Skip to main content
SpringerLink
Log in

There are more small amino acids and fewer aromatic rings in proteins of ionizing radiation-resistant bacteria

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

The identification of specific amino acids (AAs) or groups of functionally important AA residues in ionizing radiation-resistant bacteria (IRRB) is an important challenge in understanding the biological basis of resistance to ionizing radiation (IR; X-rays and gamma-rays). To address this problem, we compared homologous sites in multiple alignments of proteins of IRRB and IR-sensitive bacteria (IRSB) using the DeltaProt Toolbox. Substitution patterns were used as evidence for selection of certain AAs over others. Our results show that, in contrast to aromatic AAs, small/tiny AAs tend to be preferred in IRRB compared to IRSB. In agreement with previous experimental data showing that oxidation of AA residues is causative in the killing of irradiated cells and that IR resistance is correlated with the accumulation of divalent manganese ions (Mn2+)–peptide–orthophosphate (Pi) complexes, we proposed a chemical interpretation based on the Hard and Soft (Lewis) Acids and Bases (HSAB) concept. These findings should assist future efforts in selecting mutations for rational design of proteins with enhanced IR tolerance properties.

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

Similar content being viewed by others

References

  • Albuquerque L, Simoes C, Nobre MF, Pino NM, Battista JR, Silva MT, Rainey FA, da Costa MS (2005) Truepera radiovictrix gen. nov., sp. nov., a new radiation resistant species and the proposal of Trueperaceae fam. nov. FEMS Microbiol Lett 247(2):161–169

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410

    PubMed  CAS  Google Scholar 

  • Archetti M, Di Giulio M (2007) The evolution of the genetic code took place in an anaerobic environment. J Theor Biol 245(1):169–174

    Article  PubMed  CAS  Google Scholar 

  • Bagwell CE, Bhat S, Hawkins GM, Smith BW, Biswas T, Hoover TR, Saunders E, Han CS, Tsodikov OV, Shimkets LJ (2008) Survival in nuclear waste, extreme resistance, and potential applications gleaned from the genome sequence of Kineococcus radiotolerans SRS30216. PLoS One 3(12):e3878

    Article  PubMed  Google Scholar 

  • Barnese K, Gralla EB, Cabelli DE, Valentine JS (2008) Manganous phosphate acts as a superoxide dismutase. J Am Chem Soc 130(14):4604–4606

    Article  PubMed  CAS  Google Scholar 

  • Baudet M, Ortet P, Gaillard JC, Fernandez B, Guerin P, Enjalbal C, Subra G, de Groot A, Barakat M, Dedieu A, Armengaud J (2010) Proteomics-based refinement of Deinococcus deserti genome annotation reveals an unwonted use of non-canonical translation initiation codons. Mol Cell Proteomics 9(2):415–426

    Article  PubMed  CAS  Google Scholar 

  • Billi D, Friedmann EI, Hofer KG, Caiola MG, Ocampo-Friedmann R (2000) Ionizing-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Appl Environ Microbiol 66(4):1489–1492

    Article  PubMed  CAS  Google Scholar 

  • Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The complete genome sequence of Escherichia coli K-12. Science 5331:1453–1462

    Article  Google Scholar 

  • Chakravarty S, Varadarajan R (2000) Elucidation of determinants of protein stability through genome sequence analysis. FEBS Lett 470(1):65–69

    Article  PubMed  CAS  Google Scholar 

  • Chatgilialoglu C, Ferreri C, Torreggiani A, Salzano AM, Renzone G, Scaloni A (2011) Radiation-induced reductive modifications of sulfur-containing amino acids within peptides and proteins. J Proteome 74(11):2264–2273

    Article  CAS  Google Scholar 

  • Chen MY, Wu SH, Lin GH, Lu CP, Lin YT, Chang WC, Tsay SS (2004) Rubrobacter taiwanensis sp. nov., a novel thermophilic, radiation-resistant species isolated from hot springs. Int J Syst Evol Microbiol 54(Pt 5):1849–1855

    Article  PubMed  CAS  Google Scholar 

  • Collins MD, Hutson RA, Grant IR, Patterson MF (2000) Phylogenetic characterization of a novel radiation-resistant bacterium from irradiated pork: description of Hymenobacter actinosclerus sp. nov. Int J Syst Evol Microbiol 50(Pt 2):731–734

