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Uncorrected Proof ARTICLE IN PRESS FEMS Microbiology Letters 11035 (2003) 1^6 www.fems-microbiology.org 1 Retron reverse transcriptase rrtT is ubiquitous in strains of 2 Salmonella enterica serovar Typhimurium 3 Jitka Matiasovicova a, Marcela Faldynova a, Martina Pravcova a, Renata Karpiskova b, 4 Ivana Kolackova b, Jiri Damborsky c, Ivan Rychlik a;Ã 5 a Veterinary Research Institute, Hudcova 70, 621 32 Brno, Czech Republic 6 b National Institute of Public Health, Center for Food Chain Hygiene, Palackeho 1-3, 612 42 Brno, Czech Republic 7 c National Centre for Biomolecular Research, Masaryk University, Kotlarska 2, 611 37 Brno, Czech Republic 8 Received 19 March 2003; received in revised form 5 May 2003; accepted 5 May 2003 9 First published online 10 Abstract 11 Bacterial retron reverse transcriptases are unusual enzymes which utilise the same RNA molecule as a template and also as a primer for 12 initiation of the reverse transcription. Except for their relatively frequent presence in Myxococcus spp., they are considered as quite rare 13 proteins. However, in this study we proved that retron reverse transcriptase is frequently found in certain serovars of Salmonella enterica. 14 Using polymerase chain reaction (PCR), in strains of serovar Typhimurium, the rrtT (retron reverse transcriptase Typhimurium) gene was 15 detected in 158 out of 175 tested field strains. On the other hand, in none of the 18 tested serovar Enteritidis strains the rrtT was detected 16 in their genome. Detailed computer analysis allowed us to predict the sequence of msDNA and to propose that the final msDNA is free of 17 any RNA. Furthermore, we predict that there are at least three different classes of retron reverse transcriptases. 18 ß 2003 Published by Elsevier Science B.V. on behalf of the Federation of European Microbiological Societies. 19 20 Keywords: Retron reverse transcriptase; msDNA; Salmonella enterica serovar Typhimurium 21 22 1. Introduction inverted repeats designated as a1 and a2 play a central 38 role. Subsequently, the folded molecule is branched using 39 23 Certain bacterial species encode a speci¢c type of re- 2P-OH of guanosine residue at the 3P-end of the a2 repeat 40 24 verse transcriptases called retron reverse transcriptases and this branch is used as a primer for the initiation of 41 25 (RRTs). These have been frequently found in Myxococcus reverse transcription. As a result, cDNA complementary 42 26 sp. [6,19] while in Escherichia coli they are found in about to the loop between a1 and a2 inverted repeats is formed. 43 27 10% of ¢eld strains only [8,20]. In other bacteria, RRTs A typical end product of this process is single-stranded 44 28 have been reported very rarely. In Salmonella, RRT was cDNA (msDNA, multicopy single-stranded DNA) which 45 29 detected in four out of 70 strains of the SARB reference accumulates in bacterial cell cytoplasm [5,12]. The biolog- 46 30 collectionUNCORRECTED[30] and recently RRT (rrtE, retron reverse tran- ical role PROOF of RRT or msDNA is unknown [13]. Speculations 47 31 scriptase Enteritidis) encoded by low molecular mass plas- were presented that it may be mutagenic [26] or may con- 48 32 mid of S. Enteritidis was described [32]. Unlike retroviral trol gene expression by an antisense mechanism [27]. 49 33 reverse transcriptase, bacterial reverse transcriptases utilise RRTs are also suggested to be involved in generation of 50 34 the same RNA molecule as a template and also as a prim- promoterless cDNA of genes which can be inserted into 51 35 er for initiation of the reverse transcription. This occurs by the integron structures [29]. 52 36 a mechanism during which the template RNA molecule is Interestingly, when an integron-encoded multidrug resis- 53 37 folded into a complex secondary structure in which two tance genomic island was sequenced in Salmonella enterica 54 serovar Typhimurium (S. Typhimurium), immediately 55 downstream from it, the rrtT gene was detected on a ge- 56 1 2 * Corresponding author. Tel.: +420 (5) 41321241; netic locus resembling a phage structure [2,3]. Using stan- 57 3 Fax: +420 (5) 41211229. dard BLAST analysis with the rrtT gene sequence encoded 58 4 E-mail address: [email protected] (I. Rychlik). by the multidrug-resistant S. Typhimurium we found this 59 1 0378-1097 / 03 / $22.00 ß 2003 Published by Elsevier Science B.V. on behalf of the Federation of European Microbiological Societies. 