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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Microbiology".

Deadline for manuscript submissions: closed (30 October 2022) | Viewed by 19449

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Dr. Jean-Christophe Marvaud

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Guest Editor

Institut Micalis, Université Paris-Saclay, INRAE, AgroParisTech, 91400 Orsay, France
Interests: host-bacteria interaction; flagella; innate immune response; antibiotic resistance; bacterial toxins; non-coding RNAs
Special Issues, Collections and Topics in MDPI journals

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Dear Colleagues,

Flagella are complex and fascinating structures that allow bacteria to swim in liquid environments or to swarm on soft and moist surfaces.

To colonize hospitable environments, bacteria use chemotaxis, which is a strategy of reorientation that was first described in the peritrichously flagellated Escherichia coli; it is also known as the run–tumble motility strategy. When signaling pathways respond to stimuli, a transient reversal of the rotary direction of the flagellar motors is performed, leading to the reorientation of the cell body. With diversity among bacteria for the number, position, and shape of flagella, different modes of mobility, including flicking and wrapping, were found recently, and incentivize the analysis of the relationship between flagellar architecture and resulting motility patterns. Moreover, the synthesis and functioning of flagella are very expensive for bacteria; highly regulated gene expression by environmental conditions is observed and is an important area of research on flagella.

Flagella are also considered to be a critical virulence factor for pathogenic bacteria, with examples of host cell adhesion, entrance, and biofilm formation; studies in this area are essential to decipher the host–pathogen relationship. Finally, studies on the use of flagella as a vaccine adjuvant or as a target for vaccine in addition to studies about flagellotropic bacteriophages are important to evaluate particularly potent antibacterial therapies.

This Special Issue on bacterial flagella welcomes original results or reviews on all those various areas of basic and application-oriented research.

Dr. Jean-Christophe Marvaud
Guest Editor

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Keywords

flagellar structure
flagellar assembly
flagellar gene regulation
chemotaxis
motility
vaccine adjuvant
flagellotropic bacteriophage

Related Special Issue

Flagella 2.0 in International Journal of Molecular Sciences (6 articles)

Published Papers (9 papers)

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16 pages, 2623 KiB

Open AccessArticle

Flagellar Phenotypes Impact on Bacterial Transport and Deposition Behavior in Porous Media: Case of Salmonella enterica Serovar Typhimurium

by Xin Zheng, Hongjuan Bai, Ye Tao, Mounia Achak, Yannick Rossez and Edvina Lamy

Int. J. Mol. Sci. 2022, 23(22), 14460; https://doi.org/10.3390/ijms232214460 - 21 Nov 2022

Cited by 2 | Viewed by 1301

Abstract

Bacterial contamination of groundwater has always been an ecological problem worthy of attention. In this study, Salmonella enterica serovar Typhimurium with different flagellar phenotypes mainly characterized during host-pathogen interaction were analyzed for their transport and deposition behavior in porous media. Column transport experiments and a modified mobile-immobile model were applicated on different strains with flagellar motility (wild-type) or without motility (ΔmotAB), without flagella (ΔflgKL), methylated and unmethylated flagellin (ΔfliB), and different flagella phases (fliC^ON, fljB^ON). Results showed that flagella motility could promote bacterial transport and deposition due to their biological advantages of moving and attaching to surfaces. We also found that the presence of non-motile flagella improved bacterial adhesion according to a higher retention rate of the ΔmotAB strain compared to the ΔflgKL strain. This indicated that bacteria flagella and motility both had promoting effects on bacterial deposition in sandy porous media. Flagella phases influenced the bacterial movement; the fliC^ON strain went faster through the column than the fljB^ON strain. Moreover, flagella methylation was found to favor bacterial transport and deposition. Overall, flagellar modifications affect Salmonella enterica serovar Typhimurium transport and deposition behavior in different ways in environmental conditions. Full article

(This article belongs to the Special Issue Flagella)

