DEAD-Box RNA Helicases in Bacillus subtilis Have Multiple Functions and Act Independently from Each Other

Lehnik-Habrink, Martin; Rempeters, Leonie; Kovács, Ákos T.; Wrede, Christoph; Baierlein, Claudia; Krebber, Heike; Kuipers, Oscar P.; Stülke, Jörg

doi:10.1128/jb.01475-12

Cited by 67 publications

(82 citation statements)

References 61 publications

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“…In the case of LicT, the localization determinants are unknown. Interestingly, LicT active in transcriptional antitermination localizes to the same regions of the cell as the ribosomes (43,44). Given the coupling between transcription and translation in bacteria, it is tempting to speculate that the RNA molecules to which LicT binds recruit the protein to the subpolar regions of the cell.…”

Section: Discussionmentioning

confidence: 99%

Dynamic Localization of a Transcription Factor in Bacillus subtilis: the LicT Antiterminator Relocalizes in Response to Inducer Availability

et al. 2013

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Bacillus subtilis transports ␤-glucosides such as salicin by a dedicated phosphotransferase system (PTS). The expression of the ␤-glucoside permease BglP is induced in the presence of the substrate salicin, and this induction requires the binding of the antiterminator protein LicT to a specific RNA target in the 5= region of the bglP mRNA to prevent the formation of a transcription terminator. LicT is composed of an N-terminal RNA-binding domain and two consecutive PTS regulation domains, PRD1 and PRD2. In the absence of salicin, LicT is phosphorylated on PRD1 by BglP and thereby inactivated. In the presence of the inducer, the phosphate group from PRD1 is transferred back to BglP and consequently to the incoming substrate, resulting in the activation of LicT. In this study, we have investigated the intracellular localization of LicT. While the protein was evenly distributed in the cell in the absence of the inducer, we observed a subpolar localization of LicT if salicin was present in the medium. Upon addition or removal of the inducer, LicT rapidly relocalized in the cells. This dynamic relocalization did not depend on the binding of LicT to its RNA target sites, since the localization pattern was not affected by deletion of all LicT binding sites. In contrast, experiments with mutants affected in the PTS components as well as mutations of the LicT phosphorylation sites revealed that phosphorylation of LicT by the PTS components plays a major role in the control of the subcellular localization of this RNAbinding transcription factor.

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Section: Discussionmentioning

confidence: 99%

Dynamic Localization of a Transcription Factor in Bacillus subtilis: the LicT Antiterminator Relocalizes in Response to Inducer Availability

et al. 2013

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“…DEAD box RNA helicases are ubiquitous enzymes that participate in all aspects of RNA metabolism (7). While eukaryotes generally encode numerous DEAD box RNA helicases, 25 in yeast (8) and over 50 in Arabidopsis (9), prokaryotic genomes encode fewer members, 5 in E. coli (10) and 4 in B. subtilis (11). Structurally, RNA helicases consist of two tandem RecA-like helicase domains with N-terminal and/or C-terminal extensions that provide substrate and protein interaction domains (7).…”

Section: Importancementioning

confidence: 99%

Cyanobacterial RNA Helicase CrhR Localizes to the Thylakoid Membrane Region and Cosediments with Degradosome and Polysome Complexes in Synechocystis sp. Strain PCC 6803

et al. 2016

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The cyanobacterium Synechocystis sp. strain PCC 6803 encodes a single DEAD box RNA helicase, CrhR, whose expression is tightly autoregulated in response to cold stress. Subcellular localization and proteomic analysis results indicate that CrhR localizes to both the cytoplasmic and thylakoid membrane regions and cosediments with polysome and RNA degradosome components. Evidence is presented that either functional RNA helicase activity or a C-terminal localization signal was required for polysome but not thylakoid membrane localization. Polysome fractionation and runoff translation analysis results indicate that CrhR associates with actively translating polysomes. The data implicate a role for CrhR in translation or RNA degradation in the thylakoid region related to thylakoid biogenesis or stability, a role that is enhanced at low temperature. Furthermore, CrhR cosedimentation with polysome and RNA degradosome complexes links alteration of RNA secondary structure with a potential translation-RNA degradation complex in Synechocystis. IMPORTANCEThe interaction between mRNA translation and degradation is a major determinant controlling gene expression. Regulation of RNA function by alteration of secondary structure by RNA helicases performs crucial roles, not only in both of these processes but also in all aspects of RNA metabolism. Here, we provide evidence that the cyanobacterial RNA helicase CrhR localizes to both the cytoplasmic and thylakoid membrane regions and cosediments with actively translating polysomes and RNA degradosome components. These findings link RNA helicase alteration of RNA secondary structure with translation and RNA degradation in prokaryotic systems and contribute to the data supporting the idea of the existence of a macromolecular machine catalyzing these reactions in prokaryotic systems, an association hitherto recognized only in archaea and eukarya. C ompartmentalization of metabolic processes is crucial for cells to avoid futile cycles. While this is efficiently achieved by lipid bilayers in eukaryotic cells, this solution does not generally apply in prokaryotes. Although prokaryotes have the ability to compartmentalize using invagination of the inner cell membrane, these compartments, for example, magnetosomes, tend to perform one specific function and are not widely used (1). Prokaryotes can also form proteinaceous microcompartments in which specific reactions occur, the primary cyanobacterial example being that of carboxysomes (2). Prokaryotes do not compartmentalize routine, everyday anabolic and catabolic processes such as transcription and translation or protein and RNA decay; however, there is a growing body of evidence indicating that prokaryotes spatially confine these cellular processes (3). A prime example is the localization of the RNA degradation complex, the degradosome, to the cytoplasmic membrane (CM) in Escherichia coli (4) and Bacillus subtilis (5).The E. coli degradosome consists of RNase E, polynucleotide phosphorylase (PNPase), enolase, and the DEAD box RNA he...

