FtsEX-CwlO regulates biofilm formation by a plant-beneficial rhizobacterium Bacillus velezensis SQR9

Li, Qing X.; Li, Zunfeng; Li, Xingxing; Xia, Liming; Zhou, Xuan; Xu, Zhihui; Shao, Jiahui; Shen, Qirong; Zhang, Ruifu

doi:10.1016/j.resmic.2018.01.004

Cited by 21 publications

(14 citation statements)

References 47 publications

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“…To delete the target genes, the upstream and downstream regions that flanked the target genes were amplified from the SQR9 genome, and the erythromycin resistance gene was amplified from plasmid pAX01. The fragments were fused through overlap PCR, the fused fragments were transformed into competent cells of B. velezensis SQR9, and the transformants were screened and verified as described in a previous study (52). The primers used in this study are shown in Supplementary Table S2.…”

Section: Gene Knockout By Allelic Exchangementioning

confidence: 99%

“…The suspensions of B. velezensis strains were prepared and inoculated into the wells of 24-well polyvinylchloride (PVC) microtiter plates (Fisher Scientific, Shanghai, China) filled with MSgg medium as described previously (52). Subsequently, 14-by 14-mm sterile coverslips were inserted into the above wells, and the microtiter plates were incubated at 37 °C without shaking.…”

Section: Biofilm Assay and Microscopic Observationmentioning

confidence: 99%

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A unique genomic island-governed cannibalism in Bacillus enhanced biofilm formation through a novel regulation mechanism

Huang

Wang

et al. 2021

Preprint

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Cannibalism is a differentiation strategy and social multicellular behavior in biofilms. The novel factors and mechanisms to trigger the bacterial cannibalism remain scarce. Here, we report a novel bacillunoic acids-mediated strategy for manipulating cannibalism in Bacillus velezensis SQR9 biofilm formation. A subfraction of cells differentiate into cannibals that secrete toxic bacillunoic acids to lyse a fraction of their sensitive siblings, and the released nutrients enhance biofilm formation. Meanwhile, the self-immunity of cannibal cells was induced by bacillunoic acids. A two-component system, the OmpS-OmpR signal-transduction pathway, controls the expression of the ABC transporter BnaAB for self-immunity. Specifically, bacillunoic acids activate the autophosphorylation of OmpS, a transmembrane histidine kinase, which then transfers a phosphoryl group to its response regulator OmpR. The phosphorylation of OmpR activates the transcription of the transporter gene bnaAB by binding its promoter. Thus, bacillunoic acids are pumped out of cells by the ABC transporter BnaAB. Moreover, we discovered that strain SQR9 could use the bacillunoic acids-mediated cannibalism to optimize its community to produce more bacillunoic acids for bacterial competition. This study revealed that bacillunoic acids play a previously undiscovered dual role in both cannibalism during biofilm formation and interspecies competition, which has an important biological signiﬁcance.

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Section: Gene Knockout By Allelic Exchangementioning

confidence: 99%

Section: Biofilm Assay and Microscopic Observationmentioning

confidence: 99%

A unique genomic island-governed cannibalism in Bacillus enhanced biofilm formation through a novel regulation mechanism

Huang

Wang

et al. 2021

Preprint

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“…Strain SQR9 is widely used as biofertilizer and biocontrol agents in agricultural production with the trademark of BIO TM (Cao et al, 2012;Qiu et al, 2012). As a root colonizer, SQR9 has robust regulation systems to form a highly structured biofilm on a root surface that was found to enhance its rhizoplane colonization, during this process, the FtsEX-CwlO pathway, two-component regulatory system ResDE and DegUS as well as the signal bacillomycin D and oxygen deficiency were involved (Xu et al, 2013;Li et al, 2018;Zhou et al, 2018). Strain SQR9 efficiently promotes plant growth and suppresses soil-borne diseases (Xu et al, 2013Qiu et al, 2014), besides the antimicrobial compounds, SQR9 also benefits from its versatile metabolism that can exploit diverse root-secreted growth substrates (Zhang et al, 2015(Zhang et al, , 2016.…”

Section: Introductionmentioning

confidence: 99%

A genomic island in a plant beneficial rhizobacterium encodes novel antimicrobial fatty acids and a self‐protection shield to enhance its competition