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16 pages, 2971 KiB

Open AccessArticle

The Assembly of Flagella in Enteropathogenic Escherichia coli Requires the Presence of a Functional Type III Secretion System

by Jorge Soria-Bustos, Zeus Saldaña-Ahuactzi, Partha Samadder, Jorge A. Yañez-Santos, Ygnacio Martínez Laguna, María L. Cedillo-Ramírez and Jorge A. Girón

Int. J. Mol. Sci. 2022, 23(22), 13705; https://doi.org/10.3390/ijms232213705 - 08 Nov 2022

Cited by 3 | Viewed by 2153

Abstract

In enteropathogenic Escherichia coli (EPEC), the production of flagella and the type III secretion system (T3SS) is activated in the presence of host cultured epithelial cells. The goal of this study was to investigate the relationship between expression of flagella and the T3SS. Mutants deficient in assembling T3SS basal and translocon components (ΔespA, ΔespB, ΔespD, ΔescC, ΔescN, and ΔescV), and in secreting effector molecules (ΔsepD and ΔsepL) were tested for flagella production under several growth conditions. The ΔespA mutant did not produce flagella in any condition tested, although fliC was transcribed. The remaining mutants produced different levels of flagella upon growth in LB or in the presence of cells but were significantly diminished in flagella production after growth in Dulbecco’s minimal essential medium. We also investigated the role of virulence and global regulator genes in expression of flagella. The ΔqseB and ΔqseC mutants produced abundant flagella only when growing in LB and in the presence of HeLa cells, indicating that QseB and QseC act as negative regulators of fliC transcription. The ΔgrlR, ΔperA, Δler, Δhns, and Δfis mutants produced low levels of flagella, suggesting these regulators are activators of fliC expression. These data suggest that the presence of an intact T3SS is required for assembly of flagella highlighting the existence in EPEC of a cross-talk between these two virulence-associated T3SSs. Full article

(This article belongs to the Special Issue Flagella)

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16 pages, 3180 KiB

Open AccessArticle

Clostridioides difficile Flagellin Activates the Intracellular NLRC4 Inflammasome

by Hiba Chebly, Jean-Christophe Marvaud, Layale Safa, Assem Khalil Elkak, Philippe Hussein Kobeissy, Imad Kansau and Cécile Larrazet

Int. J. Mol. Sci. 2022, 23(20), 12366; https://doi.org/10.3390/ijms232012366 - 15 Oct 2022

Cited by 4 | Viewed by 2228

Abstract

Clostridioides difficile (C. difficile), is a major cause of nosocomial diarrhea and colitis. C. difficile flagellin FliC contributes toxins to gut inflammation by interacting with the immune Toll-like receptor 5 (TLR5) to activate nuclear factor-kappa B (NF-kB) and mitogen-activated protein kinase (MAPK) signaling pathways. Flagella of intracellular pathogens can activate the NLR family CARD domain-containing protein 4 (NLRC4) inflammasome pathway. In this study, we assessed whether flagellin of the extracellular bacterium C. difficile internalizes into epithelial cells and activates the NLRC4 inflammasome. Confocal microscopy showed internalization of recombinant green fluorescent protein (GFP)-FliC into intestinal Caco-2/TC7 cell line. Full-length GFP-FliC activates NLRC4 in Caco-2/TC7 cells in contrast to truncated GFP-FliC lacking the C-terminal region recognized by the inflammasome. FliC induced cleavage of pro-caspase-1 into two subunits, p20 and p10 as well as gasdermin D (GSDMD), suggesting the caspase-1 and NLRC4 inflammasome activation. In addition, colocalization of GFP-FliC and pro-caspase-1 was observed, indicating the FliC-dependent NLRC4 inflammasome activation. Overexpression of the inflammasome-related interleukin (interleukin (IL)-1β, IL-18, and IL-33) encoding genes as well as increasing of the IL-18 synthesis was detected after cell stimulation. Inhibition of I-kappa-B kinase alpha (IKK-α) decreased the FliC-dependent inflammasome interleukin gene expression suggesting a role of the NF-κB pathway in regulating inflammasome. Altogether, these results suggest that FliC internalizes into the Caco-2/TC7 cells and activates the intracellular NLRC4 inflammasome thus contributing to the inflammatory process of C. difficile infection. Full article

