Paradoxical DNA Repair and Peroxide Resistance Gene Conservation in Bacillus pumilus SAFR-032

Background Bacillus spores are notoriously resistant to unfavorable conditions such as UV radiation, γ-radiation, H2O2, desiccation, chemical disinfection, or starvation. Bacillus pumilus SAFR-032 survives standard decontamination procedures of the Jet Propulsion Lab spacecraft assembly facility, and both spores and vegetative cells of this strain exhibit elevated resistance to UV radiation and H2O2 compared to other Bacillus species. Principal Findings The genome of B. pumilus SAFR-032 was sequenced and annotated. Lists of genes relevant to DNA repair and the oxidative stress response were generated and compared to B. subtilis and B. licheniformis. Differences in conservation of genes, gene order, and protein sequences are highlighted because they potentially explain the extreme resistance phenotype of B. pumilus. The B. pumilus genome includes genes not found in B. subtilis or B. licheniformis and conserved genes with sequence divergence, but paradoxically lacks several genes that function in UV or H2O2 resistance in other Bacillus species. Significance This study identifies several candidate genes for further research into UV and H2O2 resistance. These findings will help explain the resistance of B. pumilus and are applicable to understanding sterilization survival strategies of microbes.

[1]  G. Reitz,et al.  DNA bipyrimidine photoproduct repair and transcriptional response of UV-C irradiated Bacillus subtilis , 2007, Archives of Microbiology.

[2]  Han Rauwerda,et al.  Analysis of Temporal Gene Expression during Bacillus subtilis Spore Germination and Outgrowth , 2007, Journal of bacteriology.

[3]  G. Reitz,et al.  Role of DNA Repair by Nonhomologous-End Joining in Bacillus subtilis Spore Resistance to Extreme Dryness, Mono- and Polychromatic UV, and Ionizing Radiation , 2007, Journal of bacteriology.

[4]  Y. Hua,et al.  Evolutionary pathways of an ancient gene recX. , 2007, Gene.

[5]  C. F. Menck,et al.  Genome analysis of DNA repair genes in the alpha proteobacterium Caulobacter crescentus , 2007, BMC Microbiology.

[6]  P. Setlow Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals , 2006, Journal of applied microbiology.

[7]  Elizabeth C. Theil,et al.  Paired Bacillus anthracis Dps (Mini-ferritin) Have Different Reactivities with Peroxide* , 2006, Journal of Biological Chemistry.

[8]  Daisuke Kihara,et al.  Enhanced automated function prediction using distantly related sequences and contextual association by PFP , 2006, Protein science : a publication of the Protein Society.

[9]  Erin M. Conlon,et al.  The forespore line of gene expression in Bacillus subtilis. , 2006, Journal of molecular biology.

[10]  G. Klug,et al.  Thioredoxins in bacteria: functions in oxidative stress response and regulation of thioredoxin genes , 2006, Naturwissenschaften.

[11]  B. Van Houten,et al.  Prokaryotic nucleotide excision repair: the UvrABC system. , 2006, Chemical reviews.

[12]  Robert P. Hausinger,et al.  The AidB Component of the Escherichia coli Adaptive Response to Alkylating Agents Is a Flavin-Containing, DNA-Binding Protein , 2006, Journal of bacteriology.

[13]  Milton H. Saier,et al.  TCDB: the Transporter Classification Database for membrane transport protein analyses and information , 2005, Nucleic Acids Res..

[14]  L. Essen,et al.  Light-driven DNA repair by photolyases , 2006, Cellular and Molecular Life Sciences CMLS.

[15]  K. Asai,et al.  Transcriptional analysis of the ylaABCD operon of Bacillus subtilis encoding a sigma factor of extracytoplasmic function family. , 2005, Genes & genetic systems.

[16]  R. Tanner,et al.  Survival of Spacecraft-Associated Microorganisms under Simulated Martian UV Irradiation , 2005, Applied and Environmental Microbiology.

[17]  Eli S. Groban,et al.  Genetic Composition of the Bacillus subtilis SOS System , 2005, Journal of bacteriology.

[18]  Eli S. Groban,et al.  Binding of the Bacillus subtilis LexA protein to the SOS operator , 2005, Nucleic acids research.

[19]  P. Setlow,et al.  Role of the Nfo (YqfS) and ExoA Apurinic/Apyrimidinic Endonucleases in Protecting Bacillus subtilis Spores from DNA Damage , 2005, Journal of bacteriology.