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“…However, fluctuating temperature may be a stressful condition encountered by A. veronii during transition from the host to the mucus. A number of genes enriched and overexpressed in the mucosal environment were related to heat shock, such as dnaK (50), as well as functions within colder environments, such as deaD and rhlE (48,59; reviewed in reference 49). This indicates that A. veronii is likely experiencing fluctuations in temperature not observed in the gut or monoculture environments, which is a reasonable conclusion as the monoculture was maintained at a steady 30°C (31).…”

Section: Discussionmentioning

confidence: 99%

“…For example, the ATP-dependent helicases DeaD and RhlE ( Fig. 2D and E) are known as DEAD box RNA helicases and are involved in various cell processes at lower temperatures, such as ribosome biogenesis (48), RNA degradation (48), and translation initiation (reviewed in reference 49). Additionally, the chaperone DnaK assists cells with protein folding after a heat shock event (50), indicating that this is associated with thermotolerance, while the chaperone GroEL is useful for the cell to adapt to osmotic stressors and protein misfolds (50).…”

Section: A Veronii Undergoes Transcriptional Tuning Within Differentmentioning

confidence: 99%

A Tale of Transmission: Aeromonas veronii Activity within Leech-Exuded Mucus

Ott

Dacks

Ryan

et al. 2016

Appl Environ Microbiol

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bTransmission, critical to the establishment and persistence of host-associated microbiotas, also exposes symbionts to new environmental conditions. With horizontal transmission, these different conditions represent major lifestyle shifts. Yet genomewide analyses of how microbes adjust their transcriptomes toward these dramatic shifts remain understudied. Here, we provide a comprehensive and comparative analysis of the global transcriptional profiles of a symbiont as it shifts between lifestyles during transmission. The gammaproteobacterium Aeromonas veronii is transmitted from the gut of the medicinal leech to other hosts via host mucosal castings, yet A. veronii can also transition from mucosal habitancy to a free-living lifestyle. These three lifestyles are characterized by distinct physiological constraints and consequently lifestyle-specific changes in the expression of stress-response genes. Mucus-bound A. veronii had the greatest expression in terms of both the number of loci and levels of transcription of stress-response mechanisms. However, these bacteria are still capable of proliferating within the mucus, suggesting the availability of nutrients within this environment. We found that A. veronii alters transcription of loci in a synthetic pathway that obtains and incorporates N-acetylglucosamine (NAG; a major component of mucus) into the bacterial cell wall, enabling proliferation. Our results demonstrate that symbionts undergo dramatic local adaptation, demonstrated by widespread transcriptional changes, throughout the process of transmission that allows them to thrive while they encounter new environments which further shape their ecology and evolution. M utualistic bacteria provide numerous advantages to their eukaryotic hosts, such as the provisioning of essential nutrients (1, 2), protection from pathogens (3, 4), and immunological priming (5). These mutualists also serve as some of the best examples of the extended phenotype (6) by providing opportunities for rapid adaptation and resilience toward dynamic ecological conditions, including broadening the host dietary range via enzymatic activities (reviewed in references 7 and 8), detoxification mechanisms (reviewed in references 9 and 10), or enhancing tolerance to environmental stressors such as fluctuating temperatures (11). Although the persistence of these relations over evolutionary time is crucial for securing adaptive potential, little is known about local adaptation and the activity of symbionts within a transmission setting.Mixed-mode transmission (MMT), integrating components of both vertical and horizontal microbial acquisition, is the predominant mechanism for obtaining microbial symbionts by a host (reviewed in reference 12). A recently described model of MMT involves the acquisition of the heterotrophic Gammaproteobacteria Aeromonas veronii, a predominant member, along with the Bacteroidetes Mucinivorans hirudinis (13, 14), of the European medicinal leech (Hirudo verbana) digestive tract microbiota. Specifically, A. veronii is found ...

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DEAD-Box RNA Helicases in Bacillus subtilis Have Multiple Functions and Act Independently from Each Other

Cited by 67 publications

References 61 publications

Dynamic Localization of a Transcription Factor in Bacillus subtilis: the LicT Antiterminator Relocalizes in Response to Inducer Availability

Dynamic Localization of a Transcription Factor in Bacillus subtilis: the LicT Antiterminator Relocalizes in Response to Inducer Availability

Cyanobacterial RNA Helicase CrhR Localizes to the Thylakoid Membrane Region and Cosediments with Degradosome and Polysome Complexes in Synechocystis sp. Strain PCC 6803

A Tale of Transmission: Aeromonas veronii Activity within Leech-Exuded Mucus

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