(This article belongs to the Special Issue Flagella)

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19 pages, 2208 KiB

Open AccessArticle

A Tripartite Efflux System Affects Flagellum Stability in Helicobacter pylori

by Katherine Gibson, Joshua K. Chu, Shiwei Zhu, Doreen Nguyen, Jan Mrázek, Jun Liu and Timothy R. Hoover

Int. J. Mol. Sci. 2022, 23(19), 11609; https://doi.org/10.3390/ijms231911609 - 01 Oct 2022

Cited by 2 | Viewed by 1651

Abstract

Helicobacter pylori uses a cluster of polar, sheathed flagella for swimming motility. A search for homologs of H. pylori proteins that were conserved in Helicobacter species that possess flagellar sheaths but were underrepresented in Helicobacter species with unsheathed flagella identified several candidate proteins. Four of the identified proteins are predicted to form part of a tripartite efflux system that includes two transmembrane domains of an ABC transporter (HP1487 and HP1486), a periplasmic membrane fusion protein (HP1488), and a TolC-like outer membrane efflux protein (HP1489). Deleting hp1486/hp1487 and hp1489 homologs in H. pylori B128 resulted in reductions in motility and the number of flagella per cell. Cryo-electron tomography studies of intact motors of the Δhp1489 and Δhp1486/hp1487 mutants revealed many of the cells contained a potential flagellum disassembly product consisting of decorated L and P rings, which has been reported in other bacteria. Aberrant motors lacking specific components, including a cage-like structure that surrounds the motor, were also observed in the Δhp1489 mutant. These findings suggest a role for the H. pylori HP1486-HP1489 tripartite efflux system in flagellum stability. Three independent variants of the Δhp1486/hp1487 mutant with enhanced motility were isolated. All three motile variants had the same frameshift mutation in fliL, suggesting a role for FliL in flagellum disassembly. Full article

(This article belongs to the Special Issue Flagella)

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16 pages, 3932 KiB

Open AccessArticle

Salmonella Regulator STM0347 Mediates Flagellar Phase Variation via Hin Invertase

by Hongou Wang, Zhiheng Tang, Baoshuai Xue, Qinghui Lu, Xiaoyun Liu and Qinghua Zou

Int. J. Mol. Sci. 2022, 23(15), 8481; https://doi.org/10.3390/ijms23158481 - 30 Jul 2022

Cited by 3 | Viewed by 2375

Abstract

Salmonella enterica is one of the most important food-borne pathogens, whose motility and virulence are highly related to flagella. Flagella alternatively express two kinds of surface antigen flagellin, FliC and FljB, in a phenomenon known as flagellar phase variation. The molecular mechanisms by which the switching orientation of the Hin-composed DNA segment mediates the expression of the fljBA promoter have been thoroughly illustrated. However, the precise regulators that control DNA strand exchange are barely understood. In this study, we found that a putative response regulator, STM0347, contributed to the phase variation of flagellin in S. Typhimurium. With quantitative proteomics and secretome profiling, a lack of STM0347 was confirmed to induce the transformation of flagellin from FliC to FljB. Real-time PCR and in vitro incubation of SMT0347 with the hin DNA segment suggested that STM0347 disturbed Hin-catalyzed DNA reversion via hin degradation, and the overexpression of Hin was sufficient to elicit flagellin variation. Subsequently, the Δstm0347 strain was outcompeted by its parental strain in HeLa cell invasion. Collectively, our results reveal the crucial role of STM0347 in Salmonella virulence and flagellar phase variation and highlight the complexity of the regulatory network of Hin-modulated flagellum phase variation in Salmonella. Full article