[20]  James R. Knight,et al.  Genome sequencing in microfabricated high-density picolitre reactors , 2005, Nature.

[21]  S. Rhee,et al.  Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. , 2005, Free radical biology & medicine.

[22]  J. Dubois,et al.  Tricksy Business: Transcriptome Analysis Reveals the Involvement of Thioredoxin A in Redox Homeostasis, Oxidative Stress, Sulfur Metabolism, and Cellular Differentiation in Bacillus subtilis , 2005, Journal of bacteriology.

[23]  Fei Chen,et al.  Recurrent isolation of hydrogen peroxide-resistant spores of Bacillus pumilus from a spacecraft assembly facility. , 2005, Astrobiology.

[24]  J. Helmann,et al.  Bacillus subtilis Paraquat Resistance Is Directed by σM, an Extracytoplasmic Function Sigma Factor, and Is Conferred by YqjL and BcrC , 2005, Journal of bacteriology.

[25]  P. Setlow,et al.  Analysis of factors that influence the sensitivity of spores of Bacillus subtilis to DNA damaging chemicals , 2005, Journal of applied microbiology.

[26]  Martin Ester,et al.  Sequence analysis PSORTb v . 2 . 0 : Expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis , 2004 .

[27]  A. McLennan,et al.  The Nudix hydrolase superfamily , 2005, Cellular and Molecular Life Sciences CMLS.

[28]  M. Noirot-Gros,et al.  Distinctive genetic features exhibited by the Y‐family DNA polymerases in Bacillus subtilis , 2004, Molecular microbiology.

[29]  M. Pedraza-Reyes,et al.  Contribution of the Mismatch DNA Repair System to the Generation of Stationary-Phase-Induced Mutants of Bacillus subtilis , 2004, Journal of bacteriology.

[30]  Guangwei Fan,et al.  Complete Genome Sequence of Rickettsia typhi and Comparison with Sequences of Other Rickettsiae , 2004, Journal of bacteriology.

[31]  E. Seeberg,et al.  The Bacillus subtilis Counterpart of the Mammalian 3-Methyladenine DNA Glycosylase Has Hypoxanthine and 1,N6-Ethenoadenine as Preferred Substrates* , 2004, Journal of Biological Chemistry.

[32]  G. Weinstock,et al.  The Atlas genome assembly system. , 2004, Genome research.

[33]  M. Hecker,et al.  Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress. , 2004, Microbiology.

[34]  R. Camerini-Otero,et al.  Characterization of the DNA Damage-inducible Helicase DinG from Escherichia coli* , 2003, Journal of Biological Chemistry.

[35]  Ron D. Appel,et al.  ExPASy: the proteomics server for in-depth protein knowledge and analysis , 2003, Nucleic Acids Res..

[36]  M. J. Jedrzejas,et al.  Bacillus Species Proteins Involved in Spore Formation and Degradation: From Identification in the Genome, to Sequence Analysis, and Determination of Function and Structure , 2003, Critical reviews in biochemistry and molecular biology.

[37]  W. Nicholson,et al.  Spore UV and acceleration resistance of endolithic Bacillus pumilus and Bacillus subtilis isolates obtained from Sonoran desert basalt: implications for lithopanspermia. , 2003, Astrobiology.

[38]  P. Jeggo,et al.  Identification of a DNA Nonhomologous End-Joining Complex in Bacteria , 2002, Science.

[39]  D. Mckay,et al.  Helicase structure and mechanism. , 2002, Current opinion in structural biology.

[40]  A. Grossman,et al.  Visualization of mismatch repair in bacterial cells. , 2001, Molecular cell.

[41]  Rolf Apweiler,et al.  InterProScan - an integration platform for the signature-recognition methods in InterPro , 2001, Bioinform..

[42]  J. Helmann,et al.  OhrR Is a Repressor of ohrA, a Key Organic Hydroperoxide Resistance Determinant in Bacillus subtilis , 2001, Journal of bacteriology.

[43]  P. Setlow Resistance of spores of Bacillus species to ultraviolet light , 2001, Environmental and molecular mutagenesis.

[44]  H. Melosh,et al.  Resistance of Bacillus Endospores to Extreme Terrestrial and Extraterrestrial Environments , 2000, Microbiology and Molecular Biology Reviews.

[45]  P. Hanawalt,et al.  A phylogenomic study of DNA repair genes, proteins, and processes. , 1999, Mutation research.

[46]  S. Salzberg,et al.  Improved microbial gene identification with GLIMMER. , 1999, Nucleic acids research.

[47]  A. Yasui,et al.  Repair of apurinic/apyrimidinic sites by UV damage endonuclease; a repair protein for UV and oxidative damage. , 1999, Nucleic acids research.

[48]  P. Setlow,et al.  Regulation of four genes encoding small, acid-soluble spore proteins in Bacillus subtilis. , 1999, Gene.

[49]  A EisenJ,et al.  DNA修復遺伝子,タンパクと過程のphylogenomic(系統発生的ゲノム)調査 , 1999 .

[50]  P. Setlow,et al.  New Small, Acid-Soluble Proteins Unique to Spores ofBacillus subtilis: Identification of the Coding Genes and Regulation and Function of Two of These Genes , 1998, Journal of bacteriology.

[51]  K. Entian,et al.  PcrA is an essential DNA helicase of Bacillus subtilis fulfilling functions both in repair and rolling‐circle replication , 1998, Molecular microbiology.

[52]  T. Horii,et al.  Inhibition of Escherichia coli RecA coprotease activities by DinI , 1998, The EMBO journal.

[53]  P. Setlow,et al.  The katX Gene, Which Codes for the Catalase in Spores of Bacillus subtilis, Is a Forespore-Specific Gene Controlled by ςF, and KatX Is Essential for Hydrogen Peroxide Resistance of the Germinating Spore , 1998, Journal of bacteriology.

[54]  M. Borodovsky,et al.  GeneMark.hmm: new solutions for gene finding. , 1998, Nucleic acids research.

[55]  P. Setlow,et al.  Alkyl hydroperoxide reductase, catalase, MrgA, and superoxide dismutase are not involved in resistance of Bacillus subtilis spores to heat or oxidizing agents , 1997, Journal of bacteriology.

[56]  S. W. Matson,et al.  A Point Mutation in Escherichia coli DNA Helicase II Renders the Enzyme Nonfunctional in Two DNA Repair Pathways , 1997, The Journal of Biological Chemistry.

[57]  J. Haber,et al.  Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae , 1996, Molecular and cellular biology.

[58]  R A Gibbs,et al.  A "double adaptor" method for improved shotgun library construction. , 1996, Analytical biochemistry.

[59]  P. Setlow Mechanisms for the prevention of damage to DNA in spores of Bacillus species. , 1995, Annual review of microbiology.

[60]  P. Setlow,et al.  Properties of Bacillus subtilis small, acid-soluble spore proteins with changes in the sequence recognized by their specific protease , 1994, Journal of bacteriology.

[61]  J. Kooistra,et al.  The Bacillus subtilis addAB genes are fully functional in Escherichia coli , 1993, Molecular microbiology.

[62]  R. Losick,et al.  Bacillus Subtilis and Other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular Genetics , 1993 .

[63]  F. Priest Systematics and Ecology of Bacillus , 1993 .

[64]  D. Cheo,et al.  Inducible DNA repair and differentiation in Bacillus subtilis: interactions between global regulons , 1992, Molecular microbiology.

[65]  S. Farr,et al.  Oxidative stress responses in Escherichia coli and Salmonella typhimurium. , 1991, Microbiological reviews.

[66]  P. Setlow,et al.  Effects of mutant small, acid-soluble spore proteins from Bacillus subtilis on DNA in vivo and in vitro , 1991, Journal of bacteriology.

[67]  L. Samson,et al.  Relative efficiencies of the bacterial, yeast, and human DNA methyltransferases for the repair of O6-methylguanine and O4-methylthymine. Suggestive evidence for O4-methylthymine repair by eukaryotic methyltransferases. , 1991, The Journal of biological chemistry.

[68]  N. Munakata,et al.  Bacillus subtilis ada operon encodes two DNA alkyltransferases. , 1990, Nucleic acids research.

[69]  H. Sambrook Molecular cloning : a laboratory manual. Cold Spring Harbor, NY , 1989 .

[70]  I. Dodd,et al.  The prediction of helix-turn-helix DNA-binding regions in proteins. A reply to Yudkin. , 1988, Protein engineering.

[71]  M. Yudkin,et al.  The prediction of helix-turn-helix DNA-binding regions in proteins. , 1987, Protein engineering.

[72]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .