Computational search for UV radiation resistance strategies in Deinococcus swuensis isolated from Paramo ecosystems

Autoři: Jorge Díaz-Riaño aff001;  Leonardo Posada aff001;  Iván Camilo Acosta aff001;  Carlos Ruíz-Pérez aff002;  Catalina García-Castillo aff002;  Alejandro Reyes aff002;  María Mercedes Zambrano aff001
Působiště autorů: Corporación Corpogen Research Center, Bogotá D.C, Colombia aff001;  Research group in Computational Biology and Microbial Ecology, Department of Biological Sciences, Universidad de Los Andes, Bogotá D.C, Colombia aff002;  Max Planck Tandem Group in Computational Biology, Universidad de Los Andes, Bogotá D.C, Colombia aff003;  Center of Genome Sciences and Systems Biology, Washington University School of Medicine, Saint Louis, MO, United States of America aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


Ultraviolet radiation (UVR) is widely known as deleterious for many organisms since it can cause damage to biomolecules either directly or indirectly via the formation of reactive oxygen species. The goal of this study was to analyze the capacity of high-mountain Espeletia hartwegiana plant phyllosphere microorganisms to survive UVR and to identify genes related to resistance strategies. A strain of Deinococcus swuensis showed a high survival rate of up to 60% after UVR treatment at 800J/m2 and was used for differential expression analysis using RNA-seq after exposing cells to 400J/m2 of UVR (with >95% survival rate). Differentially expressed genes were identified using the R-Bioconductor package NOISeq and compared with other reported resistance strategies reported for this genus. Genes identified as being overexpressed included transcriptional regulators and genes involved in protection against damage by UVR. Non-coding (nc)RNAs were also differentially expressed, some of which have not been previously implicated. This study characterized the immediate radiation response of D. swuensis and indicates the involvement of ncRNAs in the adaptation to extreme environmental conditions.

Klíčová slova:

Gene expression – Genomic libraries – Non-coding RNA – Ribosomal RNA – RNA sequencing – Sequence databases – Ultraviolet C – Ultraviolet radiation


1. Ruiz-Pérez C a., Restrepo S, Zambrano MM. Microbial and Functional Diversity within the Phyllosphere of Espeletia sp. in an Andean High Mountain Ecosystem. Appl Environ Microbiol. 2016;82(6):AEM.02781-15. doi: 10.1128/AEM.02781-15 26746719

2. Kwang-Woo J, Sangyong L, Yong-Sun B. Microbial radiation-resistance mechanisms. J Microbiol. 2017;55(7):499–507. doi: 10.1007/s12275-017-7242-5

3. Argueso JL, Westmoreland J, Mieczkowski PA, Gawel M, Petes TD, Resnick MA. Double-strand breaks associated with repetitive DNA can reshape the genome. Proc Natl Acad Sci U S A. 2008;105(33):11845–50. doi: 10.1073/pnas.0804529105 18701715

4. Wurtmann E, Wolin SL. RNA under attack: Cellular handling of RNA damage. Crit Rev Biochem Mol Biol. 2013;31(9):34–49.

5. King B, Kesavan J, Sagripanti JL. Germicidal UV sensitivity of bacteria in aerosols and on contaminated surfaces. Aerosol Sci Technol. 2011;45(5):645–53. doi: 10.1080/02786826.2010.550959

6. Gabani P, Singh O V. Radiation-resistant extremophiles and their potential in biotechnology and therapeutics. Appl Microbiol Biotechnol. 2013;97(3):993–1004. doi: 10.1007/s00253-012-4642-7 23271672

7. Cowan DA, Ramond J, Makhalanyane TP, De Maayer P. Metagenomics of extreme environments. Curr Opin Microbiol [Internet]. 2015;25:97–102. Available from: 26048196

8. Gao Q, Garcia-Pichel F. Microbial ultraviolet sunscreens. Nat Rev Microbiol. 2011;9(11):791–802. doi: 10.1038/nrmicro2649 21963801

9. Daly MJ. A new perspective on radiation resistance based on Deinococcus radiodurans. Nat Rev Microbiol [Internet]. 2009;7(3):237–45. Available from: 19172147

