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PMID: 15140832 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Systems level insights into the stress response to UV radiation in the halophilic archaeon Halobacterium NRC-1.

Genome research ·Vol. 14 ·No. 6 ·2004-06-00 ·Pages 1025-35

Baliga NS, Bjork SJ, Bonneau R, Pan M, Iloanusi C, Kottemann MC, Hood L, DiRuggiero J

Abstract

We report a remarkably high UV-radiation resistance in the extremely halophilic archaeon Halobacterium NRC-1 withstanding up to 110 J/m2 with no loss of viability. Gene knockout analysis in two putative photolyase-like genes (phr1 and phr2) implicated only phr2 in photoreactivation. The UV-response was further characterized by analyzing simultaneously, along with gene function and protein interactions inferred through comparative genomics approaches, mRNA changes for all 2400 genes during light and dark repair. In addition to photoreactivation, three other putative repair mechanisms were identified including d(CTAG) methylation-directed mismatch repair, four oxidative damage repair enzymes, and two proteases for eliminating damaged proteins. Moreover, a UV-induced down-regulation of many important metabolic functions was observed during light repair and seems to be a phenomenon shared by all three domains of life. The systems analysis has facilitated the assignment of putative functions to 26 of 33 key proteins in the UV response through sequence-based methods and/or similarities of their predicted three-dimensional structures to known structures in the PDB. Finally, the systems analysis has raised, through the integration of experimentally determined and computationally inferred data, many experimentally testable hypotheses that describe the metabolic and regulatory networks of Halobacterium NRC-1.

