Cell shape dynamics during the staphylococcal cell cycle

Monteiro, João M.; Fernandes, Pedro B.; Vaz, Filipa; Pereira, Andreia; Tavares, Andreia C.; Ferreira, Maria Teresa; Pereira, Pedro M.; Veiga, Helena; Kuru, Erkin; VanNieuwenhze, Michael S.; Brun, Yves V.; Filipe, Sérgio R.; Pinho, Mariana G.

doi:10.1038/ncomms9055

Cited by 209 publications

(275 citation statements)

References 48 publications

(88 reference statements)

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“…Spherical bacteria, such as Staphylococcus aureus, pose a different challenge for 3D biofilm development. Despite their isotropic shape, cocci divide sequentially in orthogonal planes (35). It remains to be discovered how such directional division drives 3D growth for cocci biofilms, especially in cases of cocci, such as S. aureus, that possess low levels of extracellular polysaccharide.…”

Section: Resultsmentioning

confidence: 99%

Vibrio cholerae biofilm growth program and architecture revealed by single-cell live imaging

Yan

Sharo

Stone

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

159

209

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Biofilms are surface-associated bacterial communities that are crucial in nature and during infection. Despite extensive work to identify biofilm components and to discover how they are regulated, little is known about biofilm structure at the level of individual cells. Here, we use state-of-the-art microscopy techniques to enable live singlecell resolution imaging of a Vibrio cholerae biofilm as it develops from one single founder cell to a mature biofilm of 10,000 cells, and to discover the forces underpinning the architectural evolution. Mutagenesis, matrix labeling, and simulations demonstrate that surface adhesion-mediated compression causes V. cholerae biofilms to transition from a 2D branched morphology to a dense, ordered 3D cluster. We discover that directional proliferation of rod-shaped bacteria plays a dominant role in shaping the biofilm architecture in V. cholerae biofilms, and this growth pattern is controlled by a single gene, rbmA. Competition analyses reveal that the dense growth mode has the advantage of providing the biofilm with superior mechanical properties. Our single-cell technology can broadly link genes to biofilm fine structure and provides a route to assessing cell-to-cell heterogeneity in response to external stimuli. biofilm | single cell | self-organization | community | biomechanics

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Section: Resultsmentioning

confidence: 99%

Vibrio cholerae biofilm growth program and architecture revealed by single-cell live imaging

Yan

Sharo

Stone

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

159

209

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“…To address this question, we determined the ability of the different FtsK domains to properly localize to the septum in the background of 8325-4DftsK strain, using sfGFP fusions (that we showed not to be cleaved, Fig. 5C) expressed from the pCNX plasmid (Monteiro et al, 2015).…”

Section: S Aureus Spoiiie Assembles In Foci At the Centre Of Closingmentioning

confidence: 99%

Staphylococcus aureus requires at least one FtsK/SpoIIIE protein for correct chromosome segregation

Veiga

Pinho

2016

Molecular Microbiology

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Summary Faithful coordination between bacterial cell division and chromosome segregation in rod‐shaped bacteria, such as Escherichia coli and Bacillus subtilis, is dependent on the DNA translocase activity of FtsK/SpoIIIE proteins, which move DNA away from the division site before cytokinesis is completed. However, the role of these proteins in chromosome partitioning has not been well studied in spherical bacteria. Here, it was shown that the two Staphylococcus aureus FtsK/SpoIIIE homologues, SpoIIIE and FtsK, operate in independent pathways to ensure correct chromosome management during cell division. SpoIIIE forms foci at the centre of the closing septum in at least 50% of the cells that are close to complete septum synthesis. FtsK is a multifunctional septal protein with a C‐terminal DNA translocase domain that is not required for correct chromosome management in the presence of SpoIIIE. However, lack of both SpoIIIE and FtsK causes severe nucleoid segregation and morphological defects, showing that the two proteins have partially redundant roles in S. aureus.

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“…taphylococcus aureus, a Gram-positive bacterial pathogen, replicates via septal assembly of membranes and peptidoglycan into the cross wall compartment (1,2). The peptidoglycan of the cross wall is split by murein hydrolases, separating daughter cells that assume a spherical shape (3).…”

mentioning

confidence: 99%

SagB Glucosaminidase Is a Determinant of Staphylococcus aureus Glycan Chain Length, Antibiotic Susceptibility, and Protein Secretion

et al. 2016

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The envelope of Staphylococcus aureus is comprised of peptidoglycan and its attached secondary polymers, teichoic acid, capsular polysaccharide, and protein. Peptidoglycan synthesis involves polymerization of lipid II precursors into glycan strands that are cross-linked at wall peptides. It is not clear whether peptidoglycan structure is principally determined during polymerization or whether processive enzymes affect cell wall structure and function, for example, by generating conduits for protein secretion. We show here that S. aureus lacking SagB, a membrane-associated N-acetylglucosaminidase, displays growth and cell-morphological defects caused by the exaggerated length of peptidoglycan strands. SagB cleaves polymerized glycan strands to their physiological length and modulates antibiotic resistance in methicillin-resistant S. aureus (MRSA). Deletion of sagB perturbs protein trafficking into and across the envelope, conferring defects in cell wall anchoring and secretion, as well as aberrant excretion of cytoplasmic proteins. IMPORTANCEStaphylococcus aureus is thought to secrete proteins across the plasma membrane via the Sec pathway; however, protein transport across the cell wall envelope has heretofore not been studied. We report that S. aureus sagB mutants generate elongated peptidoglycan strands and display defects in protein secretion as well as aberrant excretion of cytoplasmic proteins. These results suggest that the thick peptidoglycan layer of staphylococci presents a barrier for protein secretion and that SagB appears to extend the Sec pathway across the cell wall envelope. Staphylococcus aureus, a Gram-positive bacterial pathogen, replicates via septal assembly of membranes and peptidoglycan into the cross wall compartment (1, 2). The peptidoglycan of the cross wall is split by murein hydrolases, separating daughter cells that assume a spherical shape (3). Earlier work identified three murein hydrolases with cross-wall-splitting activities: Atl (autolysin), Sle1, and LytN (3-5). Atl and Sle1 are secreted into the extracellular milieu and subsequently cleave septal peptidoglycan at the cross wall but not elsewhere as access is restricted by teichoic acid modification of peptidoglycan (6-8). LytN, on the other hand, is secreted into the cross wall compartment (5). S. aureus Atl is synthesized as a preproenzyme with an N-terminal signal peptide and prodomain (9, 10). Secreted pro-Atl is processed to generate Atl N-acetylmuramoyl-L-Ala-amidase (Atl AM ) and Atl Nacetylglucosaminidase (Atl GL ), and each binds via GW domains to lipoteichoic acids (10-12). Earlier work demonstrated that Atl functions as an endo-␤-N-acetylglucosaminidase (12, 13). Although initially designated autolysin (Atl), the S. aureus atl mutant does not display an autolysis phenotype yet forms large clusters of incompletely separated bacteria and is defective for penicillin-induced killing (14). The LysM domains of Sle1 promote its binding to cross wall peptidoglycan, and sle1 mutants also form clusters of incompletely s...

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Cell shape dynamics during the staphylococcal cell cycle

Cited by 209 publications

References 48 publications

Vibrio cholerae biofilm growth program and architecture revealed by single-cell live imaging

Vibrio cholerae biofilm growth program and architecture revealed by single-cell live imaging

Staphylococcus aureus requires at least one FtsK/SpoIIIE protein for correct chromosome segregation

SagB Glucosaminidase Is a Determinant of Staphylococcus aureus Glycan Chain Length, Antibiotic Susceptibility, and Protein Secretion

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