flrA,flrBandflrCregulate adhesion by controlling the expression of critical virulence genes inVibrio alginolyticus

Luo, Gang; Huang, Lixing; Su, Yongquan; Qin, Yingxue; Xu, Xiaojin; Zhao, Lingmin; Yan, Qingpi

doi:10.1038/emi.2016.82

Cited by 83 publications

(64 citation statements)

References 51 publications

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“…In V. cholerae, the FlrA regulon has been limited in flagellum-coding genes to date, and the FlrA regulation of flagellum synthesis seems unaffected by FlhG (26). The deficiency of FlrA in Vibrio results in the altered expression of some virulence genes and binding to epithelial cells, while it is still unclear whether FlrA directly regulates the transcription of these genes (35,36). In contrast, FleQ in P. aeruginosa regulates many biofilm-related genes, such as pel and psl for exopolysaccharide synthesis and cdrAB, coding for an adhesin.…”

Section: Discussionmentioning

confidence: 99%

FlrA Represses Transcription of the Biofilm-Associated bpfA Operon in Shewanella putrefaciens

Cheng

et al. 2017

Appl Environ Microbiol

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Manipulation of biofilm formation in Shewanella is beneficial for application to industrial and environmental biotechnology. BpfA is an adhesin largely responsible for biofilm formation in many Shewanella species. However, the mechanism underlying BpfA production and the resulting biofilm remains vaguely understood. We previously described the finding that BpfA expression is enhanced by DosD, an oxygen-stimulated diguanylate cyclase, under aerobic growth. In the present work, we identify FlrA as a critical transcription regulator of the bpfA operon in Shewanella putrefaciens CN32 by transposon mutagenesis. FlrA acted as a repressor of the operon promoter by binding to two boxes overlapping the Ϫ10 and Ϫ35 sites recognized by 70 . DosD regulation of the expression of the bpfA operon was mediated by FlrA, and cyclic diguanylic acid (c-di-GMP) abolished FlrA binding to the operon promoter. We also demonstrate that FlhG, an accessory protein for flagellum synthesis, antagonized FlrA repression of the expression of the bpfA operon. Collectively, this work demonstrates that FlrA acts as a central mediator in the signaling pathway from c-di-GMP to BpfA-associated biofilm formation in S. putrefaciens CN32.IMPORTANCE Motility and biofilm are mutually exclusive lifestyles, shifts between which are under the strict regulation of bacteria attempting to adapt to the fluctuation of diverse environmental conditions. The FlrA protein in many bacteria is known to control motility as a master regulator of flagellum synthesis. This work elucidates its effect on biofilm formation by controlling the expression of the adhesin BpfA in S. putrefaciens CN32 in response to c-di-GMP. Therefore, FlrA plays a dual role in controlling motility and biofilm formation in S. putrefaciens CN32. The cooccurrence of flrA, bpfA, and the FlrA box in the promoter region of the bpfA operon in diverse Shewanella strains suggests that bpfA is a common mechanism that controls biofilm formation in this bacterial species.KEYWORDS FlrA, Shewanella, biofilm, cyclic di-GMP, transcriptional factor B iofilm formed by bacteria is a multicell architecture for adaptation to diverse niches (1). Shewanella can form biofilm on a variety of surfaces, such as ferric oxides, electrodes, stainless steel, and glass (2-4). This genus is also renowned for an extracellular respiration ability to reduce iron oxide, electrodes, and other extracellular electron acceptors, including heavy metal ions. Such an ability has diverse potential applications in bioengineering and bioremediation (5). Biofilm formation in Shewanella benefits close contact with solid electron acceptors, thereby accelerating iron oxide reduction and improving current output, as well as inducing spatially stratified metabolic responses during contaminant exposure (4, 6, 7). Biofilm formed by Shewanella prevents microbially induced corrosion of steel and cast iron pipes (8, 9). On the other hand, biofilm formation of Shewanella also causes problems in some circumstances. For

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Section: Discussionmentioning

confidence: 99%

FlrA Represses Transcription of the Biofilm-Associated bpfA Operon in Shewanella putrefaciens

Cheng

et al. 2017

Appl Environ Microbiol

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“…It is an opportunistic pathogen and a major cause of vibriosis in aquatic animals, resulting in severe economic losses worldwide (6,7). Recent studies suggested that V. alginolyticus is also a potential human pathogen (8).…”

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confidence: 99%

Pumilacidin-Like Lipopeptides Derived from Marine Bacterium Bacillus sp. Strain 176 Suppress the Motility of Vibrio alginolyticus

