Skip to main content
SpringerLink
Log in

Hypothetical Proteins Present During Recovery Phase of Radiation Resistant Bacterium Deinococcus radiodurans are Under Purifying Selection

  • Original Article
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Deinococcus radiodurans has an unusual capacity to recover from intense doses of ionizing radiation. The DNA repair proteins of this organism play an important role in repairing the heavily damaged DNA by employing a novel mechanism of DNA double-strand break repair. An earlier report stated that genes of many of these repair proteins are under positive selection implying that these genes have a tendency to mutate, which in turn provides selective advantage to this bacterium. Several “hypothetical proteins” are also present during the recovery phase and some of them have also been shown for their roles in radiation resistance. Therefore, we tested the selection pressure on the genes encoding these poorly characterized proteins. Our results show that a number of “hypothetical proteins” present during the repair phase have structural adaptations compared to their orthologs and the genes encoding them as well as those for the DNA repair proteins present during this phase are under purifying selection. Evidence of purifying selection in these hypothetical proteins suggests that certain novel characteristics among these proteins are conserved and seem to be under functional constraints to perform important functions during recovery process after gamma radiation damage.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Anantharaman V, Aravind L (2002) The PRC-barrel: a widespread, conserved domain shared by photosynthetic reaction center subunits and proteins of RNA metabolism. Genome Biol 3(11):RESEARCH 0061

    Article  Google Scholar 

  • Anantharaman V, Koonin EV, Aravind L (2001) Regulatory potential, phyletic distribution and evolution of ancient, intracellular small-molecule-binding domains. J Mol Biol 307(5):1271–1292

    Article  PubMed  CAS  Google Scholar 

  • Basu B, Apte SK (2012) Gamma radiation-induced proteome of Deinococcus radiodurans primarily targets DNA repair and oxidative stress alleviation. Mol Cell Proteomics 11(1):M111 011734

    PubMed  Google Scholar 

  • Bennett CB, Lewis LK, Karthikeyan G, Lobachev KS, Jin YH, Sterling JF, Snipe JR, Resnick MA (2001) Genes required for ionizing radiation resistance in yeast. Nat Genet 29(4):426–434

    Article  PubMed  CAS  Google Scholar 

  • Bentchikou E, Servant P, Coste G, Sommer S (2010) A major role of the RecFOR pathway in DNA double-strand-break repair through ESDSA in Deinococcus radiodurans. PLoS Genet 6(1):e1000774

    Article  PubMed  Google Scholar 

  • Bielawski JP, Yang Z (2004) A maximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution. J Mol Evol 59(1):121–132

    Article  PubMed  CAS  Google Scholar 

  • Das AD, Misra HS (2011) Characterization of DRA0282 from Deinococcus radiodurans for its role in bacterial resistance to DNA damage. Microbiology 157(Pt 8):2196–2205

    Article  PubMed  CAS  Google Scholar 

  • Dingle KE, Colles FM, Wareing DR, Ure R, Fox AJ, Bolton FE, Bootsma HJ, Willems RJ, Urwin R, Maiden MC (2001) Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol 39(1):14–23

    Article  PubMed  CAS  Google Scholar 

  • Ge G, Cowen L, Feng X, Widmer G (2008) Protein coding gene nucleotide substitution pattern in the apicomplexan protozoa Cryptosporidium parvum and Cryptosporidium hominis. Comp Funct Genomics. doi:10.1155/2008/879023

    PubMed  Google Scholar 

  • Harris DR, Tanaka M, Saveliev SV, Jolivet E, Earl AM, Cox MM, Battista JR (2004) Preserving genome integrity: the DdrA protein of Deinococcus radiodurans R1. PLoS Biol 2(10):e304

    Article  PubMed  Google Scholar 

  • Hennig M, Schlesier B, Dauter Z, Pfeffer S, Betzel C, Hohne WE, Wilson KS (1992) A TIM barrel protein without enzymatic activity? Crystal-structure of narbonin at 1.8 A resolution. FEBS Lett 306(1):80–84

