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There Are More Small Amino Acids and Fewer Aromatic Rings in Proteins of Ionizing Radiation-Resistant Bacteria

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There Are More Small Amino Acids and Fewer Aromatic Rings in Proteins of Ionizing Radiation-Resistant Bacteria Ann Microbiol (2013) 63:1483–1491 DOI 10.1007/s13213-013-0612-2 ORIGINAL ARTICLE There are more small amino acids and fewer aromatic rings in proteins of ionizing radiation-resistant bacteria Haïtham Sghaier & Steinar Thorvaldsen & Nadia Malek Saied Received: 5 September 2012 /Accepted: 25 January 2013 /Published online: 17 February 2013 # Springer-Verlag Berlin Heidelberg and the University of Milan 2013 Abstract The identification of specific amino acids (AAs) Introduction or groups of functionally important AA residues in ionizing radiation-resistant bacteria (IRRB) is an important challenge Ionizing radiation (IR) resistance has been observed in a broad in understanding the biological basis of resistance to ioniz- range of eubacteria, including the Deinococcus-Thermus phy- ing radiation (IR; X-rays and gamma-rays). To address this lum (many Deinococcus sp. and Truepera radiovictrix) problem, we compared homologous sites in multiple align- (Albuquerque et al. 2005), Actinobacteria (Rubrobacter radio- ments of proteins of IRRB and IR-sensitive bacteria (IRSB) tolerans, Rubrobacter xylanophilus and Kineococcus radio- using the DeltaProt Toolbox. Substitution patterns were tolerans) (Chen et al. 2004; Ferreira et al. 1999; Phillips used as evidence for selection of certain AAs over others. et al. 2002; Yoshinaka et al. 1973), Proteobacteria Our results show that, in contrast to aromatic AAs, small/- (Methylobacterium radiotolerans and Acinetobacter radiore- tiny AAs tend to be preferred in IRRB compared to IRSB. In sistens) (Ito and Iizuka 1971; Nishimura et al. 1994), agreement with previous experimental data showing that Cyanobacteria (Chroococcidiopsis sp.) (Billi et al. 2000)and oxidation of AA residues is causative in the killing of Sphingobacteria (Hymenobacter actinosclerus) (Collins et al. irradiated cells and that IR resistance is correlated with the 2000). Presently, IR-resistant bacteria (IRRB) with completely accumulation of divalent manganese ions (Mn2+)–peptide– sequenced genomes (Liolios et al. 2010) and with published orthophosphate (Pi) complexes, we proposed a chemical information regarding their radioresistance are limited in num- interpretation based on the Hard and Soft (Lewis) Acids ber and restricted in genera: Deinococcus deserti VCD115 and Bases (HSAB) concept. These findings should assist (Baudet et al. 2010; de Groot et al. 2005; de Groot et al. future efforts in selecting mutations for rational design of 2009), Deinococcus geothermalis DSM 11300 (Makarova et proteins with enhanced IR tolerance properties. al. 2007), Deinococcus maricopensis DSM21211(Pukalletal. 2011), Deinococcus proteolyticus MRP (Copeland et al. 2012), Keywords Amino acids . Comparative genomics . Ionizing Deinococcus radiodurans R1 (White et al. 1999), Kineococcus radiation . Resistant bacteria radiotolerans SRS30216 (Bagwell et al. 2008), Rubrobacter xylanophilus DSM 9941 (Ferreira et al. 1999; Liolios et al. Haïtham Sghaier and Steinar Thorvaldsen contributed equally to this 2010)andTruepera radiovictrix DSM 17093 (Ivanova et al. work. 2011). In particular, IR resistance of bacteria belonging to the : H. Sghaier (*) N. M. Saied three genera Deinococcus, Kineococcus and Rubrobacter has Research Unit UR04CNSTN01 “Medical and Agricultural been well studied (Bagwell et al. 2008; Daly 2009; Ferreira et ” Applications of Nuclear Techniques , National Center for Nuclear al. 1999). Presently, strong lines of evidence from different Sciences and Technology (CNSTN), Sidi Thabet Technopark, 2020 Sidi Thabet, Tunisia laboratories have converged to the conclusion that the accu- e-mail: [email protected] mulation of Mn2+–peptide (7–22 amino acids in length in D. – N. M. Saied radiodurans) Pi complexes represents a widespread strategy e-mail: [email protected] for protecting irradiated cytosolic enzymes from reactive oxy- gen species (ROS) (Daly 2012;Dalyetal.2010, and references S. Thorvaldsen therein). Thus, extreme IR resistance in bacteria consistently University of Tromsø, Breivika, 9037 Tromsø, Norway coincides with greatly diminished susceptibilities to oxidation e-mail: [email protected] of amino acid (AA) residues compared to IR-sensitive species 1484 Ann Microbiol (2013) 63:1483–1491 (Daly 2012). Here, our aim is to investigate functionally im- Materials and methods portant AAs in IRRB compared to IR-sensitive bacteria (IRSB). In the present study, we determined whether the AA compo- In the context of understanding the biological basis of sition inferred for a set of proteins in three IRRB different resistance phenotypes, recent research in computa- [Deinococcus radiodurans