    Article  PubMed  Google Scholar 

  • Copeland A, Zeytun A, Yassawong M, Nolan M, Lucas S, Hammon N, Deshpande S, Cheng JF, Han C, Tapia R, Goodwin LA, Pitluck S, Mavromatis K, Liolios K, Pagani I, Ivanova N, Mikhailova N, Pati A, Chen A, Palaniappan K, Land M, Hauser L, Jeffries CD, Brambilla EM, Rohde M, Sikorski J, Pukall R, Goker M, Detter JC, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP, Lapidus A (2012) Complete genome sequence of the orange-red pigmented, radioresistant Deinococcus proteolyticus type strain (MRP(T)). Stand Genomic Sci 6(2):240–250

    Article  PubMed  Google Scholar 

  • Daly MJ (2009) A new perspective on radiation resistance based on Deinococcus radiodurans. Nat Rev Microbiol 7(3):237–245

    Article  PubMed  CAS  Google Scholar 

  • Daly MJ (2012) Death by protein damage in irradiated cells. DNA Repair 11(1):12–21

    Article  PubMed  CAS  Google Scholar 

  • Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Leapman RD, Lai B, Ravel B, Li SM, Kemner KM, Fredrickson JK (2007) Protein oxidation implicated as the primary determinant of bacterial radioresistance. PLoS Biol 5(4):e92

    Article  PubMed  Google Scholar 

  • Daly MJ, Gaidamakova EK, Matrosova VY, Kiang JG, Fukumoto R, Lee DY, Wehr NB, Viteri GA, Berlett BS, Levine RL (2010) Small-molecule antioxidant proteome-shields in Deinococcus radiodurans. PLoS One 5(9):e12570

    Article  PubMed  Google Scholar 

  • de Groot A, Chapon V, Servant P, Christen R, Saux MF, Sommer S, Heulin T (2005) Deinococcus deserti sp. nov., a gamma-radiation-tolerant bacterium isolated from the Sahara Desert. Int J Syst Evol Microbiol 55(Pt 6):2441–2446

    Article  PubMed  Google Scholar 

  • de Groot A, Dulermo R, Ortet P, Blanchard L, Guerin P, Fernandez B, Vacherie B, Dossat C, Jolivet E, Siguier P, Chandler M, Barakat M, Dedieu A, Barbe V, Heulin T, Sommer S, Achouak W, Armengaud J (2009) Alliance of proteomics and genomics to unravel the specificities of Sahara bacterium Deinococcus deserti. PLoS Genet 5(3):e1000434

    Article  PubMed  Google Scholar 

  • Di Giulio M (2000) The universal ancestor lived in a thermophilic or hyperthermophilic environment. J Theor Biol 203(3):203–213

    Article  PubMed  Google Scholar 

  • Di Giulio M (2005a) The ocean abysses witnessed the origin of the genetic code. Gene 346:7–12

    Article  PubMed  Google Scholar 

  • Di Giulio M (2005b) Structuring of the genetic code took place at acidic pH. J Theor Biol 237(2):219–226

    Article  PubMed  Google Scholar 

  • Di Giulio M (2009) A methanogen hosted the origin of the genetic code. J Theor Biol 260(1):77–82

    Article  PubMed  Google Scholar 

  • Draganić IG (2005) Radiolysis of water: a look at its origin and occurrence in the nature. Radiat Phys Chem 72:181–186

    Article  Google Scholar 

  • Ferreira AC, Nobre MF, Moore E, Rainey FA, Battista JR, da Costa MS (1999) Characterization and radiation resistance of new isolates of Rubrobacter radiotolerans and Rubrobacter xylanophilus. Extremophiles 3(4):235–238

    Article  PubMed  CAS  Google Scholar 

  • Garrison WM (1987) Reaction mechanisms in the radiolysis of peptides, polypeptides, and proteins. Chem Rev 87:381–398

    Article  CAS  Google Scholar 

  • Henne A, Bruggemann H, Raasch C, Wiezer A, Hartsch T, Liesegang H, Johann A, Lienard T, Gohl O, Martinez-Arias R, Jacobi C, Starkuviene V, Schlenczeck S, Dencker S, Huber R, Klenk HP, Kramer W, Merkl R, Gottschalk G, Fritz HJ (2004) The genome sequence of the extreme thermophile Thermus thermophilus. Nat Biotechnol 22(5):547–553

    Article  PubMed  CAS  Google Scholar 

  • Ito H, Iizuka H (1971) Taxonomic studies on a radio-resistant Pseudomonas. Part XII. Studies on the microorganisms of cereal grain. Agric Biol Chem 35(10):1566–1571

