A holin and an endopeptidase are essential for chitinolytic protein secretion in <i>Serratia marcescens</i>

Hamilton, Jaeger J.; Marlow, Victoria L.; Owen, Richard; Costa, Marília de Assis Alcoforado; Guo, Meng; Buchanan, Grant; Chandra, Govind; Trost, Matthias; Coulthurst, Sarah J.; Palmer, Tracy; Stanley‐Wall, Nicola R.; Sargent, Frank

doi:10.1083/jcb.201404127

Cited by 47 publications

(110 citation statements)

References 46 publications

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“…marcescens fungal killing does not depend on the secretion of chitinases. S. marcescens secretes unusually high levels of three extracellular chitinases (ChiA, ChiB, and ChiC), enabling it to use chitin as a source of nitrogen and carbon (10,19). We hypothe- Db10 wild type and Db10-NoChi strain (lacking detectable secreted chitinase activity) were inoculated separately in the center of SOC agar petri dishes coated with 12-h-old R. oryzae 3465 mycelia and incubated at 30°C.…”

Section: Discussionmentioning

confidence: 99%

“…Because S. marcescens produces extraordinary amounts of secreted chitinases and the zygomycetes contain an unusually high proportion of chitin in their cell walls, we hypothesized that fungal killing is mediated by secreted S. marcescens chitinases. We therefore compared the spreading and killing activities of a no-Chi (⌬chiA ⌬chiB ⌬chiC) triple mutant lacking any detectable secreted chitinase activity to those of the isogenic wild-type Dba10 strain (19). There was no difference in the ability of the no-Chi mutant to spread along R. oryzae 3465 mycelia from that of the wild-type strain (Fig.…”

Section: Fig 4 S Marcescens 1 Crosses An Aerial Bridge Of R Oryzae mentioning

confidence: 99%

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Mechanisms of Bacterial (Serratia marcescens) Attachment to, Migration along, and Killing of Fungal Hyphae

Hover

Maya

Ron

et al. 2016

Appl Environ Microbiol

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We have found a remarkable capacity for the ubiquitous Gram-negative rod bacterium Serratia marcescens to migrate along and kill the mycelia of zygomycete molds. This migration was restricted to zygomycete molds and several basidiomycete species. No migration was seen on any molds of the phylum Ascomycota. S. marcescens migration did not require fungal viability or surrounding growth medium, as bacteria migrated along aerial hyphae as well. S. marcescens did not exhibit growth tropism toward zygomycete mycelium. Bacterial migration along hyphae proceeded only when the hyphae grew into the bacterial colony. S. marcescens cells initially migrated along the hyphae, forming attached microcolonies that grew and coalesced to generate a biofilm that covered and killed the mycelium. Flagellum-defective strains of S. marcescens were able to migrate along zygomycete hyphae, although they were significantly slower than the wild-type strain and were delayed in fungal killing. Bacterial attachment to the mycelium does not necessitate type 1 fimbrial adhesion, since mutants defective in this adhesin migrated equally well as or faster than the wild-type strain. Killing does not depend on the secretion of S. marcescens chitinases, as mutants in which all three chitinase genes were deleted retained wild-type killing abilities. A better understanding of the mechanisms by which S. marcescens binds to, spreads on, and kills fungal hyphae might serve as an excellent model system for such interactions in general; fungal killing could be employed in agricultural fungal biocontrol.

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Section: Discussionmentioning

confidence: 99%

Section: Fig 4 S Marcescens 1 Crosses An Aerial Bridge Of R Oryzae mentioning

confidence: 99%

Mechanisms of Bacterial (Serratia marcescens) Attachment to, Migration along, and Killing of Fungal Hyphae

Hover

Maya

Ron

et al. 2016

Appl Environ Microbiol

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“…In this case, induction of the alp genes in a subset of cells would facilitate colonization of the lung by a lysis-independent mechanism. In relation to this, it is noteworthy that in Serratia marcescens, a protein with features similar to that of a holin has been implicated in promoting the secretion of chitinases (33). It is therefore conceivable that expression of the alp genes might promote colonization of the host lung through an effect on protein secretion.…”