R1 (White et al. 1999); tional biology has allowed the identification of the pheno- Kineococcus radiotolerans SRS30216 (Phillips et al. 2002) types of organisms based on the propensity of AAs to enter and Rubrobacter xylanophilus DSM 9941 (BioProject acces- more frequently into the proteins of thermophiles/hyperther- sion PRJNA58057)] was similar to the composition of an mophiles (Di Giulio 2000), barophiles/non-barophiles (Di identical set of proteins in three IRSB [Escherichia coli K- Giulio 2005a), acidophiles/alkaliphiles (Di Giulio 2005b), 12 (Blattner et al. 1997); Thermus thermophilus HB27 (Henne aerobic/anaerobic cells (Archetti and Di Giulio 2007), mes- et al. 2004)andPseudomonas putida F1 (BioProject acces- ophiles/psychrophiles (Thorvaldsen et al. 2007) and meth- sion PRJNA58355)]. In brief, a total of 31 basal DNA repair- anophiles/non-methanophiles (Di Giulio 2009). In addition, related proteins of D. radiodurans were selected (Sghaier et the current literature provides substitution preferences of al. 2008). Orthologs were obtained using the default settings AAs that lead to the adaptation of proteins to temperature of the Basic Local Alignment Search Tool (BLAST) at the (McDonald 2001; Metpally and Reddy 2009; McDonald National Center for Biotechnology Information (NCBI) web- 2010; Saunders et al. 2003; Pasamontes and Garcia-Vallve site (Altschul et al. 1990). Multiple alignments were con- 2006; Nakashima et al. 2003). Similarly, identification of structed using the ClustalW multiple sequence alignment AAs, which if damaged by radiolysis leads to loss of enzy- program (Thompson et al. 1994). Each of the six types of matic activity, and the determination of whether particular organisms was represented with only one sequence in each AA are favored by selection at high IR doses over others, alignment by assuming no horizontal gene transfer and, hence, have long been an objective in radiobiology and protein obtained a reasonably independent dataset in the sense that all evolution research (Garrison 1987; Rea et al. 2011). sequences belonged to different phylogenetic orders. All Radiation-induced decomposition of water generates several alignments were inspected and verified manually for a mini- reactive species [e.g., hydrogen peroxide (H2O2), hydroxyl mum cut-off score of 20 % identity with all other sequences. • • radical (HO ), hydroperoxyl radical (HO 2), hydrated elec- Five proteins (DR_0856, DR_1244, DR_0099, DR_2285, − + tron (e aq) and proton (H )], which, in the presence of and DR_2584) with low identity had to be eliminated because • •− oxygen, react further so that HO and superoxide (O2 ) of uncertain alignments. The final dataset consisted of multi- are essentially the only species present in oxygenated aque- ple alignments of 26 proteins; each of 3 IRRB plus 3 IRSB ous solutions (Draganić 2005). HO• is known to be far more AA sequences. We also grouped the AAs into 12 property •− • reactive than O2 ; therefore, the major fraction of HO is groups (Taylor 1986) as follows: the acidic AA group includ- removed by the most reactive sites. In proteins, aromatic, ed aspartic acid (D) and glutamic acid (E); aliphatic: isoleu- sulfur-containing and aliphatic AA side chains are known to cine (I), leucine (L) and valine (V); aromatic: histidine (H), be the main targets of HO•-mediated damage. Aliphatic AAs phenylalanine (F), W and tyrosine (Y); basic: arginine (R), H, become more reactive with an increasing number of methyl and lysine (K); charged: R, D, E, H and K; hydrophilic: D, E, groups, but the reaction with aromatic AA residues is faster K, asparagine (N), glutamine (Q) and R; hydrophobic: alanine and easier for addition of HO• to double bonds, with tryp- (A), cysteine (C), F, I, L, methionine (M), valine (V), Wand Y; tophan (W) residues being the most prone to oxidative neutral: glycine (G), Q, serine (S) and threonine (T); non- damage by ROS (Stadtman and Levine 2003). Thus, resis- polar: A, C, G, I, L, M, F, P, V, W and Y; polar: R, N, D, E, Q, tance to radical-induced damage might be related to the H, K, S and T; small: A, C, D, G, N, P, S and V; and tiny: A, G substitution of residues highly prone to oxidative damage and S. We applied the new methods of comparative statistical with residues less prone. In order to support this hypothesis, bioinformatics as described in a recent paper by Thorvaldsen we examined different AA compositions of proteins of et al. (2010), and AA composition and substitution were IRRB and IRSB. calculated and analyzed using the DeltaProt Toolbox. Using orthologous sequences clustering along with the To analyze changes in AA composition, we applied the DeltaProt, a software toolbox for comparative genomics, we nonparametric Wilcoxon paired test, which was not restrict- conducted an analysis of multiple alignments of DNA repair ed to the assumption of statistical independence within
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