10. Kim MK, Srinivasan S, Back C, Joo ES, Lee S, Jung H. Complete genome sequence of Deinococcus swuensis, a bacterium resistant to radiation toxicity. Mol Cell Toxicol. 2015;11:315–21. doi: 10.1007/s13273-015-0031-5

11. Lee JJ, Lee HJ, Jang GS, Yu JM, Cha JY, Kim SJ, et al. Deinococcus swuensis sp. nov., a gamma-radiation-resistant bacterium isolated from soil. J Microbiol. 2013;51(3):305–11. doi: 10.1007/s12275-013-3023-y 23812810

12. Luan H, Meng N, Fu J, Chen X, Xu X, Feng Q, et al. Genome-wide transcriptome and antioxidant analyses on gamma-irradiated phases of Deinococcus radiodurans R1. PLoS One. 2014;9(1). doi: 10.1371/journal.pone.0085649

13. Yuan M, Chen M, Zhang W, Lu W, Wang J, Yang M, et al. Genome sequence and transcriptome analysis of the radioresistant bacterium Deinococcus gobiensis: Insights into the extreme environmental adaptations. PLoS One. 2012;7(3):1–11. doi: 10.1371/journal.pone.0034458

14. Tsai C, Liao R, Chou B, Contreras LM. Transcriptional Analysis of Deinococcus radiodurans Reveals Novel Small RNAs That Are Differentially Expressed under Ionizing Radiation. Appl Environ Microbiol [Internet]. 2015;81(5):1754–64. Available from: 25548054

15. Sonnleitner E, Romeo A, Blaesi U Small regulatory RNAs in Pseudomonas aeruginosa.

16. Wassarman KM. Small RNAs in bacteria: Diverse regulators of gene expression in response to environmental changes. Cell. 2002;109(2):141–4. doi: 10.1016/s0092-8674(02)00717-1 12007399

17. Kowalski MP, Krude T. Functional roles of non-coding Y RNAs. Int J Biochem Cell Biol [Internet]. 2015;66:20–9. Available from:

18. Chen X, Sim S, Wurtmann EJ, Feke A, Wolin SL. Bacterial noncoding Y RNAs are widespread and mimic tRNAs. Rna [Internet]. 2014;20(11):1715–24. Available from: 25232022

19. Chen X, Wurtmann EJ, Van Batavia J, Zybailov B, Washburn MP, Wolin SL. An ortholog of the Ro autoantigen functions in 23S rRNA maturation in D. radiodurans. Genes Dev. 2007;21(11):1328–39. doi: 10.1101/gad.1548207 17510283

20. Bodenhausen N, Horton MW, Bergelson J. Bacterial Communities Associated with the Leaves and the Roots of Arabidopsis thaliana. PLoS One. 2013;8(2). doi: 10.1371/journal.pone.0056329 23457551

21. Paulino-Lima IG, Azua-Bustos A, Vicuña R, González-Silva C, Salas L, Teixeira L, et al. Isolation of UVC-Tolerant Bacteria from the Hyperarid Atacama Desert, Chile. Microb Ecol. 2013;65(2):325–35. doi: 10.1007/s00248-012-0121-z 23001596

22. Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. doi: 10.1093/bioinformatics/btu170 24695404

23. Kopylova E, Noé L, Touzet H. SortMeRNA: Fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28(24):3211–7. doi: 10.1093/bioinformatics/bts611 23071270

24. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, et al. SILVA: A comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007;35(21):7188–96. doi: 10.1093/nar/gkm864 17947321

25. Liao Y, Smyth GK, Shi W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 2013;41(10):108–24. doi: 10.1093/nar/gkt214

26. Liao Y, Smyth GK, Shi W. FeatureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30(7):923–30. doi: 10.1093/bioinformatics/btt656 24227677

27. Huson DH, Beier S, Flade I, Górska A, El-Hadidi M, Mitra S, et al. MEGAN Community Edition—Interactive Exploration and Analysis of Large-Scale Microbiome Sequencing Data. PLoS Comput Biol. 2016;12(6):1–12. doi: 10.1371/journal.pcbi.1004957

28. Tarazona S, Furió-Tarí P, Turrá D, Di Pietro A, Nueda MJ, Ferrer A, et al. Data quality aware analysis of differential expression in RNA-seq with NOISeq R/Bioc package. Nucleic Acids Res. 2015;43(21):1–15.

