Adaptor-mediated Lon proteolysis restricts<i>Bacillus subtilis</i>hyperflagellation

Mukherjee, Sampriti; Bree, Anna C.; Liu, Jing; Patrick, Joyce E.; Chien, Peter; Kearns, Daniel B.

doi:10.1073/pnas.1417419112

Cited by 81 publications

(95 citation statements)

References 55 publications

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“…possesses no SwrA homolog, DegS may be required to produce enough DegUϳP to bind and activate the fla-che operon promoter in Paenibacillus sp. Thus, induction of flagellar genes is mainly controlled by SwrA levels in B. subtilis (12), whereas it may be controlled by DegUϳP levels in Paenibacillus sp. surface structures directly contact the external environment, the WsfP-and PBN151_4312-related regulations are expected to play important roles under surface growth conditions.…”

Section: Resultsmentioning

confidence: 99%

Surface Sensing for Paenibacillus sp. NAIST15-1 Flagellar Gene Expression on Solid Medium

Kobayashi

Kanesaki

Yoshikawa

2017

Appl Environ Microbiol

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A rhizosphere Gram-positive bacterial isolate, Paenibacillus sp. NAIST15-1, exhibits intriguing motility behavior on hard agar medium. Paenibacillus sp. shows increased transcription of flagellar genes and hyperflagellation when transferred from liquid to solid medium. Hyperflagellated cells form wandering colonies that are capable of moving around on the surface of medium containing Ն1.5% agar. Transposon mutagenesis was used to identify genes critical for motility. In addition to flagellar genes, this mutagenesis identified five nonflagellar structural genes that were important for motility. Of these, the disruption of degSU, wsfP, or PBN151_4312 resulted in a complete loss of flagellin synthesis. Analysis of flagellar gene promoter activity showed that each mutation severely reduced flagellar gene transcription in a different manner. Flagellar gene transcription was induced in liquid medium by the addition of a viscous agent, Ficoll, or by disruption of flagellar stator genes, indicating that flagellar gene transcription was induced in response to restriction of flagellar rotation. Overexpression of DegSU bypassed the requirement of flagellar rotation restriction for induction of flagellar genes. These results indicate that physical restriction of flagellar rotation by physical contact with the surface of solid medium induces flagellar gene transcription through the activation of DegSU. Further analysis revealed that the same mechanism was conserved in Bacillus subtilis. These results demonstrate that flagella act as mechanosensors to control flagellar transcription in Gram-positive bacteria.IMPORTANCE Many bacteria exist on living or nonliving surfaces in nature. Bacteria express distinct behaviors, such as surface motility and biofilm formation, to adapt to surfaces. However, it remains largely unknown how bacteria sense the surfaces on which they sit and how they induce the genes needed for growth on a surface. Swarming motility is flagellum-dependent motility on a surface. The Gram-positive bacterium Paenibacillus sp. exhibits strong swarming motility ability and is capable of moving on 1.5% agar medium. In this study, we showed that the two-component system DegSU was responsible for inducing flagellar genes in response to heavy loads on flagellar rotation in Paenibacillus sp. The same mechanism was conserved in a related species, B. subtilis, even though these two bacteria exhibit very different motility behaviors. This study shows that flagellum serves as a sensor for surface contact to induce flagellar gene transcription in these bacteria.KEYWORDS DegSU, Paenibacillus, flagellar rotation, surface sensing, swarming motility, wandering colony B acteria are capable of moving on a variety of surfaces. Swarming motility, which is defined as flagellum-dependent group motility on a solid surface, is observed in diverse bacteria (1-3). Swarming motility is distinct from swimming motility, which is flagellum-dependent movement of planktonic cells grown in an aqueous environment and requires differentia...

