Characterization of<i>Caulobacter crescentus</i>response to low temperature and identification of genes involved in freezing resistance

Mazzon, Ricardo Ruiz; Lang, Elza A. S.; Braz, Vânia Santos; Marques, Marilis V.

doi:10.1111/j.1574-6968.2008.01337.x

Cited by 21 publications

(19 citation statements)

References 46 publications

(54 reference statements)

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“…crescentus was previously identified as necessary for freezing resistance following disruption of this gene with a mini-Tn 5 insertion (29), indicating that the RNA helicase RhlE is important for low-temperature adaptation, while the RhlB helicase was shown to be part of the RNA degradosome (28). In order to evaluate the roles of both enzymes in cell growth under this condition, a deletion mutant for the rhlB gene was constructed and combined with the rhlE knockout to generate an rhlE rhlB double mutant strain.…”

Section: Resultsmentioning

confidence: 99%

“…The fragments were digested with ApaI and BamHI (upstream fragment) and BamHI and EcoRI (downstream fragment) and cloned in tandem in pNPTS138 suicide vector (M. R. K. Alley, unpublished data) digested ApaI and EcoRI. To generate the rhlB rhlE double mutant, the rhlE ::mini-Tn 5 mutation from clone 30-10H (29) was transduced with phage ϕCr30 (54) into the MM50 strain. In order to warrant a similar genetic background, the mutation was also moved by transduction into a fresh NA1000 strain.…”

Section: Methodsmentioning

confidence: 99%

“…In previous work, we showed that a transposon insertion into rhlE caused C. crescentus to become deficient in growth at low temperature and freezing survival (29), indicating that this helicase may have a role in stress response. Additionally, saturating transposon mutagenesis in the C.…”

Section: Introductionmentioning

confidence: 99%

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Association of the Cold Shock DEAD-Box RNA Helicase RhlE to the RNA Degradosome in Caulobacter crescentus

et al. 2017

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In diverse bacterial lineages, multienzyme assemblies have evolved that are central elements of RNA metabolism and RNA-mediated regulation. The aquatic Gram-negative bacterium Caulobacter crescentus, which has been a model system for studying the bacterial cell cycle, has an RNA degradosome assembly that is formed by the endoribonuclease RNase E and includes the DEAD-box RNA helicase RhlB. Immunoprecipitations of extracts from cells expressing an epitope-tagged RNase E reveal that RhlE, another member of the DEAD-box helicase family, associates with the degradosome at temperatures below those optimum for growth. Phenotype analyses of rhlE, rhlB, and rhlE rhlB mutant strains show that RhlE is important for cell fitness at low temperature and its role may not be substituted by RhlB. Transcriptional and translational fusions of rhlE to the lacZ reporter gene and immunoblot analysis of an epitope-tagged RhlE indicate that its expression is induced upon temperature decrease, mainly through posttranscriptional regulation. RNase E pulldown assays show that other proteins, including the transcription termination factor Rho, a second DEAD-box RNA helicase, and ribosomal protein S1, also associate with the degradosome at low temperature. The results suggest that the RNA degradosome assembly can be remodeled with environmental change to alter its repertoire of helicases and other accessory proteins.IMPORTANCE DEAD-box RNA helicases are often present in the RNA degradosome complex, helping unwind secondary structures to facilitate degradation. Caulobacter crescentus is an interesting organism to investigate degradosome remodeling with change in temperature, because it thrives in freshwater bodies and withstands low temperature. In this study, we show that at low temperature, the cold-induced DEAD-box RNA helicase RhlE is recruited to the RNA degradosome, along with other helicases and the Rho protein. RhlE is essential for bacterial fitness at low temperature, and its function may not be complemented by RhlB, although RhlE is able to complement for rhlB loss. These results suggest that RhlE has a specific role in the degradosome at low temperature, potentially improving adaptation to this condition.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Association of the Cold Shock DEAD-Box RNA Helicase RhlE to the RNA Degradosome in Caulobacter crescentus

et al. 2017

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“…For example, strain K31 adapted to a low-oxygen groundwater habitat was found to degrade chlorophenol in cold groundwater [33]. In particular, Caulobacter exists in ubiquitous nutrient-poor (“oligotrophic”) habitats, some species are even resistant to freezing [34]. Moreover, Caulobacter cells can produces adhesive stalks and attach themselves together that enhance nutrient uptake and biofilm formation [35].…”

