Property of cold inducible DEAD-box RNA helicase in hyperthermophilic archaea

Shimada, Yôko; Fukuda, Wakao; Akada, Yohei; Ishida, Mayumi; Nakayama, Jun‐ichi; Imanaka, Tadayuki; Fujiwara, Shinsuke

doi:10.1016/j.bbrc.2009.09.038

Cited by 24 publications

(25 citation statements)

References 28 publications

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“…Our previous study revealed that Tk-DeaD unwound singlestrand stem-looped RNA in an ATP-dependent manner in vitro (3).…”

Section: Discussionmentioning

confidence: 99%

“…In archaea, many DEAD box proteins have been identified through genome analysis. DEAD box proteins are induced by cold shock and low-temperature cell growth conditions in the hyperthermophilic archaea T. kodakarensis (3) and Methanocaldococcus jannaschii (8) and in the psychrophilic archaeon Methanococcoides burtonii (9). These findings suggest that the DEAD box RNA helicase in archaea is involved in cell adaptation to cold stress environments.…”

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confidence: 90%

“…In addition to CpkA, T. kodakarensis also possesses a cold-inducible DEAD box RNA helicase (Tk-deaD), an ortholog of which has not been identified in Pyrococcus spp. Tk-DeaD induces unwinding of single-strand stem-looped RNA in an ATP-dependent manner (3). However, the physiological role and mechanism of Tk-DeaD expression in coldtemperature adaptation remains unknown.…”

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confidence: 99%

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Importance and Determinants of Induction of Cold-Induced DEAD RNA Helicase in the Hyperthermophilic Archaeon Thermococcus kodakarensis

et al. 2013

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c Thermococcus kodakarensis, which grows optimally at 85°C, expresses cold stress-inducible DEAD box RNA helicase (Tk-deaD) when shifted to 60°C. A DDA1 deletion (⌬Tk-deaD) mutant exhibited decreased cell growth, and cells underwent lysis at 60°C in nutrient broth in the absence of elemental sulfur. In contrast, cells in medium containing elemental sulfur at 60°C did not undergo lysis, suggesting that Tk-deaD is necessary for cell growth in sulfur-free medium. To identify the element responsible for the cold response, a pTKR expression probe plasmid was constructed using thermostable catalase from Pyrobaculum calidifontis as a reporter. The plasmid pTKRD, which contained the transcription factor B recognition element, TATA region, and ShineDalgarno (SD) region, including the initiation codon of the Tk-deaD gene, exhibited cold inducibility. We also constructed a series of deletion and chimeric constructs with the glutamate dehydrogenase (gdh) promoter, whose expression is constitutive independent of culture temperatures and catalase expression. Reporter assay experiments indicated that the regulatory element is located in the region between the SD region and the initiation codon (ATG). Nucleotide sequences in the upstream regions of Tk-deaD and gdh were compared and revealed a five-adenosine (AAAAA) sequence between SD and ATG of Tk-deaD that was not present in gdh. Replacement of the repeated adenosine sequence with other sequences revealed that the AAAAA sequence is important for cold induction. This sequence-specific mechanism is unique and is one that has not been identified in other known cold-inducible genes. Ahyperthermophile is an organism that thrives at temperatures of 80°C or higher. On the universal phylogenetic tree based on 16S rRNA, hyperthermophiles are located near the root and are deeply branching (1), which suggests that they are highly primitive microorganisms and that their descendants evolved by adapting to cooler environments. Hence, study of the adaptive mechanisms of hyperthermophiles to cold environments may provide insight into evolutionary processes. When we compared the range of growth temperatures among (hyper)thermophilic archaea, a significant difference was observed in the lower-limit temperatures that appeared to be dependent on the expression of unique genes (1). For example, in the Thermococcales order, the cold-inducible chaperonin CpkA in Thermococcus kodakarensis was identified, but no ortholog of cpkA was identified in closely related Pyrococcus sp. strains, which grow at higher temperatures (2). A gene knockout study also revealed that cpkA disruption resulted in poor cell growth at cold stress temperatures but had no significant effect at optimum and higher growth temperatures. These results strongly suggest that cold-inducible proteins make adaptation possible for hyperthermophilic archaea under cold stress conditions. In addition to CpkA, T. kodakarensis also possesses a cold-inducible DEAD box RNA helicase (Tk-deaD), an ortholog of which has not been identified in Pyr...

