Identification of Bacillus subtilis SipW as a Bifunctional Signal Peptidase That Controls Surface-Adhered Biofilm Formation

Terra, Rebecca; Stanley‐Wall, Nicola R.; Cao, Gengyu; Lazazzera, Beth

doi:10.1128/jb.06780-11

Cited by 68 publications

(61 citation statements)

References 61 publications

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“…Other studies have highlighted specific determinants for multicellular development in these two liquid-air and solidliquid interfaces. For example, the PGA polymer is required for submerged-biofilm formation but not for floating pellicles (68); the signal peptidase SipW, required for TasA maturation in complex colonies, plays a regulatory role only in biofilm formation on submerged surfaces (69). The roles of the biofilm determinants identified using the pellicle model (e.g., the tapA-sipW-tasA operon, the epsA-O operon, and bslA) have to be further investigated at the solid-liquid interface.…”

Section: Discussionmentioning

confidence: 99%

Identification of ypqP as a New Bacillus subtilis Biofilm Determinant That Mediates the Protection of Staphylococcus aureus against Antimicrobial Agents in Mixed-Species Communities

Sanchez-Vizuete

Coq

Bridier³

et al. 2015

Appl Environ Microbiol

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In most habitats, microbial life is organized in biofilms, three-dimensional edifices sustained by extracellular polymeric substances that enable bacteria to resist harsh and changing environments. Under multispecies conditions, bacteria can benefit from the polymers produced by other species ("public goods"), thus improving their survival under toxic conditions. A recent study showed that a Bacillus subtilis hospital isolate (NDmed) was able to protect Staphylococcus aureus from biocide action in multispecies biofilms. In this work, we identified ypqP, a gene whose product is required in NDmed for thick-biofilm formation on submerged surfaces and for resistance to two biocides widely used in hospitals. NDmed and S. aureus formed mixed biofilms, and both their spatial arrangement and pathogen protection were mediated by YpqP. Functional ypqP is present in other natural B. subtilis biofilm-forming isolates. However, the gene is disrupted by the SP␤ prophage in the weak submerged-biofilm-forming strains NCIB3610 and 168, which are both less resistant than NDmed to the biocides tested. Furthermore, in a 168 laboratory strain cured of the SP␤ prophage, the reestablishment of a functional ypqP gene led to increased thickness and resistance to biocides of the associated biofilms. We therefore propose that YpqP is a new and important determinant of B. subtilis surface biofilm architecture, protection against exposure to toxic compounds, and social behavior in bacterial communities. Bacillus subtilis is a nonpathogenic Gram-positive bacterium that can be found in its natural habitats as free cells or associated with surfaces in biofilms. In the soil, B. subtilis strains have been shown to form surface-associated communities on plant tissues that protect them from infection by pathogens (1-3). Because of its ability to resist stress through biofilm or spore formation, the bacterium has been isolated from extreme environments, such as sand deserts, clouds, and the digestive tracts of animals (4 -6). As well as its ubiquitous presence in diverse habitats, B. subtilis has been used extensively in biotechnological applications, such as the production of natto, a traditional Japanese food made of fermented soybeans (7), and the production of industrial enzymes and pharmaceutical proteins (8, 9). As a generally recognized as safe (GRAS) organism, B. subtilis is also used as a biocontrol agent in agriculture and livestock buildings (10 -14) and as a probiotic agent to improve human and animal health by preventing gastrointestinal infections (15,16).In fundamental research, B. subtilis has emerged as the model organism for deciphering the complex genetic regulation involved in the biofilm mode of life of Gram-positive bacteria. The domesticated strain B. subtilis 168 has been widely used to dissect metabolic and cellular processes. However, this strain is not able to form robust pellicles and complex colonies like those of its parental strain, NCIB3610, a descendant of the original Marburg strain that was deposited in 1951 (17)....