    Article  PubMed  CAS  Google Scholar 

  • Iwami J, Murakami Y, Nagano K, Nakamura H, Yoshimura F (2007) Further evidence that major outer membrane proteins homologous to OmpA in Porphyromonas gingivalis stabilize bacterial cells. Oral Microbiol Immunol 22(5):356–360

    Article  PubMed  CAS  Google Scholar 

  • Iyer LM, Koonin EV, Aravind L (2001) Adaptations of the helix-grip fold for ligand binding and catalysis in the START domain superfamily. Proteins 43(2):134–144

    Article  PubMed  CAS  Google Scholar 

  • Kalmokoff ML, Austin JW, Cyr TD, Hefford MA, Teather RM, Selinger LB (2009) Physical and genetic characterization of an outer-membrane protein (OmpM1) containing an N-terminal S-layer-like homology domain from the phylogenetically Gram-positive gut anaerobe Mitsuokella multacida. Anaerobe 15(3):74–81

    Article  PubMed  CAS  Google Scholar 

  • Kim JI, Cox MM (2002) The RecA proteins of Deinococcus radiodurans and Escherichia coli promote DNA strand exchange via inverse pathways. Proc Natl Acad Sci USA 99(12):7917–7921

    Article  PubMed  CAS  Google Scholar 

  • Kota S, Misra HS (2008) Identification of a DNA processing complex from Deinococcus radiodurans. Biochem Cell Biol 86(5):448–458

    Article  PubMed  CAS  Google Scholar 

  • Kota S, Kamble VA, Rajpurohit YS, Misra HS (2010) ATP-type DNA ligase requires other proteins for its activity in vitro and its operon components for radiation resistance in Deinococcus radiodurans in vivo. Biochem Cell Biol 88(5):783–790

    Article  PubMed  CAS  Google Scholar 

  • LaLonde JM, Bernlohr DA, Banaszak LJ (1994) The up-and-down beta-barrel proteins. FASEB J 8(15):1240–1247

    PubMed  CAS  Google Scholar 

  • Lan R, Reeves PR (2001) When does a clone deserve a name? A perspective on bacterial species based on population genetics. Trends Microbiol 9(9):419–424

    Article  PubMed  CAS  Google Scholar 

  • Leppanen VM, Tossavainen H, Permi P, Lehtio L, Ronnholm G, Goldman A, Kilpelainen I, Pihlajamaa T (2007) Crystal structure of the N-terminal NC4 domain of collagen IX, a zinc binding member of the laminin-neurexin-sex hormone binding globulin (LNS) domain family. J Biol Chem 282(32):23219–23230

    Article  PubMed  Google Scholar 

  • Lipton MS, Pasa-Tolic L, Anderson GA, Anderson DJ, Auberry DL, Battista JR, Daly MJ, Fredrickson J, Hixson KK, Kostandarithes H, Masselon C, Markillie LM, Moore RJ, Romine MF, Shen Y, Stritmatter E, Tolic N, Udseth HR, Venkateswaran A, Wong KK, Zhao R, Smith RD (2002) Global analysis of the Deinococcus radiodurans proteome by using accurate mass tags. Proc Natl Acad Sci USA 99(17):11049–11054

    Article  PubMed  CAS  Google Scholar 

  • 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(7):4191–4196

    Article  PubMed  CAS  Google Scholar 

  • Lu H, Gao G, Xu G, Fan L, Yin L, Shen B, Hua Y (2009) Deinococcus radiodurans PprI switches on DNA damage response and cellular survival networks after radiation damage. Mol Cell Proteomics 8(3):481–494

    Article  PubMed  CAS  Google Scholar 

  • Marina A, Waldburger CD, Hendrickson WA (2005) Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein. EMBO J 24(24):4247–4259

    Article  PubMed  CAS  Google Scholar 

  • Mennecier S, Servant P, Coste G, Bailone A, Sommer S (2006) Mutagenesis via IS transposition in Deinococcus radiodurans. Mol Microbiol 59(1):317–325