Section: Discussionmentioning

confidence: 99%

A self-lysis pathway that enhances the virulence of a pathogenic bacterium

McFarland

Dolben

LeRoux

et al. 2015

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

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In mammalian cells, programmed cell death (PCD) plays important roles in development, in the removal of damaged cells, and in fighting bacterial infections. Although widespread among multicellular organisms, there are relatively few documented instances of PCD in bacteria. Here we describe a potential PCD pathway in Pseudomonas aeruginosa that enhances the ability of the bacterium to cause disease in a lung infection model. Activation of the system can occur in a subset of cells in response to DNA damage through cleavage of an essential transcription regulator we call AlpR. Cleavage of AlpR triggers a cell lysis program through de-repression of the alpA gene, which encodes a positive regulator that activates expression of the alpBCDE lysis cassette. Although this is lethal to the individual cell in which it occurs, we find it benefits the population as a whole during infection of a mammalian host. Thus, host and pathogen each may use PCD as a survival-promoting strategy. We suggest that activation of the Alp cell lysis pathway is a disease-enhancing response to bacterial DNA damage inflicted by the host immune system.

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“…A recent study also revealed that a holin-like gene, chiW, and a putative endopeptidase gene, chiX, were required for secretion of three chitinase virulence factors in the opportunistic Gram-negative pathogen Serratia marcescens (Hamilton et al, 2014). While biofilm formation has been shown to be affected by the production of functional filamentous prophage Pf1 and Pf4 in P. aeruginosa (Rice et al, 2009;Webb et al, 2004), the mechanisms whereby defective prophages affect biofilm formation in E. coli are not well understood (Wang et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

The lysis cassette of DLP12 defective prophage is regulated by RpoE

et al. 2015

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Expression of the lysis cassette (essD, ybcT, rzpD/rzoD) from the defective lambdoid prophage at the 12th minute of Escherichia coli's genome (DLP12) is required in some strains for proper curli expression and biofilm formation. Regulating production of the lytic enzymes encoded by these genes is critical for maintaining cell wall integrity. In lambdoid phages, late-gene regulation is mediated by the vegetative sigma factor RpoD and the lambda antiterminator Q l . We previously demonstrated that DLP12 contains a Q-like protein (Q DLP12 ) that positively regulates transcription of the lysis cassette, but the sigma factor responsible for this transcription initiation remained to be elucidated. In silico analysis of essDp revealed the presence of a putative 235 and 210 sigma site recognized by the extracytoplasmic stress response sigma factor, RpoE. In this work, we report that RpoE overexpression promoted transcription from essDp in vivo, and in vitro using purified RNAP. We demonstrate that the 235 region is important for RpoE binding in vitro and that this region is also important for Q DLP12 -mediated transcription of essDp in vivo. A bacterial two-hybrid assay indicated that Q DLP12 and RpoE physically interact in vivo, consistent with what is seen for Q l and RpoD.We propose that RpoE regulates transcription of the DLP12 lysis genes through interaction with Q DLP12 and that proper expression is dependent on an intact 235 sigma region in essDp.This work provides evidence that the unique Q-dependent regulatory mechanism of lambdoid phages has been co-opted by E. coli harbouring defective DLP12 and has been integrated into the tightly controlled RpoE regulon.

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A holin and an endopeptidase are essential for chitinolytic protein secretion in Serratia marcescens

Abstract: A holin (ChiW) and an endopeptidase (ChiX) operate in tandem as components of a protein secretion system used by the gram-negative bacterium Serratia marcescens to secrete the chitinolytic machinery.

Cited by 47 publications

References 46 publications

Mechanisms of Bacterial (Serratia marcescens) Attachment to, Migration along, and Killing of Fungal Hyphae

Mechanisms of Bacterial (Serratia marcescens) Attachment to, Migration along, and Killing of Fungal Hyphae

A self-lysis pathway that enhances the virulence of a pathogenic bacterium

The lysis cassette of DLP12 defective prophage is regulated by RpoE

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