(This article belongs to the Special Issue Flagella)

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13 pages, 21569 KiB

Open AccessArticle

Diguanylate Cyclase (DGC) Implicated in the Synthesis of Multiple Bacteriocins via the Flagellar-Type III Secretion System Produced by Pectobacterium carotovorum subsp. carotovorum

by Ruchi Briam James Sersenia Lagitnay, Han-Ling Chen, Yen-Chun Chen and Duen-Yau Chuang

Int. J. Mol. Sci. 2022, 23(10), 5649; https://doi.org/10.3390/ijms23105649 - 18 May 2022

Viewed by 2338

Abstract

The plant pathogen Pectobacterium carotovorum subsp. carotovorum (previously Erwinia carotovora subsp. carotovora) causes soft rot and stem rot diseases in a variety of crops, including Chinese cabbage, potato, and tomato. The flagellar-type III secretion systems were used by Pcc’s virulence mechanism to export proteins or bacteriocins to the outside of the cell. DGC, a virulence factor that cyclizes c-di-GMP, a common secondary signal in physiological processes and toxin control systems of many bacteria, was discovered in Pcc’s genomic DNA. The dgc gene in Pcc was blocked using the method of homologous recombination in our study. In the in vivo setting, the results demonstrated that the dgc knockout strain does not release low molecular weight bacteriocins. The bacteriocin gene (carocin S2, carocin S3, carocin S4) and the flagellar-type III secretion system genes were also unable to be transcribed by the dgc knockout strain in the transcription experiment. We also observed that the amount of bacteriocin expressed changed when the amount of L-glutamine in the environment exceeded a particular level. These data suggested that L-glutamine influenced physiological processes in Pcc strains in some way. We hypothesized a relationship between dgc and the genes involved in Pcc LMWB external export via the flagellar-type secretion system based on these findings. In this study, the current findings led us to propose a mechanism in which DGC’s cyclic di-GMP might bind to receptor proteins and positively regulate bacteriocin transcription as well as the synthesis, mobility, and transport of toxins. Full article

(This article belongs to the Special Issue Flagella)

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14 pages, 3039 KiB

Open AccessArticle

Molecular Characterization of Three Tandemly Located Flagellin Genes of Stenotrophomonas maltophilia

by Cheng-Mu Wu, Hsin-Hui Huang, Li-Hua Li, Yi-Tsung Lin and Tsuey-Ching Yang

Int. J. Mol. Sci. 2022, 23(7), 3863; https://doi.org/10.3390/ijms23073863 - 31 Mar 2022

Cited by 6 | Viewed by 1758

Abstract

Stenotrophomonas maltophilia is a motile, opportunistic pathogen. The flagellum, which is involved in swimming, swarming, adhesion, and biofilm formation, is considered a virulence factor for motile pathogens. Three flagellin genes, fliC1, fliC2, and fliC3, were identified from the sequenced S. maltophilia genome. FliC1, fliC2, and fliC3 formed an operon, and their encoding proteins shared 67–82% identity. Members of the fliC1C2C3 operon were deleted individually or in combination to generate single mutants, double mutants, and a triple mutant. The contributions of the three flagellins to swimming, swarming, flagellum morphology, adhesion, and biofilm formation were assessed. The single mutants generally had a compromise in swimming and no significant defects in swarming, adhesion on biotic surfaces, and biofilm formation on abiotic surfaces. The double mutants displayed obvious defects in swimming and adhesion on abiotic and biotic surfaces. The flagellin-null mutant lost swimming ability and was compromised in adhesion and biofilm formation. All tested mutants demonstrated substantial but different flagellar morphologies, supporting that flagellin composition affects filament morphology. Bacterial swimming motility was significantly compromised under an oxidative stress condition, irrespective of flagellin composition. Collectively, the utilization of these three flagellins for filament assembly equips S. maltophilia with flagella adapted to provide better ability in swimming, adhesion, and biofilm formation for its pathogenesis. Full article