    Article  PubMed  CAS  Google Scholar 

  • Misra HS, Khairnar NP, Kota S, Shrivastava S, Joshi VP, Apte SK (2006) An exonuclease I-sensitive DNA repair pathway in Deinococcus radiodurans: a major determinant of radiation resistance. Mol Microbiol 59(4):1308–1316

    Article  PubMed  CAS  Google Scholar 

  • Narumi I, Satoh K, Cui S, Funayama T, Kitayama S, Watanabe H (2004) PprA: a novel protein from Deinococcus radiodurans that stimulates DNA ligation. Mol Microbiol 54(1):278–285

    Article  PubMed  CAS  Google Scholar 

  • Nekrutenko A, Makova KD, Li WH (2002) The K(A)/K(S) ratio test for assessing the protein-coding potential of genomic regions: an empirical and simulation study. Genome Res 12(1):198–202

    Article  PubMed  CAS  Google Scholar 

  • Nielsen R, Bustamante C, Clark AG, Glanowski S, Sackton TB, Hubisz MJ, Fledel-Alon A, Tanenbaum DM, Civello D, White TJ, Adams MD JJS, Cargill M (2005) A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol 3(6):e170

    Article  PubMed  Google Scholar 

  • Novichkov PS, Wolf YI, Dubchak I, Koonin EV (2009) Trends in prokaryotic evolution revealed by comparison of closely related bacterial and archaeal genomes. J Bacteriol 191(1):65–73

    Article  PubMed  CAS  Google Scholar 

  • Omelchenko MV, Wolf YI, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Daly MJ, Koonin EV, Makarova KS (2005) Comparative genomics of Thermus thermophilus and Deinococcus radiodurans: divergent routes of adaptation to thermophily and radiation resistance. BMC Evol Biol 5:57

    Article  PubMed  Google Scholar 

  • Petersen L, Bollback JP, Dimmic M, Hubisz M, Nielsen R (2007) Genes under positive selection in Escherichia coli. Genome Res 17(9):1336–1343

    Article  PubMed  CAS  Google Scholar 

  • Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, Muller J, Arnold R, Rattei T, Letunic I, Doerks T, Jensen LJ, von Mering C, Bork P (2012) eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res 40(Database issue):D284-289

    Google Scholar 

  • Price MS, Chao LY, Marletta MA (2007) Shewanella oneidensis MR-1 H-NOX regulation of a histidine kinase by nitric oxide. Biochemistry 46(48):13677–13683

    Article  PubMed  CAS  Google Scholar 

  • Puehringer S, RoseFigura J, Metlitzky M, Toyama H, Klinman JP, Schwarzenbacher R (2008) Structural studies of mutant forms of the PQQ-forming enzyme PqqC in the presence of product and substrate. Proteins 78(11):2554–2562

    Google Scholar 

  • Rothfuss H, Lara JC, Schmid AK, Lidstrom ME (2006) Involvement of the S-layer proteins Hpi and SlpA in the maintenance of cell envelope integrity in Deinococcus radiodurans R1. Microbiology 152(Pt 9):2779–2787

    Article  PubMed  CAS  Google Scholar 

  • Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5(4):725–738

    Article  PubMed  CAS  Google Scholar 

  • Sghaier H, Ghedira K, Benkahla A, Barkallah I (2008) Basal DNA repair machinery is subject to positive selection in ionizing-radiation-resistant bacteria. BMC Genomics 9:297

    Article  PubMed  Google Scholar 

  • Siebold C, Arnold I, Garcia-Alles LF, Baumann U, Erni B (2003) Crystal structure of the Citrobacter freundii dihydroxyacetone kinase reveals an eight-stranded alpha-helical barrel ATP-binding domain. J Biol Chem 278(48):48236–48244

    Article  PubMed  CAS  Google Scholar 

  • Siew N, Fischer D (2003) Unravelling the ORFan puzzle. Comp Funct Genomics 4(4):432–441

    Article  PubMed  CAS  Google Scholar 

  • Slade D, Radman M (2011) Oxidative stress resistance in Deinococcus radiodurans. Microbiol Mol Biol Rev 75(1):133–191