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Section: Resultsmentioning

confidence: 99%

Surface Sensing for Paenibacillus sp. NAIST15-1 Flagellar Gene Expression on Solid Medium

Kobayashi

Kanesaki

Yoshikawa

2017

Appl Environ Microbiol

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“…SwrA is the master swarming regulator that accumulates following surface contact. This SwrA accumulation results from a lack of proteolysis by the LonA AAAϩ protease/SmiA adaptor (98). While the exact mechanism that relieves proteolysis of SwrA is under investigation (D. Kearns, unpublished data), this surface contact-controlled transcription regulation allows differentiation into swarmer cells.…”

Section: Surface Sensing and Signal Transductionmentioning

confidence: 99%

Recent Advances and Future Prospects in Bacterial and Archaeal Locomotion and Signal Transduction

et al. 2017

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The structure and function of two-component and chemotactic signaling and different aspects related to the motility of bacteria and archaea are key research areas in modern microbiology. Escherichia coli is the traditional model organism used to study chemotaxis signaling and motility. However, the recent study of a wide range of bacteria and even some archaea with different lifestyles has provided new insight into the ecophysiology of chemotaxis, which is essential for the establishment of different pathogens or beneficial bacteria in a host. The expanded range of model organisms has also permitted the study of chemosensory pathways unrelated to chemotaxis, multiple chemotaxis pathways within an organism, and new types of chemoreceptors. This research has greatly benefitted from technical advances in the field of cryomicroscopy, which continues to reveal with increasing resolution the complexity and diversity of large protein complexes like the flagellar motor or chemoreceptor arrays. In addition, sensitive instruments now allow an increasing number of experiments to be conducted at the single-cell level, thereby revealing information that is beginning to bridge the gap between individual cells and population behavior. Evidence has also accumulated showing that bacteria have evolved different mechanisms for surface sensing, which appears to be mediated by flagella and possibly type IV pili, and that the downstream signaling involves chemosensory pathways and two-component-system-based processes. Herein, we summarize the recent advances and research tendencies in this field as presented at the latest Bacterial Locomotion and Signal Transduction (BLAST XIV) conference.KEYWORDS chemotaxis, flagella, flagellar motility, signal transduction, two-component regulatory systems T he capacity to sense and respond to changes in environmental cues is an essential feature of the prokaryotic lifestyle. As a consequence, bacteria and archaea have evolved an array of different molecular mechanisms that permit the detection of signals in order to generate appropriate cellular responses. These responses are mediated primarily by one-and two-component systems, as well as chemosensory signaling pathways (1-4). Whereas the former systems mediate changes primarily at the transcriptional level, chemosensory pathways form the basis for chemotaxis, the directed movement of prokaryotes in compound gradients. The study of signaling processes is not only of fundamental interest but may also contribute to the tackling of one of the central clinical problems, which is the increasing amount of antibiotic-resistant pathogens. There is now a significant amount of data indicating that interference with signal transduction systems, motility, and chemotaxis can be an alternative strategy to weaken or block pathogens (5, 6).In

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“…It was further shown that LonA-mediated degradation of SwrA happens only in the presence of swarming motility inhibitor A (SmiA). SwrA mutants that were resistant to proteolysis and caused hyperswarming were identified; it was speculated that these mutated residues were required for SmiA interaction (8). Gerard Wong (UCLA, Los Angeles, CA) presented his collaboration with George O'Toole with a surprising finding on surface sensing in Pseudomonas aeruginosa PA14.…”

Section: Bacterial Adhesion Factors and The Planktonic To Biofilm Lifmentioning

confidence: 99%

Biofilms 2015: Multidisciplinary Approaches Shed Light into Microbial Life on Surfaces

et al. 2016

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The 7th ASM Conference on Biofilms was held in Chicago, Illinois, from 24 to 29 October 2015. The conference provided an international forum for biofilm researchers across academic and industry platforms, and from different scientific disciplines, to present and discuss new findings and ideas. The meeting covered a wide range of topics, spanning environmental sciences, applied biology, evolution, ecology, physiology, and molecular biology of the biofilm lifestyle. This report summarizes the presentations with regard to emerging biofilm-related themes.

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Adaptor-mediated Lon proteolysis restrictsBacillus subtilishyperflagellation

Cited by 81 publications

References 55 publications

Surface Sensing for Paenibacillus sp. NAIST15-1 Flagellar Gene Expression on Solid Medium

Surface Sensing for Paenibacillus sp. NAIST15-1 Flagellar Gene Expression on Solid Medium

Recent Advances and Future Prospects in Bacterial and Archaeal Locomotion and Signal Transduction

Biofilms 2015: Multidisciplinary Approaches Shed Light into Microbial Life on Surfaces

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