Xiu

Zhang

et al. 2017

Appl Environ Microbiol

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Bacterial motility is a crucial factor during the invasion and colonization processes of pathogens, which makes it an attractive therapeutic drug target. Here, we isolated a marine bacterium (Vibrio alginolyticus strain 178) from a seamount in the tropical West Pacific that exhibits vigorous motility on agar plates and severe pathogenicity to zebrafish. We found that V. alginolyticus 178 motility was significantly suppressed by another marine bacterium, Bacillus sp. strain 176, isolated from the same niche. We isolated, purified, and characterized two different cyclic lipopeptides (CLPs) from Bacillus sp. 176 using high-performance liquid chromatography, mass spectrometry, and nuclear magnetic resonance spectroscopy. The two related CLPs have a pumilacidin-like structure and were both effective inhibitors of V. alginolyticus 178 motility. The CLPs differ by only one methylene group in their fatty acid chains. In addition to motility suppression, the CLPs also induced cell aggregation in the medium and reduced adherence of V. alginolyticus 178 to glass substrates. Notably, upon CLP treatment, the expression levels of two V. alginolyticus flagellar assembly genes (flgA and flgP) dropped dramatically. Moreover, the CLPs inhibited biofilm formation in several other strains of pathogenic bacteria without inducing cell death. This study indicates that CLPs from Bacillus sp. 176 show promise as antimicrobial lead compounds targeting bacterial motility and biofilm formation with a low potential for eliciting antibiotic resistance.IMPORTANCE Pathogenic bacteria often require motility to establish infections and subsequently spread within host organisms. Thus, motility is an attractive therapeutic target for the development of novel antibiotics. We found that cyclic lipopeptides (CLPs) produced by marine bacterium Bacillus sp. strain 176 dramatically suppress the motility of the pathogenic bacterium Vibrio alginolyticus strain 178, reduce biofilm formation, and promote cellular aggregation without inducing cell death. These findings suggest that CLPs hold great promise as potential drug candidates targeting bacterial motility and biofilm formation with a low overall potential for triggering antibiotic resistance.KEYWORDS lipopeptide, pumilacidin, Vibrio alginolyticus, motility, antibiotic, antimicrobial, antibiofilm B acterial motility is one of several crucial factors during the initial infection and colonization processes of pathogens. In particular, it helps pathogens overcome the repulsive forces between the bacterial cell wall and the host tissues and facilitates host attachment (1-3). The flagellum is one of the main locomotive organelles respon-

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“…clpC is thought to serve as a molecular chaperone with a significant role in Bacillus subtilis sporulation (Nanamiya et al., ). As bacterial adhesion to the host surface is critical for pathogen invasion (Chen et al., ; Luo et al., ), it is important that probiotics compete with pathogens for adhesion sites. Flagella are reported to be important for bacterial adhesion (Qin et al., ; Wang et al., ).…”

Section: Discussionmentioning

confidence: 99%

The complete genome sequence of Exiguobacterium arabatum W‐01 reveals potential probiotic functions

Cong

Jiang

et al. 2017

MicrobiologyOpen

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Shrimp is extensively cultured worldwide. Shrimp farming is suffering from a variety of diseases. Probiotics are considered to be one of the effective methods to prevent and cure shrimp diseases. Exiguobacterium arabatum W‐01, a gram‐positive and orange‐pigmented bacterium, was isolated from the intestine of a healthy Penaeus vannamei specimen. Whole‐genome sequencing revealed a genome of 2,914,854 bp, with 48.02% GC content. In total, 3,083 open reading frames (ORFs) were identified, with an average length of 843.98 bp and a mean GC content of 48.11%, accounting for 89.27% of the genome. Among these ORFs, 2,884 (93.5%) genes were classified into Clusters of Orthologous Groups (COG) families comprising 21 functional categories, and 1,650 ORFs were classified into 83 functional Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways. A total of 27 rRNA operons and 68 tRNAs were identified, with all 20 amino acids represented. In addition, 91 genomic islands, 68 potential prophages, and 33 tandem repeats, but no clustered regularly interspaced short palindromic repeats (CRISPRs), were found. No resistance genes and only one virulence gene were identified. Among the 150 secreted proteins of E. arabatum W‐01, a variety of transport system substrate‐binding proteins, enzymes, and biosynthetic proteins, which play important roles in the uptake and metabolism of nutrients, were found. Two adherence‐related protein genes and 31 flagellum‐related protein genes were also identified. Taken together, these results indicate potential probiotic functions for E. arabatum W‐01.

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flrA,flrBandflrCregulate adhesion by controlling the expression of critical virulence genes inVibrio alginolyticus

Cited by 83 publications

References 51 publications

FlrA Represses Transcription of the Biofilm-Associated bpfA Operon in Shewanella putrefaciens

FlrA Represses Transcription of the Biofilm-Associated bpfA Operon in Shewanella putrefaciens

Pumilacidin-Like Lipopeptides Derived from Marine Bacterium Bacillus sp. Strain 176 Suppress the Motility of Vibrio alginolyticus

The complete genome sequence of Exiguobacterium arabatum W‐01 reveals potential probiotic functions

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