    Article  Google Scholar 

  • Ivanova N, Rohde C, Munk C, Nolan M, Lucas S, Del Rio TG, Tice H, Deshpande S, Cheng JF, Tapia R, Han C, Goodwin L, Pitluck S, Liolios K, Mavromatis K, Mikhailova N, Pati A, Chen A, Palaniappan K, Land M, Hauser L, Chang YJ, Jeffries CD, Brambilla E, Rohde M, Goker M, Tindall BJ, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP, Lapidus A (2011) Complete genome sequence of Truepera radiovictrix type strain (RQ-24). Stand Genomic Sci 4(1):91–99

    Article  PubMed  CAS  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8(3):275–282

    PubMed  CAS  Google Scholar 

  • Liolios K, Chen IM, Mavromatis K, Tavernarakis N, Hugenholtz P, Markowitz VM, Kyrpides NC (2010) The Genomes On Line Database (GOLD) in 2009: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res 38:D346–D354

    Article  PubMed  CAS  Google Scholar 

  • Makarova KS, Omelchenko MV, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Lapidus A, Copeland A, Kim E, Land M, Mavrommatis K, Pitluck S, Richardson PM, Detter C, Brettin T, Saunders E, Lai B, Ravel B, Kemner KM, Wolf YI, Sorokin A, Gerasimova AV, Gelfand MS, Fredrickson JK, Koonin EV, Daly MJ (2007) Deinococcus geothermalis: the pool of extreme radiation resistance genes shrinks. PLoS One 2(9):e955

    Article  PubMed  Google Scholar 

  • McDonald JH (2001) Patterns of temperature adaptation in proteins from the bacteria Deinococcus radiodurans and Thermus thermophilus. Mol Biol Evol 18(5):741–749

    Article  PubMed  CAS  Google Scholar 

  • McDonald JH (2010) Temperature adaptation at homologous sites in proteins from nine thermophile-mesophile species pairs. Genome Biol Evol 2:267–276

    Article  PubMed  Google Scholar 

  • McNaughton RL, Reddi AR, Clement MH, Sharma A, Barnese K, Rosenfeld L, Gralla EB, Valentine JS, Culotta VC, Hoffman BM (2010) Probing in vivo Mn2+ speciation and oxidative stress resistance in yeast cells with electron-nuclear double resonance spectroscopy. Proc Natl Acad Sci USA 107(35):15335–15339

    Article  PubMed  CAS  Google Scholar 

  • Metpally RP, Reddy BV (2009) Comparative proteome analysis of psychrophilic versus mesophilic bacterial species: Insights into the molecular basis of cold adaptation of proteins. BMC Genomics 10:11

    Article  PubMed  Google Scholar 

  • Nakashima H, Fukuchi S, Nishikawa K (2003) Compositional changes in RNA, DNA and proteins for bacterial adaptation to higher and lower temperatures. J Biochem 133(4):507–513

    Article  PubMed  CAS  Google Scholar 

  • Nishimura Y, Uchida K, Tanaka K, Ino T, Ito H (1994) Radiation sensitivities of Acinetobacter strains isolated from clinical sources. J Basic Microbiol 34(5):357–360

    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 

  • Pasamontes A, Garcia-Vallve S (2006) Use of a multi-way method to analyze the amino acid composition of a conserved group of orthologous proteins in prokaryotes. BMC Bioinforma 7:257

    Article  Google Scholar 

  • Pearson RG (1963) Hard and soft acids and bases. J Am Chem Soc 85:3533–3543

    Article  CAS  Google Scholar 

  • Phillips RW, Wiegel J, Berry CJ, Fliermans C, Peacock AD, White DC, Shimkets LJ (2002) Kineococcus radiotolerans sp. nov., a radiation-resistant, gram-positive bacterium. Int J Syst Evol Microbiol 52(Pt 3):933–938

    Article  PubMed  CAS  Google Scholar 

  • Pride DT, Meinersmann RJ, Wassenaar TM, Blaser MJ (2003) Evolutionary implications of microbial genome tetranucleotide frequency biases. Genome Res 13(2):145–158

