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αr9 RNA

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αr9 is a family of bacterial small non-coding RNAs with representatives in a broad group of α-proteobacteria from the order Hyphomicrobiales. The first member of this family (Smr9C) was found in a Sinorhizobium meliloti 1021 locus located in the chromosome (C). Further homology and structure conservation analysis have identified full-length Smr9C homologs in several nitrogen-fixing symbiotic rhizobia (i.e. R. leguminosarum bv.viciae, R. leguminosarum bv. trifolii, R. etli, and several Mesorhizobium species), in the plant pathogens belonging to Agrobacterium species (i.e. A. tumefaciens, A. vitis, A. radiobacter, and Agrobacterium H13) as well as in a broad spectrum of Brucella species (B. ovis, B. canis, B. abortus and B. microtis, and several biovars of B. melitensis). αr9C RNA species are 144-158 nt long (Table 1) and share a well defined common secondary structure consisting of seven conserved regions (Figure 1). Most of the αr9 transcripts can be catalogued as trans-acting sRNAs expressed from well-defined promoter regions of independent transcription units within intergenic regions (IGRs) of the α-proteobacterial genomes (Figure 5).

Discovery and structure

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Smr9C sRNA was described by del Val et al.[1] in the intergenic regions (IGRs) of the reference S. meliloti 1021 strain (http://iant.toulouse.inra.fr/bacteria/annotation/cgi/rhime.cgi). Northern hybridization experiments confirmed that the predicted smr9C locus did express a single transcript of the expected size, which accumulated differentially in free-living and endosymbiotic bacteria. TAP-based 5'-RACE experiments mapped the transcription start site (TSS) of the full-length Smr9C transcript to the 1,398,425 nt position in the S. meliloti 1021 genome (http://iant.toulouse.inra.fr/bacteria/annotation/cgi/rhime.cgi) whereas the 3'-end was assumed to be located at the 1,398,277 nt position matching the last residue of the consecutive stretch of Us of a bona fide Rho-independent terminator (Figure 5). Parallel and later studies[2][3] in which Smr9C transcript is referred to as Igr#3 or sra32 independently confirmed the expression this sRNA in S. meliloti and in its closely related strain 2011. Recent deep sequencing-based characterization of the small RNA fraction (50-350 nt) of S. meliloti 2011 further confirmed the expression of Smr9C (here referred to as SmelC289), and mapped the 5'- and 3´-ends of the full-length transcript to positions 1,398,423 and 1,398,279, respectively, in the S. meliloti 1021 genome.[4]

The nucleotide sequence of Smr9C was initially used as query to search against the Rfam database (version 10.0; http://www.sanger.ac.uk/Software/Rfam). This homology search rendered no matches to known bacterial sRNA in this database. Smr9C was next BLASTed with default parameters against all the currently available bacterial genomes (1,615 sequences at 20 April 2011; https://www.ncbi.nlm.nih.gov). The regions exhibiting significant homology to the query sequence (78-89% similarity) were extracted to create a Covariance Model (CM) from a seed alignment using Infernal (version1.0)[5] (Figure 2). This CM was used in a further search for new members of the αr9 family in the existing bacterial genomic databases.

Figure 1: Covariance Model in stockholm format showing the consensus structure for the αr9 family. Each of the stems represented by the structure line#=GC SS_cons is in a different color. To download the covariance model click here.

The results were manually inspected to deduce a consensus secondary structure for the family (Figure 1 and Figure 2). The consensus structure was also independently predicted with the program locARNATE[6] with very similar predictions. The manual inspection of the sequences found with the CM using Infernal allowed finding 26 true homolog sequences, all of them present as single chromosomal copies in the α-proteobacterial genomes. The rhizobial species encoding the 12 closer homologs to Smr9C were: two R. leguminosarum trifolii strains (WSM2304 and WSM1235), two R. etli strains CFN 42 and CIAT 652, the reference R. leguminosarum bv. viciae 3841 strain, Rhizobium NGR234, and the Agrobacterium species A. vitis,A. tumefaciens, A. radiobacter and A. H13. All these sequences showed significant Infernal E-values (1.50e-39 – 14.02e-21) and bit-scores. The rest of the sequences found with the model showed high E-values between (3.40e-12 and 2.62e-04) but lower bit-scores and are encoded by Brucella species (B. ovis, B. canis, B. abortus, B. microtis, and several biobars of B. melitensis), Brucella anthropi and the Mesorhizobum species M. loti, M. ciceri and M. BNC.