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“…Our previous study revealed that Tk-DeaD unwound singlestrand stem-looped RNA in an ATP-dependent manner in vitro (3).…”

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 90%

mentioning

confidence: 99%

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Importance and Determinants of Induction of Cold-Induced DEAD RNA Helicase in the Hyperthermophilic Archaeon Thermococcus kodakarensis

et al. 2013

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“…This archaeon grows at temperatures between 60°C and 100°C but optimally at 85°C. Under low-or high-temperature-stressed conditions, T. kodakarensis produces cold-or heat-inducible chaperones to adapt to unfavorable growth environments (4,5,30). The lipid composition of the membrane also changes depending on the growth shift (20).…”

Section: (Pathway Ii)mentioning

confidence: 99%

Dual Biosynthesis Pathway for Longer-Chain Polyamines in the Hyperthermophilic Archaeon Thermococcus kodakarensis

et al. 2010

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The open reading frames (ORFs) TK0240, TK0474, and TK0882, annotated as agmatine ureohydrolase genes, were disrupted. Only the TK0882 gene disruptant showed a growth defect at 85°C and 93°C, and the growth was partially retrieved by the addition of spermidine. In the TK0882 gene disruptant, agmatine and N 1 -aminopropylagmatine accumulated in the cytoplasm. Recombinant TK0882 was purified to homogeneity, and its ureohydrolase characteristics were examined. It possessed a 43-fold-higher k cat /K m value for N 1 -aminopropylagmatine than for agmatine, suggesting that TK0882 functions mainly as N 1 -aminopropylagmatine ureohydrolase to produce spermidine. TK0147, annotated as spermidine/spermine synthase, was also studied. The TK0147 gene disruptant showed a remarkable growth defect at 85°C and 93°C. Moreover, large amounts of agmatine but smaller amounts of putrescine accumulated in the disruptant. Purified recombinant TK0147 possessed a 78-fold-higher k cat /K m value for agmatine than for putrescine, suggesting that TK0147 functions primarily as an aminopropyl transferase to produce N 1 -aminopropylagmatine. In T. kodakarensis, spermidine is produced mainly from agmatine via N 1 -aminopropylagmatine. Furthermore, spermine and N 4 -aminopropylspermine were detected in the TK0147 disruptant, indicating that TK0147 does not function to produce spermine and long-chain polyamines.

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“…Factors such as DEAD box helicases (27), prefoldins (4), and membrane components (21) are thought to be involved in the ability of this organism to adapt to such wide temperature ranges. Apart from such factors, T. kodakarensis possesses a unique cold-inducible chaperonin, CpkA, in addition to a conventional heat-inducible one, CpkB (8,13).…”

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Indole-3-Glycerol-Phosphate Synthase Is Recognized by a Cold-Inducible Group II Chaperonin in Thermococcus kodakarensis

Gao

Danno

Fujii

et al. 2012

Appl Environ Microbiol

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ABSTRACTThermococcus kodakarensisoptimally grows at 85°C and possesses two chaperonins, cold-inducible CpkA and heat-inducible CpkB. Gene disruptants DA1 (ΔcpkA) and DB1 (ΔcpkB) showed decreased cell growth at 60°C and 93°C, respectively. The DB2 mutant (ΔcpkA∷cpkBΔcpkB), whosecpkBgene was expressed under the control of thecpkApromoter, did not grow at 60°C, and the DB3 mutant [ΔcpkA(1–524)∷cpkB(1–524) ΔcpkB], whose CpkA amino acid residues 1 to 524 were replaced with corresponding CpkB residues that maintained the C-terminal region intact, grew at 60°C, implying that the CpkA C-terminal region plays a key role in cell growth at 60°C. To screen for specific CpkA target proteins, comparative pulldown studies with anti-Cpk were performed using cytoplasmic fractions from DA1 cells cultivated at 93°C and DB1 cells cultivated at 60°C. Among the proteins coprecipitated with anti-Cpk, TK0252, encoding indole-3-glycerol-phosphate synthase (TrpC), showed the highest Mascot score. Counter-pulldown experiments were also performed on DA1 and DB1 extracts using anti-TrpC. CpkA coimmunoprecipitated with anti-TrpC while CpkB did not. The results obtained indicate that TrpC is a specific target for CpkA. The effects of Cpks on denatured TrpC were then examined. The refolding of partially denatured TrpC was accelerated by the addition of CpkA but not by adding CpkB. DA1 cells grew optimally in minimal medium only in the presence of tryptophan but hardly grew in the absence of tryptophan at 60°C. It has been suggested that a lesion of functional TrpC is caused bycpkAdisruption, resulting in tryptophan auxotrophy.

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Property of cold inducible DEAD-box RNA helicase in hyperthermophilic archaea

Cited by 24 publications

References 28 publications

Importance and Determinants of Induction of Cold-Induced DEAD RNA Helicase in the Hyperthermophilic Archaeon Thermococcus kodakarensis

Importance and Determinants of Induction of Cold-Induced DEAD RNA Helicase in the Hyperthermophilic Archaeon Thermococcus kodakarensis

Dual Biosynthesis Pathway for Longer-Chain Polyamines in the Hyperthermophilic Archaeon Thermococcus kodakarensis

Indole-3-Glycerol-Phosphate Synthase Is Recognized by a Cold-Inducible Group II Chaperonin in Thermococcus kodakarensis

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