriol. 1997; 179(9):2823-34. PMC: 179041. DOI: 10.1128/jb.179.9.2823-2834.1997. View

20.

Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M . Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol. 2006; 2:2006.0008. PMC: 1681482. DOI: 10.1038/msb4100050. View