Table 1: Smr9C homologs in other symbionts and pathogens
CM model Name GI accession number begin end strand %GC length Organism
αr9 Smr9C gi|15963753|ref|NC_003047.1| 1398277 1398425 - 46 149 Sinorhizobium meliloti 1021
αr9 Smedr9C gi|150395228|ref|NC_009636.1| 979747 979902 - 48 150 Sinorhizobium medicae WSM419 chromosome
αr9 Sfr9C gi|227820587|ref|NC_012587.1| 1130001 1130150 - 47 150 Sinorhizobium fredii NGR234 chromosome
αr9 Atr9C gi|159184118|ref|NC_003062.2| 1275297 1275443 - 47 147 Agrobacterium tumefaciens str. C58 chromosome circular
αr9 AH13r9C gi|325291453|ref|NC_015183.1| 1215580 1215726 - 48 147 Agrobacterium sp. H13-3 chromosome
αr9 ReCIATr9C gi|190889639|ref|NC_010994.1| 1684929 1685072 - 48 144 Rhizobium etli CIAT 652
αr9 Arr9CI gi|222084201|ref|NC_011985.1| 1481975 1482119 - 49 145 Agrobacterium radiobacter K84 chromosome 1
αr9 Rlt2304r9C gi|209547612|ref|NC_011369.1| 1296506 1296650 - 48 145 Rhizobium leguminosarum bv. trifolii WSM2304 chromosome
αr9 Avr9CI gi|222147015|ref|NC_011989.1| 1448510 1448659 - 45 150 Agrobacterium vitis S4 chromosome 1
αr9 Rlvr9C gi|116249766|ref|NC_008380.1| 1802936 1803079 - 49 144 Rhizobium leguminosarum bv. viciae 3841
αr9 Rlt1325r9C gi|241202755|ref|NC_012850.1| 1354593 1354736 - 47 144 Rhizobium leguminosarum bv. trifolii WSM1325
αr9 ReCFNr9C gi|86355669|ref|NC_007761.1| 1703203 1703345 - 47 143 Rhizobium etli CFN 42
αr9 Mlr9C gi|57165207|ref|NC_002678.2| 1127217 1127363 + 54 145 Mesorhizobium loti MAFF303099 chromosome
αr9 Mcr9C gi|319779749|ref|NC_014923.1| 3449639 3449786 - 52 148 Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome
αr9 Bcr9CI gi|161617991|ref|NC_010103.1| 796281 796428 - 49 148 Brucella canis ATCC 23365 chromosome I
αr9 Bs23445r9CI gi|163842277|ref|NC_010169.1| 817762 817909 - 49 148 Brucella suis ATCC 23445 chromosome I
αr9 Bm16Mr9CI gi|17986284|ref|NC_003317.1| 1187596 1187743 + 49 146 Brucella melitensis bv. 1 str. 16M chromosome I
αr9 BaS19r9CI gi|189023268|ref|NC_010742.1| 817898 818045 - 49 148 Brucella abortus S19 chromosome 1
αr9 Bm23457r9CI gi|225851546|ref|NC_012441.1| 819377 819523 - 50 147 Brucella melitensis ATCC 23457 chromosome I
αr9 Bs1330r9CI gi|56968325|ref|NC_004310.3| 797917 798064 - 49 148 Brucella suis 1330 chromosome I
αr9 Ba19941r9CI gi|62288991|ref|NC_006932.1| 819597 819744 - 49 148 Brucella abortus bv. 1 str. 9-941 chromosome I
αr9 Bmar9CI gi|82698932|ref|NC_007618.1| 815875 816022 - 49 148 Brucella melitensis biovar Abortus 2308 chromosome I
αr9 Bor9CI gi|148558820|ref|NC_009505.1| 822712 822859 - 49 148 Brucella ovis ATCC 25840 chromosome I
αr9 Bmir9CI gi|256368465|ref|NC_013119.1| 802078 802225 - 49 148 Brucella microti CCM 4915 chromosome 1
αr9 Oar9CI gi|153007346|ref|NC_009667.1| 2529108 2529255 + 48 146 Brucella anthropi ATCC 49188 chromosome 1
αr9 MsBCNr9C gi|110632362|ref|NC_008254.1| 1141776 1141933 - 50 158 Mesorhizobium sp. BNC1
Figure 2: Consensus secondary structure of the αr9 members predicted by RNA[7] and RNAalifold.[8] Smr9C is coloured according to base pair probabilities, the color probability scale is indicated in the drawing. The αr9 family structure is coloured following a base conservation scheme. Red: base pair occurring in all sequences used to generate the consensus; yellow: two types of base pairing occur; Green: three types of base pairing occur. The shading of base pairs represents: Saturated, no inconsistent sequences; Pale, one inconsistent sequence; Very pale, two inconsistent sequences.
Figure 3: Phylogenetic distribution of known and predicted αr9 genes. Gene numbers are based on computational analysis using the program Infernal. Legend: Smr9C = Sinorhizobium meliloti 1021 (NC_003047), Smedr9C = Sinorhizobium medicae WSM419 chromosome (NC_009636), Sfr9C = Sinorhizobium fredii NGR234 chromosome (NC_012587), Atr9C = Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062), AH13r9C = Agrobacterium sp. H13-3 chromosome (NC_015183), ReCIATr9C = Rhizobium etli CIAT 652 (NC_010994), Arr9CI = Agrobacterium radiobacter K84 chromosome 1 (NC_011985), Rlt2304r9C = Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369), Avr9CI = Agrobacterium vitis S4 chromosome 1 (NC_011989), Rlvr9C = Rhizobium leguminosarum bv. viciae 3841 (NC_008380), Rlt1325r9C = Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850), ReCFNr9C = Rhizobium etli CFN 42 (NC_007761), Mlr9C = Mesorhizobium loti MAFF303099 chromosome (NC_002678), Mcr9C = Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923), Bcr9CI = Brucella canis ATCC 23365 chromosome I (NC_010103), Bs23445r9CI = Brucella suis ATCC 23445 chromosome I (NC_010169), Bm16Mr9CI = Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317), BaS19r9CI = Brucella abortus S19 chromosome 1 (NC_010742), Bm23457r9CI = Brucella melitensis ATCC 23457 chromosome I (NC_012441), Bs1330r9CI = Brucella suis 1330 chromosome I (NC_004310), Ba19941r9CI = Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932), Bmar9CI = Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618), Bor9CI = Brucella ovis ATCC 25840 chromosome I (NC_009505), Bmir9CI = Brucella microti CCM 4915 chromosome 1 (NC_013119), Oar9CI = Brucella anthropi ATCC 49188 chromosome 1 (NC_009667), MsBCNr9C = Mesorhizobium sp. BNC1 (NC_008254).