    Article  PubMed  CAS  Google Scholar 

  • Pukall R, Zeytun A, Lucas S, Lapidus A, Hammon N, Deshpande S, Nolan M, Cheng JF, Pitluck S, Liolios K, Pagani I, Mikhailova N, Ivanova N, Mavromatis K, Pati A, Tapia R, Han C, Goodwin L, Chen A, Palaniappan K, Land M, Hauser L, Chang YJ, Jeffries CD, Brambilla EM, Rohde M, Goker M, Detter JC, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP (2011) Complete genome sequence of Deinococcus maricopensis type strain (LB-34). Stand Genomic Sci 4(2):163–172

    Article  PubMed  CAS  Google Scholar 

  • Rea G, Lambreva M, Polticelli F, Bertalan I, Antonacci A, Pastorelli S, Damasso M, Johanningmeier U, Giardi MT (2011) Directed evolution and in silico analysis of reaction centre proteins reveal molecular signatures of photosynthesis adaptation to radiation pressure. PLoS One 6(1):e16216

    Article  PubMed  CAS  Google Scholar 

  • Saunders NF, Thomas T, Curmi PM, Mattick JS, Kuczek E, Slade R, Davis J, Franzmann PD, Boone D, Rusterholtz K, Feldman R, Gates C, Bench S, Sowers K, Kadner K, Aerts A, Dehal P, Detter C, Glavina T, Lucas S, Richardson P, Larimer F, Hauser L, Land M, Cavicchioli R (2003) Mechanisms of thermal adaptation revealed from the genomes of the Antarctic Archaea Methanogenium frigidum and Methanococcoides burtonii. Genome Res 13(7):1580–1588

    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 

  • Sghaier H, Satoh K, Ohba H, Narumi I (2010) Assessing the role of RecA protein in the radioresistant bacterium Deinococcus geothermalis. Afr J Biochem Res 4(4):111–118

    CAS  Google Scholar 

  • Sghaier H, Satoh K, Narumi I (2011) In silico method to predict functional similarity between two RecA orthologs. J Biomol Screen 16(4):457–459

    Article  PubMed  CAS  Google Scholar 

  • Stadtman ER (1993) Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu Rev Biochem 62:797–821

    Article  PubMed  CAS  Google Scholar 

  • Stadtman ER, Levine RL (2003) Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25(3–4):207–218

    Article  PubMed  CAS  Google Scholar 

  • Taylor WR (1986) The classification of amino acid conservation. J Theor Biol 119(2):205–218

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Thorvaldsen S, Hjerde E, Fenton C, Willassen NP (2007) Molecular characterization of cold adaptation based on ortholog protein sequences from Vibrionaceae species. Extremophiles 11(5):719–732

    Article  PubMed  CAS  Google Scholar 

  • Thorvaldsen S, Fla T, Willassen NP (2010) DeltaProt: a software toolbox for comparative genomics. BMC Bioinformatics 11:573

    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 

  • Yoshinaka T, Yano K, Yamaguchi H (1973) Isolation of highly radioresistant bacterium, Arthrobacter radiotolerans nov.sp. Agric Biol Chem 37(10):2269–2275

  • Yun YS, Lee YN (2004) Purification and some properties of superoxide dismutase from Deinococcus radiophilus, the UV-resistant bacterium. Extremophiles 8(3):237–242

    Google Scholar 

Download references

Acknowledgments

This work was performed under the auspices of the Tunisian National Centre for Nuclear Science and Technology (CNSTN) in collaboration with the Norwegian University of Tromsø.

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

H.S. and S.T. conceived the study and compiled the data. S.T. developed algorithms and performed calculations. H.S. and S.T. analyzed the results and wrote the paper. N.M.S. performed chemical analyses. All authors have approved the final version.

Author information

Authors and Affiliations

  1. Research Unit UR04CNSTN01 “Medical and Agricultural Applications of Nuclear Techniques”, National Center for Nuclear Sciences and Technology (CNSTN), Sidi Thabet Technopark, 2020, Sidi Thabet, Tunisia

    Haïtham Sghaier & Nadia Malek Saied

  2. University of Tromsø, Breivika, 9037, Tromsø, Norway

    Steinar Thorvaldsen

Authors
  1. Haïtham Sghaier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Steinar Thorvaldsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nadia Malek Saied
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Haïtham Sghaier.

Additional information

Haïtham Sghaier and Steinar Thorvaldsen contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sghaier, H., Thorvaldsen, S. & Saied, N.M. There are more small amino acids and fewer aromatic rings in proteins of ionizing radiation-resistant bacteria. Ann Microbiol 63, 1483–1491 (2013). https://doi.org/10.1007/s13213-013-0612-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-013-0612-2

Keywords

Search

Navigation