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Section: Discussionmentioning

confidence: 99%

Identification of ypqP as a New Bacillus subtilis Biofilm Determinant That Mediates the Protection of Staphylococcus aureus against Antimicrobial Agents in Mixed-Species Communities

Sanchez-Vizuete

Coq

Bridier³

et al. 2015

Appl Environ Microbiol

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“…Thus, SipW and other closely related SPI enzymes most likely employ a conventional Ser-His-Asp catalytic triad or a Ser-His catalytic dyad similar to that of the ER SPC (152,175). Very recently, it was reported that the 20 C-terminal residues of SipW, which localize in the cytoplasm, serve a potentially nonenzymatic function in the regulation of biofilm formation on solid surfaces (145). Site-directed mutagenesis data show that the signal peptidase activity of SipW is dispensable for the formation of this type of biofilms.…”

Section: Signal Peptidase Imentioning

confidence: 99%

Membrane Proteases in the Bacterial Protein Secretion and Quality Control Pathway

Dalbey

Wang

Dijl

2012

Microbiol Mol Biol Rev

126

129

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SUMMARY Proteolytic cleavage of proteins that are permanently or transiently associated with the cytoplasmic membrane is crucially important for a wide range of essential processes in bacteria. This applies in particular to the secretion of proteins and to membrane protein quality control. Major progress has been made in elucidating the structure-function relationships of many of the responsible membrane proteases, including signal peptidases, signal peptide hydrolases, FtsH, the rhomboid protease GlpG, and the site 1 protease DegS. These enzymes employ very different mechanisms to cleave substrates at the cytoplasmic and extracytoplasmic membrane surfaces or within the plane of the membrane. This review highlights the different ways that bacterial membrane proteases degrade their substrates, with special emphasis on catalytic mechanisms and substrate delivery to the respective active sites.

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“…In vivo, the polymerization of TasA into amyloid fibers requires all three members of the tapA-sipW-tasA operon (20). SipW is a bifunctional protein that has dedicated signal peptidase activity for processing and secretion of TapA and TasA and also regulates expression of genes involved in exopolysaccharide production (25)(26)(27). TasA is the main component of the fibers, and TapA is a minor component that is copurified in a 1:100 ratio with TasA (28).…”

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confidence: 99%

Functional Analysis of the Accessory Protein TapA in Bacillus subtilis Amyloid Fiber Assembly

et al. 2014

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bBacillus subtilis biofilm formation relies on the assembly of a fibrous scaffold formed by the protein TasA. TasA polymerizes into highly stable fibers with biochemical and morphological features of functional amyloids. Previously, we showed that assembly of TasA fibers requires the auxiliary protein TapA. In this study, we investigated the roles of TapA sequences from the C-terminal and N-terminal ends and TapA cysteine residues in its ability to promote the assembly of TasA amyloid-like fibers. We found that the cysteine residues are not essential for the formation of TasA fibers, as their replacement by alanine residues resulted in only minor defects in biofilm formation. Mutating sequences in the C-terminal half had no effect on biofilm formation. However, we identified a sequence of 8 amino acids in the N terminus that is key for TasA fiber formation. Strains expressing TapA lacking these 8 residues were completely defective in biofilm formation. In addition, this TapA mutant protein exhibited a dominant negative effect on TasA fiber formation. Even in the presence of wild-type TapA, the mutant protein inhibited fiber assembly in vitro and delayed biofilm formation in vivo. We propose that this 8-residue sequence is crucial for the formation of amyloid-like fibers on the cell surface, perhaps by mediating the interaction between TapA or TapA and TasA molecules.

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Identification of Bacillus subtilis SipW as a Bifunctional Signal Peptidase That Controls Surface-Adhered Biofilm Formation

Cited by 68 publications

References 61 publications

Identification of ypqP as a New Bacillus subtilis Biofilm Determinant That Mediates the Protection of Staphylococcus aureus against Antimicrobial Agents in Mixed-Species Communities

Identification of ypqP as a New Bacillus subtilis Biofilm Determinant That Mediates the Protection of Staphylococcus aureus against Antimicrobial Agents in Mixed-Species Communities

Membrane Proteases in the Bacterial Protein Secretion and Quality Control Pathway

Functional Analysis of the Accessory Protein TapA in Bacillus subtilis Amyloid Fiber Assembly

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