Expression information

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Parallel studies assessed Smr9C expression in S. meliloti 1021 under different biological conditions; i.e. bacterial growth in TY, minimal medium (MM) and luteolin-MM broth and endosymbiotic bacteria (i.e. mature symbiotic alfalfa nodules)[1] and high salt stress, oxidative stress and cold and hot shock stresses.[3] Expression of Smr9C in free-living bacteria was found to be growth-dependent, being the gene strongly down-regulated when bacteria entered the stationary phase, whereas no expression was detected in endosymbiotic bacteria. Recent deep sequencing data[4] further revealed up-regulation of Smr9C upon salt, acidic, cold-shock and heat shock stresses. Recent co-inmuno precipitation experiments[9] corroborate that Smr9C, does bind the bacterial protein Hfq for efficient target binding.

Promoter analysis

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All the promoter regions of the αr9 family members examined so far are very conserved in a sequence stretch extending up to 80 bp upstream of the transcription start site of the sRNA. All loci have recognizable σ70-dependent promoters showing a -35/-10 consensus motif CTTAGAC-n17-CTATAT, which has been previously shown to be widely conserved among several other genera in the α-subgroup of proteobacteria.[10] To identify binding sites for other known transcription factors we used the fasta sequences provided by RegPredict[11](http://regpredict.lbl.gov/regpredict/help.html), and used those position weight matrices (PSWM) provided by RegulonDB[12] (http://regulondb.ccg.unam.mx). We built PSWM for each transcription factor from the RegPredict sequences using the Consensus/Patser program, choosing the best final matrix for motif lengths between 14 and 30 bps a threshold average E-value < 10E-10 for each matrix was established, (see "Thresholded consensus" in http://gps-tools2.its.yale.edu). Moreover, we searched for conserved unknown motifs using MEME[13] (http://meme.sdsc.edu/meme4_6_1/intro.html) and used relaxed regular expressions (i.e. pattern matching) over all Smr9C homologs promoters. This studies revealed the presence of 30 bp long region very conserved between positions -40 and -75, conserved MEME motif, (Figure 5). This sequence was present in all but one of the smrC9 homologs found, but no significant similarity to known transcription factor binding sites matrices could be established.[14]

Figure 4: Alignment of the promoter region of the αr9 members. All members presented putative σ70 promoters with -35 and -10 boxes marked in green and red respectively. The motif found conserved in all αr9 family members is marked with an orange box.