Section: Discussionmentioning

confidence: 99%

Crude Oil Treatment Leads to Shift of Bacterial Communities in Soils from the Deep Active Layer and Upper Permafrost along the China-Russia Crude Oil Pipeline Route

Yang

Zhao

et al. 2014

PLoS ONE

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The buried China-Russia Crude Oil Pipeline (CRCOP) across the permafrost-associated cold ecosystem in northeastern China carries a risk of contamination to the deep active layers and upper permafrost in case of accidental rupture of the embedded pipeline or migration of oil spills. As many soil microbes are capable of degrading petroleum, knowledge about the intrinsic degraders and the microbial dynamics in the deep subsurface could extend our understanding of the application of in-situ bioremediation. In this study, an experiment was conducted to investigate the bacterial communities in response to simulated contamination to deep soil samples by using 454 pyrosequencing amplicons. The result showed that bacterial diversity was reduced after 8-weeks contamination. A shift in bacterial community composition was apparent in crude oil-amended soils with Proteobacteria (esp. α-subdivision) being the dominant phylum, together with Actinobacteria and Firmicutes. The contamination led to enrichment of indigenous bacterial taxa like Novosphingobium, Sphingobium, Caulobacter, Phenylobacterium, Alicylobacillus and Arthrobacter, which are generally capable of degrading polycyclic aromatic hydrocarbons (PAHs). The community shift highlighted the resilience of PAH degraders and their potential for in-situ degradation of crude oil under favorable conditions in the deep soils.

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“…Caulobacter crescentus is a free-living and oligotrophic alphaproteobacterium widespread in aquatic environments and able to grow at temperatures as low as 4°C, and it shows an outstanding resistance to freezing (33). The C. crescentus genome contains four paralogues of csp genes, two of them (cspA and cspB) being cold induced, encoding proteins containing a single cold shock domain (CSD), and the other two (cspC and cspD) being stationary phase induced, encoding proteins with two CSDs (4,31).…”

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confidence: 99%

Cold Shock Genes cspA and cspB from Caulobacter crescentus Are Posttranscriptionally Regulated and Important for Cold Adaptation

et al. 2012

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Cold shock proteins (CSPs) are nucleic acid binding chaperones, first described as being induced to solve the problem of mRNA stabilization after temperature downshift. Caulobacter crescentus has four CSPs: CspA and CspB, which are cold induced, and CspC and CspD, which are induced only in stationary phase. In this work we have determined that the synthesis of both CspA and CspB reaches the maximum levels early in the acclimation phase. The deletion of cspA causes a decrease in growth at low temperature, whereas the strain with a deletion of cspB has a very subtle and transient cold-related growth phenotype. The cspA cspB double mutant has a slightly more severe phenotype than that of the cspA mutant, suggesting that although CspA may be more important to cold adaptation than CspB, both proteins have a role in this process. Gene expression analyses were carried out using cspA and cspB regulatory fusions to the lacZ reporter gene and showed that both genes are regulated at the transcriptional and posttranscriptional levels. Deletion mapping of the long 5=-untranslated region (5=-UTR) of each gene identified a common region important for cold induction, probably via translation enhancement. In contrast to what was reported for other bacteria, these cold shock genes have no regulatory regions downstream from ATG that are important for cold induction. This work shows that the importance of CspA and CspB to C. crescentus cold adaptation, mechanisms of regulation, and pattern of expression during the acclimation phase apparently differs in many aspects from what has been described so far for other bacteria.

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Characterization ofCaulobacter crescentusresponse to low temperature and identification of genes involved in freezing resistance

Cited by 21 publications

References 46 publications

Association of the Cold Shock DEAD-Box RNA Helicase RhlE to the RNA Degradosome in Caulobacter crescentus

Association of the Cold Shock DEAD-Box RNA Helicase RhlE to the RNA Degradosome in Caulobacter crescentus

Crude Oil Treatment Leads to Shift of Bacterial Communities in Soils from the Deep Active Layer and Upper Permafrost along the China-Russia Crude Oil Pipeline Route

Cold Shock Genes cspA and cspB from Caulobacter crescentus Are Posttranscriptionally Regulated and Important for Cold Adaptation

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