A Specialized Peptidoglycan Synthase Promotes
            <i>Salmonella</i>
            Cell Division inside Host Cells

Castanheira, Sónia; Cestero, Juan J.; Rico-Pérez, Gadea; García, Pablo D.; Cava, Felipe; Ayala, Juan A.; Pucciarelli, M. Graciela; Portillo, Francisco García‐del

doi:10.1128/mbio.01685-17

Cited by 38 publications

(99 citation statements)

References 48 publications

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“…In particular, we speculate that pH affects many, if not all, of the extracellular divisome proteins either by directly impacting activity or through more subtle changes in protein-protein interactions. Consistent with this model, we and others have previously identified a multitude of pH sensitive extracellular cell wall enzymes with diverse enzymatic functions [43,67–69]. S. aureus and S. pneumoniae still undergo pH-dependent changes in size but lack identifiable homologs of FtsN (SI Appendix, Figure S3) [70], indicating the existence of additional pH-responsive divisome components at least in these organisms.…”

Section: Discussionsupporting

confidence: 80%

Environmental pH impacts division assembly and cell size inEscherichia coli

Mueller

Westfall

Levin

2019

Preprint

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Cell size is a complex trait, derived from both genetic and environmental factors. Environmental determinants of bacterial cell size identified to date primarily target assembly of cytosolic components of the cell division machinery. Whether certain environmental cues also impact cell size through changes in the assembly or activity of extracytoplasmic division proteins remains an open question. Here, we identify extracellular pH as a modulator of cell division and a key determinant of cell size across evolutionarily distant bacterial species. In the Gram-negative model organism Escherichia coli, our data indicate environmental pH impacts the length at which cells divide by altering the ability of the terminal cell division protein FtsN to localize to the cytokinetic machinery and activate division. Acidic environments lead to enrichment of FtsN at the septum and activation of division at a reduced cell length, while alkaline pH inhibits FtsN localization and suppress division activation. Altogether, our work reveals a previously unappreciated role for pH in bacterial cell size control.

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Section: Discussionsupporting

confidence: 80%

Environmental pH impacts division assembly and cell size inEscherichia coli

Mueller

Westfall

Levin

2019

Preprint

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“…The ftsI mutation we identified in S. enterica only arose in co-culture environments, despite being associated with increased ampicillin resistance. This is particularly interesting as ftsI activity is implicated in interactions between S. enterica and the human immune system (33).…”

Section: Discussionmentioning

confidence: 99%

“…could be mitigated by growing S. enterica under acidic conditions (pH<5.8); under these conditions, a second PBP3, which they called PBP3SAL, is expressed (33). In light of this, we plated co-culture populations containing Q142* or +A mutations in ftsI on LB of pH 4.7.…”

Section: Castanheira Et Al Recently Demonstrated That the Lethality mentioning

confidence: 99%

Cross-feeding modulates the rate and mechanism of antibiotic resistance evolution in a model microbial community of Escherichia coli and Salmonella enterica

Adamowicz

Muza

Chacón

et al. 2019

Preprint

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Author contributions: E.M.A, M.A.M., J.M.C. and W.R.H. designed research; E.M.A, M.A.M., and J.M.C. performed research; E.M.A., J.M.C., and W.R.H. analyzed data; and E.M.A., J.M.C., and W.R.H. wrote the paper. AbstractWith antibiotic resistance rates on the rise, it is critical to understand how microbial species interactions influence the evolution of resistance. We have previously shown that in obligate mutualisms the survival of any one species (regardless of its intrinsic resistance) is contingent on the resistance of its cross-feeding partners, setting the community antibiotic tolerance at that of the 'weakest link' species. In this study, we extended that hypothesis to test whether obligate cross-feeding would limit the extent and mechanisms of antibiotic resistance evolution. In both rifampicin and ampicillin treatments, we observed that resistance evolved more slowly in obligate co-cultures of E. coli and S. enterica than in monocultures. While we observed similar mechanisms of resistance arising under rifampicin selection, under ampicillin selection different resistance mechanisms arose in co-cultures and monocultures. In particular, mutations in an essential cell division protein, ftsI, arose in S. enterica only in co-culture. A simple mathematical model demonstrated that reliance on a partner is sufficient to slow the rate of adaptation, and can change the distribution of adaptive mutations that are acquired. Our results demonstrate that cooperative metabolic interactions can be an important modulator of resistance evolution in microbial communities. Significance statementLittle is known about how ecological interactions between bacteria influence the evolution of antibiotic resistance. We tested the impact of metabolic interactions on resistance evolution in an engineered two-species bacterial community. Through experimental and modeling work, we found that obligate metabolic interdependency slows the rate of resistance acquisition, and can change the type and magnitude of resistance mutations that evolve. This work suggests that resistance evolution may be slowed by targeting both a pathogen and its metabolic partners with antibiotics. Additionally, we showed that community context can generate novel trajectories through which antibiotic resistance evolves.