Genomic context

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Most of the members of the αr9 family are trans-encoded sRNAs transcribed from independent promoters in chromosomal IGRs. Exceptions are the cis-encoded antisense Smr9C homologs of A. tumefaciens and B. microti, which are located in the opposite strand of annotated genes, partially overlapping ORFs. Most of the neighboring genes of the seed alignment's members were not annotated and thus were further manually curated.[15][16][17] The predicted protein products of these overlapping ORFs could not be assigned to any functional category on the basis of the amino acid sequence homology. However, the genomic regions of almost all αr9 sRNAs exhibited a great degree of conservation including the sRNA-coding sequence and the upstream and downstream genes which have been predicted to code for a prolyl-tRNA syntethase (proS) and a transmembrane protein, respectively. Partial synteny of the αr9 genomic regions was observed in a few cases such as, S. medicae where instead of a proS gene an FAD-dependent pyridine nucleotide-disulfide oxidoreductase encoding gene was found upstream of the αr9 locus, and Mesorhizobium loti where no transmembrane coding gene was recognizable downstream of the sRNA gene. A special case is the Brucella group, where primary automatic annotation over their genomes identified ORFs smaller than 30 aa overlapping with the predicted αr9 sRNA in the same strand. These predicted ORFs, neither show any similarity with database entries nor any motif or signatures when searched against family and motif databases such as Interpro,[18] PFAM[19] or Smart,[20] and thus, are considered here as missannotations not registered in the genomic context graph.