2 doi:10.1016/S0378-1097(03)00398-7 FEMSLE 11035 3-6-03 ARTICLE IN PRESS 2 J. Matiasovicova et al. / FEMS Microbiology Letters 11035 (2003) 1^6 60 gene also in the genome of the non-resistant completely ware was used also for primer design. The ¢rst primer pair 88 61 sequenced S. Typhimurium LT2 [28]. This suggested that (RTFor: 5P-GAA CTA TTG CTC ATC CTT CG-3P/ 89 62 the rrtT may not be a rare gene in Salmonella. We have RTRev: 5P-GTA ACG TGA CGG TTA TGT CC-3P) al- 90 63 therefore collected ¢eld strains of S. Typhimurium and lowed the detection of rrtT gene in di¡erent Salmonella 91 64 other serovars and detected the presence of rrtT by poly- serovars. The second primer pair (msDNAFor: 5P-GGA 92 65 merase chain reaction (PCR). In selected strains, produc- AGG AAG GTT ATC ATT GG-3P/msDNARev: 5P-GTC 93 66 tion of msDNA was tested. Obtained results together with TAT CCC TAA AAC TGG GG-3P) allowed for the am- 94 67 detailed sequence analysis allowed us to classify the rrtT, pli¢cation of the predicted msDNA locus and was used for 95 68 together with retrons of Vibrio cholerae, Vibrio parahae- generation of the probe used in DNA hybridisation. Sec- 96 69 molyticus, and E. coli Ec78 and Ec83, among a speci¢c ondary structure of the predicted msDNA was calculated 97 70 subclass of retron reverse transcriptases. using an algorithm available at http://www.bioinfo.rpi.e- 98 du/applications/mfold/. 99 The translated sequence of the rrtT gene from S. Typh- 100 71 2. Materials and methods imurium was searched against SWISS-PROT+TrEMBL 101 databases using BLAST P v2.0 algorithm [1] and BLO- 102 72 2.1. Bacterial strains and growth conditions SUM62 matrix. E-value threshold 0.001 was used for the 103 search. Protein sequences were aligned using Clustal X 104 73 Altogether 236 strains of S. enterica belonging to 12 v1.8 [14]. Duplicated, incomplete and non-conserved se- 105 74 serovars were included in this study. These strains be- quences were removed from the alignment (Table 1) and 106 75 longed to serovar Typhimurium (n = 175 strains), Enter- phylogenetic tree was constructed by the neighbour-join- 107 76 itidis (n = 18), Hadar (n = 13), Saintpaul (n = 10), Agona ing method [33]. Secondary elements of S. Typhimurium 108 77 (n = 5), Heidelberg (n = 6), Derby (n = 2), Stanley (n = 2), RrtT were predicted using PSI-PRED v2.4 [15]. 109 78 Schwarzengrund (n = 2), and individual strains of serovars 79 Indiana, Dublin and Gallinarum. Strains of S. Typhimuri- 2.3. Detection and initial characterisation of multicopy 110 80 um JD42 (rrtTþ, msDNAþ) and JD29 (rrtT3, msDNA3), single-stranded DNA 111 81 and serovar Enteritidis SE2159 (rrtEþ, sdsDNAþ) [32] 82 were used as controls in PCR. All the strains were grown The msDNA was isolated as described previously [19]. 112 83 in Luria Bertani (LB) broth or LB agar (Difco) at 37‡C. After electrophoresis in 13% polyacrylamide gel, the DNA 113 was visualised by staining with Sybr Gold £uorescent dye 114 84 2.2. Computer analysis and primer design (Molecular Probes, USA). To characterise the msDNA in 115 detail, it was treated with 10 U of DNase Iml 31 for 30 116 85 GeneCompar software (Applied Maths, Belgium) was min at 37‡C, 20 U of S1 nuclease for 30 min at 23‡C, 10 117 86 used for basic sequence analysis including cluster analysis Wg of RNase A ml31 for 30 min at 37‡C, 10 U of RNase 118 87 of nucleotide sequences of msDNA locus. The same soft- H for 30 min at 23‡C, and restriction endonuclease Sau3A 119 Table 1 Sequences of the retron reverse transcriptases retrieved from SWISS-PROT+TrEMBL and analysed in this study 1 SWISS-PROT Code Protein name Organism Ref. 2 Q9FDH6 RT_ST reverse transcriptase, RrtT S. Typhimurium [2] 3 Q9S1F2 RET_VC reverse transcriptase V. cholerae [34] 4 NAa RET_VP reverse transcriptase V. parahaemolyticus NPb 5 Q47526 RET_EC reverse transcriptase, retron Ec83 E. coli [23] 6 Q46666 RET_EC2 reverse transcriptase, retron Ec78 E. coli [25] 7 P23070 RT86_EC RNA-directed DNA polymerase, retron EC86 E. coli [24] 8 Q99S60UNCORRECTED SAV2209_SA hypothetical protein SAV2209 PROOFStaphylococcus aureus [17] 9 Q8TP23 MA2102_MA hypothetical protein MA2102 Methanosarcina acetivorans [7] 10 P23071 RT65_MX RNA-directed DNA polymerase, retron MX65 Myxococcus xanthus [10] 11 P23072 RT16_MX RNA-directed DNA polymerase, retron MX162 M. xanthus [11] 12 Q53751 RT163_SA reverse transcriptase Stigmatella aurantiaca [9] 13 Q50210 RT_ML reverse transcriptase Melittangium lichenicola [31] 14 Q8RGW6 FN0161_FN RNA-directed DNA polymerase Fusobacterium nucleatum [16] 15 Q05804 RT107_EC RNA-directed DNA polymerase, retron EC107 E. coli [21] 16 Q8P4T0 XCC3626_XC RNA-directed DNA polymerase Xanthomonas campestris [4] 17 P21325 RT67_EC RNA-directed DNA polymerase, retron EC67 E. coli [21] 18 Q8VRM1 RET_NE reverse transcriptase RT-Ne144 Nannocystis exedens NP 19 Q9L7Z6 RRT_SE retron reverse transcriptase, RrtE S. Enteritidis [32] 20 aSWISS-PROT code not available (BAC06578). 21 bNP, not published. FEMSLE 11035 3-6-03 ARTICLE IN PRESS J. Matiasovicova et al. / FEMS Microbiology Letters 11035 (2003) 1^6 3 120 for 30 min at 37‡C.
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