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“…Singh et al also identified in E. coli three periplasmic PG endopeptidases, Spr, YdhO and YebA, all dispensable in laboratory media but with the requirement of at least one of the three for growth (Singh, SaiSree, Amrutha, & Reddy, 2012). S. Typhimurium up-regulates a specialized PBP that is active only in acidic pH and promotes cell division in intracellular bacteria (Castanheira et al, 2017). This work also showed the capacity of this 'intracellularly-induced PBP' to drive cell division in mutants lacking PBP3, which is essential in E. coli (Castanheira, Cestero, Garcia-del Portillo, & Pucciarelli, 2018;Castanheira et al, 2017).…”

Section: Redundan C Y and S Pecializ Ati On Of P G Enz Yme S In Intmentioning

confidence: 99%

“…S. Typhimurium up-regulates a specialized PBP that is active only in acidic pH and promotes cell division in intracellular bacteria (Castanheira et al, 2017). This work also showed the capacity of this 'intracellularly-induced PBP' to drive cell division in mutants lacking PBP3, which is essential in E. coli (Castanheira, Cestero, Garcia-del Portillo, & Pucciarelli, 2018;Castanheira et al, 2017). These latter findings highlight the suitability of working with facultative intracellular bacterial pathogens to uncover new phenomena related to PG plasticity and specialization of PG enzymes M. tuberculosis has also five l,d-transpeptidases (Squeglia, Ruggiero, & Berisio, 2018).…”

Section: Redundan C Y and S Pecializ Ati On Of P G Enz Yme S In Intmentioning

confidence: 99%

Building peptidoglycan inside eukaryotic cells: A view from symbiotic and pathogenic bacteria

Portillo

2020

Molecular Microbiology

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The peptidoglycan (PG), as the exoskeleton of most prokaryotes, maintains a defined shape and ensures cell integrity against the high internal turgor pressure. These important roles have attracted researchers to target PG metabolism in order to control bacterial infections. Most studies, however, have been performed in bacteria grown under laboratory conditions, leading to only a partial view on how the PG is synthetized in natural environments. As a case in point, PG metabolism and its regulation remain poorly understood in symbiotic and pathogenic bacteria living inside eukaryotic cells. This review focuses on the PG metabolism of intracellular bacteria, emphasizing the necessity of more in vivo studies involving the analysis of enzymes produced in the intracellular niche and the isolation of PG from bacteria residing within eukaryotic cells. The review also points to persistent infections caused by some intracellular bacterial pathogens and the extent at which the PG could contribute to establish such physiological state. Based on recent evidences, I speculate on the idea that certain structural features of the PG may facilitate attenuation of intracellular growth. Lastly, I discuss recent findings in endosymbionts supporting a cooperation between host and bacterial enzymes to assemble a mature PG.

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A Specialized Peptidoglycan Synthase Promotes Salmonella Cell Division inside Host Cells

Cited by 38 publications

References 48 publications

Environmental pH impacts division assembly and cell size inEscherichia coli

Environmental pH impacts division assembly and cell size inEscherichia coli

Cross-feeding modulates the rate and mechanism of antibiotic resistance evolution in a model microbial community of Escherichia coli and Salmonella enterica

Building peptidoglycan inside eukaryotic cells: A view from symbiotic and pathogenic bacteria

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