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The Evolution of RecD Outside of the RecBCD Complex

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Abstract

The common understanding of the function of RecD, as derived predominantly from studies in Escherichia coli, is that RecD is one of three enzymes in the RecBCD double-stranded break repair DNA recombination complex. However, comparative genomics has revealed that many organisms possess a recD gene even though the other members of the complex, recB and recC, are not present. Further, bioinformatic analyses have shown that there is substantial sequence dissimilarity between recD genes associated with recB and recC (recD1), and those that are not associated with recBC (recD2). Deinococcus radiodurans, known for its extraordinary DNA repair capability, is one such organism that does not possess either recB or recC, and yet does possess a recD gene. The recD of D. radiodurans was deleted and this mutant was shown to have a capacity to repair double-stranded DNA breaks equivalent to wild-type. The phylogenetic history of recD was studied using a dataset of 120 recD genes from 91 fully sequenced species. The analysis focused upon the role of gene duplication and functional genomic context in the evolution of recD2, which appears to have undergone numerous independent events resulting in duplicate recD2 genes. The role of RecD as part of the RecBCD complex appears to have a divergence from an earlier ancestral RecD function still preserved in many species including D. radiodurans.

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References

  • Amundsen SK, Taylor AF, Chaudhury AM, Smith GR (1986) recD: the gene for an essential third subunit of exonuclease V. Proc Natl Acad Sci USA 83:5558–5562

    Article  CAS  PubMed  Google Scholar 

  • Battista JR (1997) Against all odds: the survival strategies of Deinococcus radiodurans. Annu Rev Microbiol 51:203–224

    Article  CAS  PubMed  Google Scholar 

  • Benzer S (1961) On the topography of the genetic fine structure. Proc Natl Acad Sci USA 47:403–415

    Article  CAS  PubMed  Google Scholar 

  • Bidle KA, Bartlett DH (1999) RecD function is required for high-pressure growth of a deep-sea bacterium. J Bacteriol 181:2330–2337

    CAS  PubMed  Google Scholar 

  • Biek DP, Cohen SN (1986) Identification and characterization of recD, a gene affecting plasmid maintenance and recombination in Escherichia coli. J Bacteriol 167:594–603

    CAS  PubMed  Google Scholar 

  • Blount ZD, Borland CZ, Lenski RE (2008) Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc Natl Acad Sci USA 105:7899–7906

    Article  CAS  PubMed  Google Scholar 

  • Boussau B, Blanquart S, Necsulea A, Lartillot N, Gouy M (2008) Parallel adaptations to high temperatures in the Archaean eon. Nature 456:942–946

    Article  CAS  PubMed  Google Scholar 

  • Chaudhury AM, Smith GR (1984) A new class of Escherichia coli recBC mutants: implications for the role of RecBC enzyme in homologous recombination. Proc Natl Acad Sci USA 81:7850–7854

    Article  CAS  PubMed  Google Scholar 

  • Chaussee MS, Wilson J, Hill SA (1999) Characterization of the recD gene of Neisseria gonorrhoeae MS11 and the effect of recD inactivation on pilin variation and DNA transformation. Microbiology 145(Pt 2):389–400

    Article  CAS  PubMed  Google Scholar 

  • Chedin F, Kowalczykowski SC (2002) A novel family of regulated helicases/nucleases from Gram-positive bacteria: insights into the initiation of DNA recombination. Mol Microbiol 43:823–834

    Article  CAS  PubMed  Google Scholar 

  • Ciccarelli FD, Doerks T, Von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283–1287

    Article  CAS  PubMed  Google Scholar 

  • Cromie GA (2009) Phylogenetic ubiquity and shuffling of the bacterial RecBCD and AddAB complexes. J Bacteriol 191(16):5076–5084

    Article  CAS  PubMed  Google Scholar 

  • Dillingham MS, Spies M, Kowalczykowski SC (2003) RecBCD enzyme is a bipolar DNA helicase. Nature 423:893–897

    Article  CAS  PubMed  Google Scholar 

  • Earl AM, Rankin SK, Kim KP, Lamendola ON, Battista JR (2002) Genetic evidence that the uvsE gene product of Deinococcus radiodurans R1 is a UV damage endonuclease. J Bacteriol 184:1003–1009

    Article  CAS  PubMed  Google Scholar 

  • Emmerson PT (1968) Recombination deficient mutants of Escherichia coli K-12 that map between thyA and argA. Genetics 60:19–30