29. Sha Y, Phan J, May W. Effect of low-expression gene filtering on detection of differentially expressed genes in RNA-seq data. Eng Med Biol Soc (EMBC), 2015 37th Annu Int Conf IEEE (pp 6461-6464). 2015;70(12):773–9.

30. Mistry J, Finn RD, Eddy SR, Bateman A, Punta M. Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res. 2013;41(12). doi: 10.1093/nar/gkt263 23598997

31. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, et al. The Pfam protein families database: Towards a more sustainable future. Nucleic Acids Res. 2016;44(D1):D279–85. doi: 10.1093/nar/gkv1344 26673716

32. Kalvari I, Argasinska J, Quinones-Olvera N, Nawrocki EP, Rivas E, Eddy SR, et al. Rfam 13.0: shifting to a genome-centric resource for non-coding RNA families. Nucleic Acids Res [Internet]. 2017;(November):1–8. Available from:

33. Pruitt KD, Tatusova T, Maglott DR. NCBI reference sequences (RefSeq): A curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 2007;35(SUPPL. 1):501–4.

34. Nawrocki EP, Eddy SR. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics. 2013;29(22):2933–5. doi: 10.1093/bioinformatics/btt509 24008419

35. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res [Internet]. 2001;29(9):e45. Available from: 11328886

36. Chen F, Sorek R, Hugenholtz P, Lindquist EA, Froula JL, He S, et al. Validation of two ribosomal RNA removal methods for microbial metatranscriptomics. Nat Methods. 2010;7(10):807–12. doi: 10.1038/nmeth.1507 20852648

37. Conesa A, Madrigal P, Tarazona S, Gomez-Cabrero D, Cervera A, McPherson A, et al. A survey of best practices for RNA-seq data analysis. Genome Biol. 2016;17(1):1–19. doi: 10.1186/s13059-016-1047-4

38. Slade D, Radman M. Oxidative Stress Resistance in Deinococcus radiodurans. Microbiology and Molecular Biology Reviews [Internet]. 2011;75(1):133–191 p. Available from: 21372322

39. Barquist L, Burge SW, Gardner PP. Studying RNA homology and conservation with infernal: From single sequences to RNA families. Curr Protoc Bioinforma. 2016;2016:12.13.1–12.13.25. doi: 10.1002/cpbi.4

40. Arrieta JM, Weinbauer MG, Gerhard J, Mari S. Interspecific Variability in Sensitivity to UV Radiation and Subsequent Recovery in Selected Isolates of Marine Bacteria. Appl Environ Microbiol. 2000;66(4):1468–73. doi: 10.1128/aem.66.4.1468-1473.2000 10742228

41. Gascón J, Oubiña A, Pérez-Lezaun A, Urmeneta J. Sensitivity of selected bacterial species to UV radiation. Curr Microbiol. 1995;30(3):177–82. doi: 10.1007/bf00296205 7765851

42. Sundin GW, Jacobs JL. Ultraviolet radiation (UVR) sensitivity analysis and UVR survival strategies of a bacterial community from the phyllosphere of field-grown peanut (Arachis hypogeae L.). Microb Ecol. 1999;38(1):27–38. doi: 10.1007/s002489900152 10384007

43. Wei LI, Yun MA, Fangzhu X, Shuya HE. Ionizing Radiation Resistance in Deinococcus Radiodurans. Adv Nat Sci. 2014;7(2):6–14.

44. Gerber E, Bernard R, Castang S, Chabot N, Coze F, Dreux-Zigha A, et al. Deinococcus as new chassis for industrial biotechnology: Biology, physiology and tools. J Appl Microbiol. 2015;119(1):1–10. doi: 10.1111/jam.12808 25809882

45. Daly MJ. Death by protein damage in irradiated cells. DNA Repair (Amst) [Internet]. 2011;11(1):12–21. Available from:

46. Ozsolak F, Platt AR, Jones DR, Reifenberger JG, Sass LE, McInerney P, et al. Direct RNA sequencing. Nature [Internet]. 2009;461(7265):814–8. Available from: 19776739