    Article  PubMed  CAS  Google Scholar 

  • Slade D, Lindner AB, Paul G, Radman M (2009) Recombination and replication in DNA repair of heavily irradiated Deinococcus radiodurans. Cell 136(6):1044–1055

    Article  PubMed  CAS  Google Scholar 

  • Soding J (2005) Protein homology detection by HMM–HMM comparison. Bioinformatics 21(7):951–960

    Article  PubMed  Google Scholar 

  • Soyer Y, Orsi RH, Rodriguez-Rivera LD, Sun Q, Wiedmann M (2009) Genome wide evolutionary analyses reveal serotype specific patterns of positive selection in selected Salmonella serotypes. BMC Evol Biol 9:264

    Article  PubMed  Google Scholar 

  • Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34(Web Server issue):W609-612

    Google Scholar 

  • Tai V, Poon AF, Paulsen IT, Palenik B (2011) Selection in coastal Synechococcus (cyanobacteria) populations evaluated from environmental metagenomes. PLoS ONE 6(9):e24249

    Article  PubMed  CAS  Google Scholar 

  • Tanaka A, Hirano H, Kikuchi M, Kitayama S, Watanabe H (1996) Changes in cellular proteins of Deinococcus radiodurans following gamma-irradiation. Radiat Environ Biophys 35(2):95–99

    Article  PubMed  Google Scholar 

  • Tanaka M, Earl AM, Howell HA, Park M-J, Eisen JA, Peterson SN, Battista JR (2004) Analysis of Deinococcus radiodurans’ transcriptional response to ionizing radiation and desiccation reveals novel proteins that contribute to extreme radioresistance. Genetics 168:21–33

    Article  PubMed  Google Scholar 

  • Tautz D, Domazet-Loso T (2011) The evolutionary origin of orphan genes. Nat Rev Genet 12(10):692–702

    Article  PubMed  CAS  Google Scholar 

  • Wallace JG, Zhou Z, Breaker RR (2012) OLE RNA protects extremophilic bacteria from alcohol toxicity. Nucleic Acids Res 40(14):6898–6907

    Article  PubMed  CAS  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, Minton KW, Fleischmann RD, Ketchum KA, Nelson KE, Salzberg S, Smith HO, Venter JC, Fraser CM (1999) Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286(5444):1571–1577

    Article  PubMed  CAS  Google Scholar 

  • Yamamura A, Okada A, Kameda Y, Ohtsuka J, Nakagawa N, Ebihara A, Nagata K, Tanokura M (2009) Structure of TTHA1623, a novel metallo-beta-lactamase superfamily protein from Thermus thermophilus HB8. Acta Crystallogr Sect F Struct Biol Cryst Commun 65(Pt 5):455–459

    Article  PubMed  CAS  Google Scholar 

  • Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24(8):1586–1591

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, dos Reis M (2011) Statistical properties of the branch-site test of positive selection. Mol Biol Evol 28(3):1217–1228

    Article  PubMed  CAS  Google Scholar 

  • Zhang C, Wei J, Zheng Z, Ying N, Sheng D, Hua Y (2005) Proteomic analysis of Deinococcus radiodurans recovering from gamma-irradiation. Proteomics 5(1):138–143

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. S. K. Apte, for his constant support and encouragement while pursuing this work.

Author information

Authors and Affiliations

  1. Molecular Biology Division, Bhabha Atomic Research Centre, Mumbai, 400085, India

    Anubrata D. Das & Hari S. Misra

Authors
  1. Anubrata D. Das
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hari S. Misra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hari S. Misra.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material (DOC 78 kb)

Supplementary material (DOC 490 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Das, A.D., Misra, H.S. Hypothetical Proteins Present During Recovery Phase of Radiation Resistant Bacterium Deinococcus radiodurans are Under Purifying Selection. J Mol Evol 77, 31–42 (2013). https://doi.org/10.1007/s00239-013-9577-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-013-9577-9

Keywords

Search

Navigation