Wang

Zhang

et al. 2019

Environmental Microbiology

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Summary Rhizobacteria devote a relatively large percentage of their genomes to encode bioactive natural products that are important for competition in the rhizosphere. In this study, a plant beneficial rhizobacterium Bacillus velezensis SQR9 was discovered to produce novel antibacterial fatty acids, Bacillunoic acids, which are encoded on a genomic island (GI). This GI contains a hybrid type I fatty acid synthase (FAS)‐polyketide synthase (PKS) system and an ABC transporter. The FAS was predicted to synthesize a primer that was transferred to the PKS to synthesize Bacillunoic acids. The synthesized Bacillunoic acids inhibit the growth of diverse bacteria, with the strongest activity against closely related Bacillus strains, the ABC transporter exported the toxic Bacillunoic acids upon their induction for protecting the producing strain. The inhibition of other Bacillus strains by Bacillunoic acids extended the antimicrobial spectrum of SQR9 and enhanced its competition with closely related root‐associated bacteria. So, through the obtaining of this GI by horizontal gene transfer, strain SQR9 not only acquired a competitive weapon but also acquired a self‐protecting shield, which increased its competition with other rhizobacteria.

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“…In contrast, the FtsEX of B. subtilis has no obvious role in cell division but instead controls the peptidoglycan hydrolase CwlO, which plays an important role in cell wall expansion during cell elongation (19,34,35) and regulates entry into sporulation (36). FtsEX was recently reported to be involved in other biological processes such as control of both the early and late stages of cytokinesis in the alphaproteobacterium Caulobacter crescentus (37) or control of the activity of autolysin CwlO to regulate biofilm formation in Bacillus velezensis strain SQR9, a plant-beneficial rhizobacterium (38). S. pneumoniae and most other Gram-positive bacteria synthesize a complete septal cross wall before cell separation takes place at the end of the cell cycle.…”

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confidence: 99%

Structural Characterization of the Essential Cell Division Protein FtsE and Its Interaction with FtsX in Streptococcus pneumoniae

Alcorlo

Straume

Lutkenhaus

et al. 2020

mBio

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FtsEX is a membrane complex widely conserved across diverse bacterial genera and involved in critical processes such as recruitment of division proteins and in spatial and temporal regulation of muralytic activity during cell division or sporulation. FtsEX is a member of the ABC transporter superfamily. The component FtsX is an integral membrane protein, whereas FtsE is an ATPase and is required for the transmission of a conformational signal from the cytosol through the membrane to regulate the activity of cell wall hydrolases in the periplasm. Both proteins are essential in the major human respiratory pathogenic bacterium Streptococcus pneumoniae, and FtsX interacts with the modular peptidoglycan hydrolase PcsB at the septum. Here, we report high-resolution structures of pneumococcal FtsE bound to different nucleotides. Structural analysis revealed that FtsE contains all the conserved structural motifs associated with ATPase activity and afforded interpretation of the in vivo dimeric arrangement in both the ADP and ATP states. Interestingly, three specific FtsE regions with high structural plasticity were identified that shape the cavity in which the cytosolic region of FtsX would be inserted. The residues corresponding to the FtsX coupling helix, responsible for contacting FtsE, were identified and validated by in vivo mutagenesis studies showing that this interaction is essential for cell growth and proper morphology. IMPORTANCE Bacterial cell division is a central process that requires exquisite orchestration of both the cell wall biosynthetic and lytic machineries. The essential membrane complex FtsEX, widely conserved across bacteria, plays a central role by recruiting proteins to the divisome apparatus and by regulating periplasmic muralytic activity from the cytosol. FtsEX is a member of the type VII family of the ABC-superfamily, but instead of being a transporter, it couples the ATP hydrolysis catalyzed by FtsE to mechanically transduce a conformational signal that provokes the activation of peptidoglycan (PG) hydrolases. So far, no structural information is available for FtsE. Here, we provide the structural characterization of FtsE, confirming its ATPase nature and revealing regions with high structural plasticity which are key for FtsE binding to FtsX. The complementary binding region in FtsX has also been identified and validated in vivo. Our results provide evidence on how the difference between the ATP/ADP-bound states in FtsE would dramatically alter the interaction of FtsEX with the PG hydrolase PcsB in pneumococcal division.

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FtsEX-CwlO regulates biofilm formation by a plant-beneficial rhizobacterium Bacillus velezensis SQR9

Cited by 21 publications

References 47 publications

A unique genomic island-governed cannibalism in Bacillus enhanced biofilm formation through a novel regulation mechanism

A unique genomic island-governed cannibalism in Bacillus enhanced biofilm formation through a novel regulation mechanism

A genomic island in a plant beneficial rhizobacterium encodes novel antimicrobial fatty acids and a self‐protection shield to enhance its competition

Structural Characterization of the Essential Cell Division Protein FtsE and Its Interaction with FtsX in Streptococcus pneumoniae

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