MeSH Terms
Animals Archaeal Proteins/physiology Cricetinae DNA Repair/genetics Deoxyribodipyrimidine Photo-Lyase/deficiency Gene Expression Profiling/methods Gene Expression Regulation, Archaeal/genetics,radiation effects Halobacterium/classification,enzymology,genetics,radiation effects Light Mesocricetus/genetics Mice Mutation/genetics RNA, Archaeal/genetics RNA, Messenger/genetics Repressor Proteins/genetics Sequence Homology, Nucleic Acid Survival Rate Time Factors Transcription Factors/genetics Ultraviolet Rays
Chemicals
Archaeal Proteins RNA, Archaeal RNA, Messenger Repressor Proteins Sin3b protein, mouse Transcription Factors Deoxyribodipyrimidine Photo-Lyase
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Baliga Nitin S
Institute for Systems Biology, Seattle, Washington 98103, USA. nbaliga@systemsbiology.org
Bjork Sarah J
Bonneau Richard
Pan Min
Iloanusi Chika
Kottemann Molly C H
Hood Leroy
DiRuggiero Jocelyne
References (47)
47 references, click to expand
  1. Testing for differentially-expressed genes by maximum-likelihood analysis of microarray data.
    J Comput Biol. 2000;7(6):805-17 PMID: 11382363
  2. De novo prediction of three-dimensional structures for major protein families.
    J Mol Biol. 2002 Sep 6;322(1):65-78 PMID: 12215415
  3. Crystal structure of thermostable DNA photolyase: pyrimidine-dimer recognition mechanism.
    Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13560-5 PMID: 11707580
  4. SCOP database in 2002: refinements accommodate structural genomics.
    Nucleic Acids Res. 2002 Jan 1;30(1):264-7 PMID: 11752311
  5. Coordinate regulation of energy transduction modules in Halobacterium sp. analyzed by a global systems approach.
    Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14913-8 PMID: 12403819
  6. The KEGG database.
    Novartis Found Symp. 2002;247:91-101; discussion 101-3, 119-28, 244-52 PMID: 12539951
  7. CASP and CAFASP experiments and their findings.
    Methods Biochem Anal. 2003;44:501-7 PMID: 12647401
  8. Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation.
    Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):4191-6 PMID: 12651953
  9. An archaeal XPF repair endonuclease dependent on a heterotrimeric PCNA.
    Mol Microbiol. 2003 Apr;48(2):361-71 PMID: 12675797
  10. Repair of UV damage in Halobacterium salinarum.
    Biochem Soc Trans. 2003 Jun;31(Pt 3):694-8 PMID: 12773185
  11. Cytoscape: a software environment for integrated models of biomolecular interaction networks.
    Genome Res. 2003 Nov;13(11):2498-504 PMID: 14597658
  12. Systems approaches applied to the study of Saccharomyces cerevisiae and Halobacterium sp.
    Cold Spring Harb Symp Quant Biol. 2003;68:345-57 PMID: 15338636
  13. Control of transmembrane ion fluxes to select halorhodopsin-deficient and other energy-transduction mutants of Halobacterium halobium.
    Proc Natl Acad Sci U S A. 1982 Jul;79(14):4308-12 PMID: 6289299
  14. DNA photorepair: chromophore composition and function in two classes of DNA photolyases.
    Biofactors. 1990 Oct;2(4):207-11 PMID: 2282137
  15. A human nuclear uracil DNA glycosylase is the 37-kDa subunit of glyceraldehyde-3-phosphate dehydrogenase.
    Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8460-4 PMID: 1924305
  16. Synthesis of reinitiated transcripts by mammalian RNA polymerase II is controlled by elongation factor SII.
    EMBO J. 1993 Dec;12(12):4677-84 PMID: 8223477
  17. Out of the shadows and into the light: the emergence of DNA repair.
    Trends Biochem Sci. 1995 Oct;20(10):381 PMID: 8533146
  18. Positive and negative elements involved in the differential regulation by heme and oxygen of the HEM13 gene (coproporphyrinogen oxidase) in Saccharomyces cerevisiae.
    Curr Genet. 1995 Nov;28(6):503-11 PMID: 8593679
  19. The repair of ultraviolet light-induced DNA damage in the halophilic archaebacteria, Halobacterium cutirubrum, Halobacterium halobium and Haloferax volcanii.
    Mutat Res. 1996 Sep 2;364(1):25-32 PMID: 8814335
  20. SCOP: a structural classification of proteins database.
    Nucleic Acids Res. 1997 Jan 1;25(1):236-9 PMID: 9016544
  21. Genetic responses of the thermophilic archaeon Sulfolobus acidocaldarius to short-wavelength UV light.
    J Bacteriol. 1997 Sep;179(18):5693-8 PMID: 9294423
  22. Complete genome sequence of Methanobacterium thermoautotrophicum deltaH: functional analysis and comparative genomics.
    J Bacteriol. 1997 Nov;179(22):7135-55 PMID: 9371463
  23. A primitive pathway of porphyrin biosynthesis and enzymology in Desulfovibrio vulgaris.
    Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):4853-8 PMID: 9560192
  24. Nucleotide excision repair in the third kingdom.
    J Bacteriol. 1998 Nov;180(21):5796-8 PMID: 9791138
  25. The use of gene clusters to infer functional coupling.
    Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):2896-901 PMID: 10077608
  26. Assigning protein functions by comparative genome analysis: protein phylogenetic profiles.
    Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4285-8 PMID: 10200254
  27. Detecting protein function and protein-protein interactions from genome sequences.
    Science. 1999 Jul 30;285(5428):751-3 PMID: 10427000
  28. Enzymatic repair of 5-formyluracil. I. Excision of 5-formyluracil site-specifically incorporated into oligonucleotide substrates by alka protein (Escherichia coli 3-methyladenine DNA glycosylase II).
    J Biol Chem. 1999 Aug 27;274(35):25136-43 PMID: 10455195
  29. The CATH protein family database: a resource for structural and functional annotation of genomes.
    Proteomics. 2002 Jan;2(1):11-21 PMID: 11788987
  30. Rosetta in CASP4: progress in ab initio protein structure prediction.
    Proteins. 2001;Suppl 5:119-26 PMID: 11835488
  31. The economics of ribosome biosynthesis in yeast.
    Trends Biochem Sci. 1999 Nov;24(11):437-40 PMID: 10542411
  32. The Pfam protein families database.
    Nucleic Acids Res. 2000 Jan 1;28(1):263-6 PMID: 10592242
  33. A phylogenomic study of DNA repair genes, proteins, and processes.
    Mutat Res. 1999 Dec 7;435(3):171-213 PMID: 10606811
  34. Homologous gene knockout in the archaeon Halobacterium salinarum with ura3 as a counterselectable marker.
    Mol Microbiol. 2000 Feb;35(3):667-76 PMID: 10672188
  35. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae.
    Nature. 2000 Feb 10;403(6770):623-7 PMID: 10688190
  36. Bacterial cryptochrome and photolyase: characterization of two photolyase-like genes of Synechocystis sp. PCC6803.
    Nucleic Acids Res. 2000 Jun 15;28(12):2353-62 PMID: 10871367
  37. Genome sequence of Halobacterium species NRC-1.
    Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):12176-81 PMID: 11016950
  38. The COG database: new developments in phylogenetic classification of proteins from complete genomes.
    Nucleic Acids Res. 2001 Jan 1;29(1):22-8 PMID: 11125040
  39. The protein-protein interaction map of Helicobacter pylori.
    Nature. 2001 Jan 11;409(6817):211-5 PMID: 11196647
  40. Remodeling of yeast genome expression in response to environmental changes.
    Mol Biol Cell. 2001 Feb;12(2):323-37 PMID: 11179418
  41. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli.
    Genetics. 2001 May;158(1):41-64 PMID: 11333217
  42. DNA mismatch repair and mutation avoidance pathways.
    J Cell Physiol. 2002 Apr;191(1):28-41 PMID: 11920679
  43. Characterization of Arabidopsis photolyase enzymes and analysis of their role in protection from ultraviolet-B radiation.
    J Exp Bot. 2002 May;53(371):1005-15 PMID: 11971912
  44. Transcriptional response of Saccharomyces cerevisiae to DNA-damaging agents does not identify the genes that protect against these agents.
    Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):8778-83 PMID: 12077312
  45. A powerful non-homology method for the prediction of operons in prokaryotes.
    Bioinformatics. 2002;18 Suppl 1:S329-36 PMID: 12169563
  46. The genomics of yeast responses to environmental stress and starvation.
    Funct Integr Genomics. 2002 Sep;2(4-5):181-92 PMID: 12192591
  47. Understanding the adaptation of Halobacterium species NRC-1 to its extreme environment through computational analysis of its genome sequence.
    Genome Res. 2001 Oct;11(10):1641-50 PMID: 11591641
Article Info
Journal
Genome research
Abbr.
Genome Res
ISSN
1088-9051
DOI
10.1101/gr.1993504
Email
nbaliga@systemsbiology.org
Published
2004-06-00
Epub
2004-00-12
Pages
1025-35
Language
English
Region
United States
NLM ID
9518021
PMCID
PMC419780
Subset
IM
Grants
CSR NIH HHS · RG522002 · United States
External Links
PubMed source DOI: 10.1101/gr.1993504 PMC Full Text View journal details
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