    CAS  PubMed  Google Scholar 

  • Felsenstein J (1989) PHYLIP—Phylogeny Inference Package (Version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz H-R, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, Bateman A (2008) The Pfam protein families database. Nucleic Acids Res 36:D281–D288

    Article  CAS  PubMed  Google Scholar 

  • Howard-Flanders P, Theriot L (1966) Mutants of Escherichia coli K-12 defective in DNA repair and in genetic recombination. Genetics 53:1137–1150

    CAS  PubMed  Google Scholar 

  • Hughes AL (1994) The evolution of functionally novel proteins after gene duplication. Proc Biol Sci 256:119–124

    Article  CAS  PubMed  Google Scholar 

  • Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, Rupp R (2007) Dendroscope—an interactive viewer of large phylogenetic trees. BMC Bioinform 8:460

    Article  Google Scholar 

  • Hutchison CA, Montague MG (2002) Mycoplasmas and the minimal genome concept. In: Razin S, Herrmann R (eds) Molecular biology and pathogenicity of mycoplasmas. Plenum Pub Corp, Jerusalem, pp 221–253

    Chapter  Google Scholar 

  • Imlay JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science 240:1302–1309

    Article  CAS  PubMed  Google Scholar 

  • Khairnar NP, Kamble VA, Misra HS (2008) RecBC enzyme overproduction affects UV and gamma radiation survival of Deinococcus radiodurans. DNA Repair (Amst) 7:40–47

    Article  CAS  Google Scholar 

  • Kickstein E, Harms K, Wackernagel W (2007) Deletions of recBCD or recD influence genetic transformation differently and are lethal together with a recJ deletion in Acinetobacter baylyi. Microbiology 153:2259–2270

    Article  CAS  PubMed  Google Scholar 

  • Lloyd RG, Porton MC, Buckman C (1988) Effect of recF, recJ, recN, recO and ruv mutations on ultraviolet survival and genetic recombination in a recD strain of Escherichia coli K12. Mol Gen Genet 212:317–324

    Article  CAS  PubMed  Google Scholar 

  • Lovett ST, Luisi-DeLuca C, Kolodner RD (1988) The genetic dependence of recombination in recD mutants of Escherichia coli. Genetics 120:37–45

    CAS  PubMed  Google Scholar 

  • Masters CI, Smith MD, Gutman PD, Minton KW (1991) Heterozygosity and instability of amplified chromosomal insertions in the radioresistant bacterium Deinococcus radiodurans. J Bacteriol 173:6110–6117

    CAS  PubMed  Google Scholar 

  • Mattimore V, Battista JR (1996) Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J Bacteriol 178:633–637

    CAS  PubMed  Google Scholar 

  • Mehr IJ, Seifert HS (1998) Differential roles of homologous recombination pathways in Neisseria gonorrhoeae pilin antigenic variation, DNA transformation and DNA repair. Mol Microbiol 30:697–710

    Article  CAS  PubMed  Google Scholar 

  • Meima R, Lidstrom ME (2000) Characterization of the minimal replicon of a cryptic Deinococcus radiodurans SARK plasmid and development of versatile Escherichia coliD. radiodurans shuttle vectors. Appl Environ Microbiol 66:3856–3867

    Article  CAS  PubMed  Google Scholar 

  • Miesel L, Roth JR (1994) Salmonella recD mutations increase recombination in a short sequence transduction assay. J Bacteriol 176:4092–4103

    CAS  PubMed  Google Scholar 

  • Moseley BE, Copland HJ (1975) Isolation and properties of a recombination-deficient mutant of Micrococcus radiodurans. J Bacteriol 121:422–428

    CAS  PubMed  Google Scholar 

  • Peterson JD, Umayam LA, Dickinson TM, Hickey EK, White O (2001) The comprehensive microbial resource. Nucleic Acids Res 29:123–125

    Article  CAS  PubMed  Google Scholar 

  • Regha K, Satapathy AK, Ray MK (2005) RecD plays an essential function during growth at low temperature in the antarctic bacterium Pseudomonas syringae Lz4W. Genetics 170:1473–1484

    Article  CAS  PubMed  Google Scholar 

  • Rocha EP, Cornet E, Michel B (2005) Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLoS Genet 1:e15

    Article  PubMed  Google Scholar 

  • Saikrishnan K, Griffiths SP, Cook N, Court R, Wigley DB (2008) DNA binding to RecD: role of the 1B domain in SF1B helicase activity. EMBO J 27:2222–2229