47. Dulermo R, Onodera T, Coste G, Passot F, Dutertre M, Porteron M, et al. Identification of new genes contributing to the extreme radioresistance of Deinococcus radiodurans using a Tn5-based transposon mutant library. PLoS One. 2015;10(4):1–26. doi: 10.1371/journal.pone.0124358

48. Lord DM, Uzgoren Baran A, Soo VWC, Wood TK, Peti W, Page R. McbR/YncC: Implications for the mechanism of ligand and DNA binding by a bacterial gntr transcriptional regulator involved in biofilm formation. Biochemistry. 2014;53(46):7223–31. doi: 10.1021/bi500871a 25376905

49. Agapov AA, Kulbachinskiy A. V. Mechanisms of stress resistance and gene regulation in the radioresistant bacterium Deinococcus radiodurans. Biochem [Internet]. 2015;80(10):1201–16. Available from:

50. Liesa M, Qiu W, Shirihai OS. Mitochondrial ABC transporters function: The role of ABCB10 (ABC-me) as a novel player in cellular handling of reactive oxygen species. Biochim Biophys Acta—Mol Cell Res [Internet]. 2012;1823(10):1945–57. Available from:

51. Tong L, Lee S, Denu JM. Hydrolase regulates NAD+ metabolites and modulates cellular redox. J Biol Chem. 2009;284(17):11256–66. doi: 10.1074/jbc.M809790200 19251690

52. Makarova KS, Aravind L, Daly MJ, Koonin E V. Specific expansion of protein families in the radioresistant bacterium Deinococcus radiodurans. Genetica. 2000;108(1):25–34. doi: 10.1023/a:1004035424657 11145417

53. Makarova KS, Omelchenko M V., Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, et al. Deinococcus geothermalis: The pool of extreme radiation resistance genes shrinks. PLoS One. 2007;2(9). doi: 10.1371/journal.pone.0000955 17895995

54. Ott E, Kawaguchi Y, Kölbl D, Chaturvedi P, Nakagawa K, Yamagishi A, et al. Proteometabolomic response of Deinococcus radiodurans exposed to UVC and vacuum conditions: Initial studies prior to the Tanpopo space mission. PLoS One. 2017;12(12):1–25. doi: 10.1371/journal.pone.0189381

55. Ohtani N, Tomita M, Itaya M. An extreme thermophile, Thermus thermophilus, is a polyploid bacterium. J Bacteriol. 2010;192(20):5499–505. doi: 10.1128/JB.00662-10 20729360

56. Dib J, Motok J, Zenoff VF, Ordoñez O, Farías ME. Occurrence of resistance to antibiotics, UV-B, and arsenic in bacteria isolated from extreme environments in high-altitude (above 4400 m) Andean wetlands. Curr Microbiol. 2008;56(5):510–7. doi: 10.1007/s00284-008-9103-2 18330637

57. Guerrero-Beltrán JA, Barbosa-Cánovas G V. Advantages and Limitations on Processing Foods by UV Light. Food Sci Technol Int. 2004;10(3):137–47. doi: 10.1177/1082013204044359

58. Hengge-Aronis R. Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev [Internet]. 2002;66(3):373–95, table of contents. Available from: 12208995

59. Rasis M, Segal G. The LetA-RsmYZ-CsrA regulatory cascade, together with RpoS and PmrA, post-transcriptionally regulates stationary phase activation of Legionella pneumophila Icm/Dot effectors. Mol Microbiol. 2009;72(4):995–1010. doi: 10.1111/j.1365-2958.2009.06705.x 19400807

60. Kyuma T, Kizaki H, Ryuno H, Sekimizu K, Kaito C. 16S rRNA methyltransferase KsgA contributes to oxidative stress resistance and virulence in Staphylococcus aureus. Biochimie [Internet]. 2015;119:166–74. Available from: 26545800

61. Fields JA, Thompson SA. Campylobacter jejuni CsrA mediates oxidative stress responses, biofilm formation, and host cell invasion. J Bacteriol. 2008;190(9):3411–6. doi: 10.1128/JB.01928-07 18310331

62. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 2009;10(1):57–63. doi: 10.1038/nrg2484 19015660

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden