Abstract
Objectives
A 2′,3′-cyclic phosphodiesterase gene (drCPDase) has been characterized from Deinococcus radiodurans and is involved in the robust resistance of this organism.
Results
Cells lacking 2′,3′-cyclic phosphodiesterase gene (drCPDase) showed modest growth defects and displayed increased sensitivities to high doses of various DNA-damaging agents including ionizing radiation, mitomycin C, UV and H2O2. The transcriptional level of drCPDase increased after H2O2 treatment. Additional nucleotide monophosphate partially recovered the phenotype of drCPDase knockout cells. Complementation of E. coli with drCPDase resulted in enhanced H2O2 resistance.
Conclusions
The 2′,3′-cyclic phosphodiesterase (drCPDase) contributes to the extreme resistance of D. radiodurans and is presumably involved in damaged nucleotide detoxification.
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References
Arn EA, Abelson JN (1996) The 2′-5′ RNA ligase of Escherichia coli - purification, cloning, and genomic disruption. J Biol Chem 271:31145–31153
Cao Z, Mueller CW, Julin DA (2010) Analysis of the recJ gene and protein from Deinococcus radiodurans. DNA Rep 9(1):66–75
Chen H, Xu G, Zhao Y, Tian B, Lu H, Yu X, Xu Z, Ying N, Hu S, Hua Y (2008) A novel OxyR sensor and regulator of hydrogen peroxide stress with one cysteine residue in Deinococcus radiodurans. PLoS ONE 3:e1602
Cheng K, Chen X, Xu G, Wang L, Xu H, Yang S, Zhao Y, Hua Y (2015) Biochemical and functional characterization of the NurA-HerA complex from Deinococcus radiodurans. J Bacteriol 197:2048–2061
Cheng K, Xu H, Chen X, Wang L, Tian B, Zhao Y, Hua Y (2016) Structural basis for DNA 5 -end resection by RecJ. Elife 5:e14294
Daly MJ, Gaidamakova EK, Matrosova VY, Kiang JG, Fukumoto R, Lee DY, Wehr NB, Viteri GA, Berlett BS, Levine RL (2010) Small-molecule antioxidant proteome-shields in Deinococcus radiodurans. PLoS ONE 5:e12570
Gao G, Lu H, Huang L, Hua Y (2005) Construction of DNA damage response gene pprI function-deficient and function-complementary mutants in Deinococcus radiodurans. Chin Sci Bull 50:311–316
Ishino Y, Narumi I (2015) DNA repair in hyperthermophilic and hyperradioresistant microorganisms. Curr Opin Microbiol 25:103–112
Krisko A, Radman M (2013) Biology of extreme radiation resistance: the way of Deinococcus radiodurans. Cold Spring Harb Perspect Biol 5:a012765
Lappe-Siefke C, Goebbels S, Gravel M, Nicksch E, Lee J, Braun PE, Griffiths IR, Nave KA (2003) Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 33:366–374
Li M, Sun H, Feng Q, Lu H, Zhao Y, Zhang H, Xu X, Jiao J, Wang L, Hua Y (2013) Extracellular dGMP enhances Deinococcus radiodurans tolerance to oxidative stress. PLoS ONE 8:e54420
Lin J, Hu Y, Tian B, Hua Y (2009) Evolution of double MutT/Nudix domain-containing proteins: similar domain architectures from independent gene duplication-fusion events. J Genet Genom 36:603–610
Lin L, Dai S, Tian B, Li T, Yu J, Liu C, Wang L, Xu H, Zhao Y, Hua Y (2016) DqsIR quorum sensing-mediated gene regulation of the extremophilic bacterium Deinococcus radiodurans in response to oxidative stress. Mol Microbiol 100:527–541
Liu Y, Zhou J, Omelchenko MV, Beliaev AS, Venkateswaran A, Stair J, Wu L, Thompson DK, Xu D, Rogozin IB, Gaidamakova EK, Zhai M, Makarova KS, Koonin EV, Daly MJ (2003) Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation. Proc Natl Acad Sci USA 100:4191–4196
Munteanu A, Uivarosi V, Andries A (2015) Recent progress in understanding the molecular mechanisms of radioresistance in Deinococcus bacteria. Extremophiles 19:707–719
Ngo KV, Molzberger ET, Chitteni-Pattu S, Cox MM (2013) Regulation of Deinococcus radiodurans RecA protein function via modulation of active and inactive nucleoprotein filament states. J Biol Chem 288:21351–21366
Phizicky EM, Hopper AK (2010) tRNA biology charges to the front. Gene Dev 24:1832–1860
Popow J, Schleiffer A, Martinez J (2012) Diversity and roles of (t)RNA ligases. Cell Mol Life Sci 69:2657–2670
Remus BS, Shuman S (2013) A kinetic framework for tRNA ligase and enforcement of a 2′-phosphate requirement for ligation highlights the design logic of an RNA repair machine. RNA 19:659–669
Remus BS, Jacewicz A, Shuman S (2014) Structure and mechanism of E. coli RNA 2′,3′-cyclic phosphodiesterase. RNA 20:1697–1705
Schwer B, Sawaya R, Ho CK, Shuman S (2004) Portability and fidelity of RNA-repair systems. Proc Natl Acad Sci USA 101:2788–2793
Xu W, Shen J, Dunn CA, Desai S, Bessman MJ (2001) The Nudix hydrolases of Deinococcus radiodurans. Mol Microbiol 39:286–290
Zhang H, Xu Q, Lu M, Xu X, Wang Y, Wang L, Zhao Y, Hua Y (2014) Structural and functional studies of MutS2 from Deinococcus radiodurans. DNA Repair 21:111–119
Acknowledgements
This work was supported by the Zhejiang Provincial Natural Science Foundation for Outstanding Young Scientists (LR16C050002) and grants from the National Natural Science Foundation of China (31670819, 31670065).
Supporting information
Supplementary Table 1—Bacterial strains and plasmids.
Supplementary Table 2—Primers used for cloning and real time PCR.
Supplementary Fig. 1—Sequence alignments of the CPDase family proteins.
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Han, W., Zhou, C., Cheng, J. et al. Characterization and role of a 2′,3′-cyclic phosphodiesterase from Deinococcus radiodurans . Biotechnol Lett 39, 1211–1217 (2017). https://doi.org/10.1007/s10529-017-2349-7
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DOI: https://doi.org/10.1007/s10529-017-2349-7