    Article  CAS  PubMed  Google Scholar 

  • Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504

    Article  CAS  PubMed  Google Scholar 

  • Servinsky MD, Julin DA (2007) Effect of a recD mutation on DNA damage resistance and transformation in Deinococcus radiodurans. J Bacteriol 189:5101–5107

    Article  CAS  PubMed  Google Scholar 

  • Singleton MR, Dillingham MS, Gaudier M, Kowalczykowski SC, Wigley DB (2004) Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks. Nature 432:187–193

    Article  CAS  PubMed  Google Scholar 

  • Slade D, Linder A, Paul G, Radman M (2009) Recombination and replication in DNA repair of heavily irradiated Deinococcus radiodurans. Cell 136:1044–1055

    Article  CAS  PubMed  Google Scholar 

  • Spies M, Kowalczykowski SC (2005) Homologous recombination by the RecBCD and RecF pathways. In: Higgins NP (ed) The bacterial chromosome. ASM Press, Washington, DC, pp 389–403

    Google Scholar 

  • Takami H, Nakasone K, Takaki Y, Maeno G, Sasaki R, Masui N, Fuji F, Hirama C, Nakamura Y, Ogasawara N, Kuhara S, Horikoshi K (2000) Complete genome sequence of the alkaliphilic bacterium Bacillus halodurans and genomic sequence comparison with Bacillus subtilis. Nucleic Acids Res 28:4317–4331

    Article  CAS  PubMed  Google Scholar 

  • Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:1–14

    Article  Google Scholar 

  • Taylor AF, Smith GR (2003) RecBCD enzyme is a DNA helicase with fast and slow motors of opposite polarity. Nature 423:889–893

    Article  CAS  PubMed  Google Scholar 

  • Thaler DS, Sampson E, Siddiqi I, Rosenberg SM, Thomason LC, Stahl FW, Stahl MM (1989) Recombination of bacteriophage lambda in recD mutants of Escherichia coli. Genome 31:53–67

    CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  Google Scholar 

  • White O, Eisen JA, Heidelberg JF, Hickey EK, Peterson JD, Dodson RJ, Haft DH, Gwinn ML, Nelson WC, Richardson DL, Moffat KS, Qin H, Jiang L, Pamphile W, Crosby M, Shen M, Vamathevan JJ, Lam P, McDonald L, Utterback T, Zalewski C, Makarova KS, Aravind L, Daly MJ, Fraser CM et al (1999) Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286:1571–1577

    Article  CAS  PubMed  Google Scholar 

  • Willetts NS, Mount DW (1969) Genetic analysis of recombination-deficient mutants of Escherichia coli K-12 carrying rec mutations cotransducible with thyA. J Bacteriol 100:923–934

    CAS  PubMed  Google Scholar 

  • Yu M, Souaya J, Julin DA (1998) The 30-kDa C-terminal domain of the RecB protein is critical for the nuclease activity, but not the helicase activity, of the RecBCD enzyme from Escherichia coli. Proc Natl Acad Sci USA 95:981–986

    Article  CAS  PubMed  Google Scholar 

  • Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298

    Article  Google Scholar 

  • Zhou Q, Zhang X, Xu H, Xu B, Hua Y (2007) A new role of Deinococcus radiodurans RecD in antioxidant pathway. FEMS Microbiol Lett 271:118–125

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was supported by the Office of Science (BER), U.S. Department of Energy, Grant No. DE-FC02-02ER63453. We graciously acknowledge Dr. John Battista and Dr. Mary Lidstrom for generously providing reagents. We thank Mr. Jim Puhl of NIST for his help with the ionizing radiation experiments. We are grateful to members of the Synthetic Biology group at the J. Craig Venter Institute, especially Dr. John Glass, Dr. Chuck Merryman and Ms. Cindi Pfannkoch for stimulating discussions. We thank Mikkel Algire and Radha Krishnakumar for critical reading of this manuscript. We thank Jonathan Badger for his phylipFasta script and general help and advice on constructing a recD phylogeny.

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Correspondence to Ray-Yuan Chuang or Sanjay Vashee.

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Montague, M., Barnes, C., Smith, H.O. et al. The Evolution of RecD Outside of the RecBCD Complex. J Mol Evol 69, 360–371 (2009). https://doi.org/10.1007/s00239-009-9290-x

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