(This article belongs to the Special Issue Flagella)

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23 pages, 708 KiB

Open AccessReview

Flagellotropic Bacteriophages: Opportunities and Challenges for Antimicrobial Applications

by Nathaniel C. Esteves and Birgit E. Scharf

Int. J. Mol. Sci. 2022, 23(13), 7084; https://doi.org/10.3390/ijms23137084 - 25 Jun 2022

Cited by 14 | Viewed by 2831

Abstract

Bacteriophages (phages) are the most abundant biological entities in the biosphere. As viruses that solely infect bacteria, phages have myriad healthcare and agricultural applications including phage therapy and antibacterial treatments in the foodservice industry. Phage therapy has been explored since the turn of the twentieth century but was no longer prioritized following the invention of antibiotics. As we approach a post-antibiotic society, phage therapy research has experienced a significant resurgence for the use of phages against antibiotic-resistant bacteria, a growing concern in modern medicine. Phages are extraordinarily diverse, as are their host receptor targets. Flagellotropic (flagellum-dependent) phages begin their infection cycle by attaching to the flagellum of their motile host, although the later stages of the infection process of most of these phages remain elusive. Flagella are helical appendages required for swimming and swarming motility and are also of great importance for virulence in many pathogenic bacteria of clinical relevance. Not only is bacterial motility itself frequently important for virulence, as it allows pathogenic bacteria to move toward their host and find nutrients more effectively, but flagella can also serve additional functions including mediating bacterial adhesion to surfaces. Flagella are also a potent antigen recognized by the human immune system. Phages utilizing the flagellum for infections are of particular interest due to the unique evolutionary tradeoff they force upon their hosts: by downregulating or abolishing motility to escape infection by a flagellotropic phage, a pathogenic bacterium would also likely attenuate its virulence. This factor may lead to flagellotropic phages becoming especially potent antibacterial agents. This review outlines past, present, and future research of flagellotropic phages, including their molecular mechanisms of infection and potential future applications. Full article

(This article belongs to the Special Issue Flagella)

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10 pages, 1576 KiB

Open AccessBrief Report

Naïve CD4⁺ T Cell Activation in the Nasal-Associated Lymphoid Tissue following Intranasal Immunization with a Flagellin-Based Subunit Vaccine

by John T. Bates

Int. J. Mol. Sci. 2022, 23(24), 15572; https://doi.org/10.3390/ijms232415572 - 08 Dec 2022

Viewed by 1346

Abstract

The nasal-associated lymphoid tissues (NALT) are generally accepted as an immune induction site, but the activation of naïve T-cells in that compartment has not been well-characterized. I wanted to determine if early events in naïve CD4⁺ T cell activation and the extent of antigen specific cell division are similar in NALT to that observed in other secondary lymphoid compartments. I performed antigen tracking experiments and analyzed the activation of naïve antigen-specific CD4⁺ T cells in the nasal-associated lymphoid tissues (NALT). I directly observed transepithelial transport of fluorescently labeled antigen from the lumen of the airway to the interior of the NALT two hours following immunization. One day following intranasal (i.n.) immunization with antigen and adjuvant, antigen-specific CD4⁺ T cells in the NALT associated as clusters, while antigen-specific CD4⁺ T cells in control mice immunized with adjuvant only remained dispersed. The antigen-specific CD4⁺ populations in the NALT and cranial deep cervical lymph nodes of immunized mice expanded significantly by day three following immunization. These findings are consistent with initial activation of naïve CD4⁺ T cells in the NALT and offer insight into adjuvant mechanism of flagellin in the upper respiratory compartment. Full article

(This article belongs to the Special Issue Flagella)

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