Figure 5: Genomic context scheme of Smr9C and its closest homologues in α-proteobacteria. The αr9 RNA genes are represented by red arrows and the flanking ORFs by arrows on different colors depending on their product function (legend). Numbers indicate the αr9 RNA gene's and flanking ORFs coordinates in each organism genome database. The gene strand is represented with the file direction. On the left of the figure identification names are used which correspond to a certain organism: αr9_Smr9C = Sinorhizobium meliloti 1021 (NC_003047), αr9_Smedr9C = Sinorhizobium medicae WSM419 chromosome (NC_009636), αr9_Sfr9C = Sinorhizobium fredii NGR234 chromosome (NC_012587), αr9_Atr9C = Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062), αr9_AH13r9C = Agrobacterium sp. H13-3 chromosome (NC_015183), αr9_ReCIATr9C = Rhizobium etli CIAT 652 (NC_010994), αr9_Arr9CI = Agrobacterium radiobacter K84 chromosome 1 (NC_011985), αr9_Rlt2304r9C = Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369), αr9_Avr9CI = Agrobacterium vitis S4 chromosome 1 (NC_011989), αr9_Rlvr9C = Rhizobium leguminosarum bv. viciae 3841 (NC_008380), αr9_Rlt1325r9C = Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850), αr9_ReCFNr9C = Rhizobium etli CFN 42 (NC_007761), αr9_Mlr9C = Mesorhizobium loti MAFF303099 chromosome (NC_002678), αr9_Mcr9C = Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923), αr9_Bcr9CI = Brucella canis ATCC 23365 chromosome I (NC_010103), αr9_Bs23445r9CI = Brucella suis ATCC 23445 chromosome I (NC_010169), αr9_Bm16Mr9CI = Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317), αr9_BaS19r9CI = Brucella abortus S19 chromosome 1 (NC_010742), αr9_Bm23457r9CI = Brucella melitensis ATCC 23457 chromosome I (NC_012441), αr9_Bs1330r9CI = Brucella suis 1330 chromosome I (NC_004310), αr9_Ba19941r9CI = Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932), αr9_Bmar9CI = Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618), αr9_Bor9CI = Brucella ovis ATCC 25840 chromosome I (NC_009505), αr9_Bmir9CI = Brucella microti CCM 4915 chromosome 1 (NC_013119), αr9_Oar9CI = Brucella anthropi ATCC 49188 chromosome 1 (NC_009667), αr9_MsBCNr9C = Mesorhizobium sp. BNC1 (NC_008254).
Table 2: Detailed Genomic context information of the αr9 sRNA members.
Family Feature Name Strand Begin End Protein name Annotation Organism
αr9_Smr9C gene SMc01933 R 1397889 1398104 NP_385391.1 transmembrane protein Sinorhizobium meliloti 1021 (NC_003047)
αr9_Smr9C sRNA Smr9C R 1398277 1398425 Sinorhizobium meliloti 1021 (NC_003047)
αr9_Smr9C gene SMc01934 D 1398815 1400143 NP_385392.1 prolyl-tRNA sybthetase Sinorhizobium meliloti 1021 (NC_003047)
αr9_Rlt2304r9C gene Rleg2_1278 D 1296067 1296342 YP_002280798.1 transmembrane protein function DUF146 Rhizobium leguminosarum bv trifolii WSM2304 chromosome (NC_011369)
αr9_Rlt2304r9C sRNA Rlt2304r9C R 1296506 1296650 Rhizobium leguminosarum bv trifolii WSM2304 chromosome (NC_011369)
αr9_Rlt2304r9C gene Rleg2_1279 D 1296935 1298257 YP_002280799.1 prolyl-tRNA sybthetase Rhizobium leguminosarum bv trifolii WSM2304 chromosome (NC_011369)
αr9_Rlt1325r9C gene Rleg_1370 D 1354155 1354430 YP_002975201.1 transmembrane protein Rhizobium leguminosarum bv trifolii WSM1325 (NC_012850)
αr9_Rlt1325r9C sRNA Rlt1325r9C R 1354593 1354736 Rhizobium leguminosarum bv trifolii WSM1325 (NC_012850)
αr9_Rlt1325r9C gene Rleg_1371 D 1355021 1356343 YP_002975202.1 prolyl-tRNA sybthetase Rhizobium leguminosarum bv trifolii WSM1325 (NC_012850)
αr9_ReCFNr9C gene RHE_CH01622 D 1702700 1703041 YP_469148.1 transmembrane protein Rhizobium etli CFN 42 (NC_007761)
αr9_ReCFNr9C sRNA ReCFNr9C R 1703203 1703345 Rhizobium etli CFN 42 (NC_007761)
αr9_ReCFNr9C gene RHE_CH01623 D 1703629 1704951 YP_469149.2 prolyl-tRNA sybthetase Rhizobium etli CFN 42 (NC_007761)
αr9_Smedr9C gene Smed_0907 D 979229 979498 YP_001326597.1 transmembrane protein Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr9_Smedr9C sRNA Smedr9C R 979747 979753 Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr9_Smedr9C gene Smed_0908 D 980177 981469 YP_001326598.1 FAD-dependent pyridine nucleotide-disulfide oxidoreductas Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr9_Rlvr9C gene RL1718 D 1802432 1802773 YP_767322.1 transmembrane protein Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr9_Rlvr9C sRNA Rlvr9C R 1802936 1803079 Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr9_Rlvr9C gene RL1719 D 1803364 1804686 YP_767323.1 prolyl-tRNA sybthetase Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr9_Atr9C gene Atu1286 D 1274803 1275072 NP_354296.2 transmembrane protein Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062)
αr9_Atr9C sRNA Atr9C R 1275297 1275443 Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062)
αr9_Atr9C gene Atu1288 D 1275738 1277060 NP_354297.2 prolyl-tRNA sybthetase Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062)
αr9_ReCIATr9C gene RHECIAT_CH0001694 D 1684473 1684766 YP_001977846.1 transmembrane protein Rhizobium etli CIAT 652 (NC_010994)
αr9_ReCIATr9C sRNA ReCIATr9C R 1684929 1685072 Rhizobium etli CIAT 652 (NC_010994)
αr9_ReCIATr9C gene RHECIAT_CH0001695 D 1685356 1686678 YP_001977847.1 prolyl-tRNA sybthetase Rhizobium etli CIAT 652 (NC_010994)
αr9_Arr9CI gene Arad_1869 D 1481492 1481770 YP_002544124.1 transmembrane protein Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr9_Arr9CI sRNA Arr9CI R 1481975 1482119 Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr9_Arr9CI gene Arad_1870 D 1482307 1483734 YP_002544125.1 prolyl-tRNA sybthetase Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr9_Sfr9C gene NGR_c10670 D 1129571 1129840 YP_002825606.1 transmembrane protein Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr9_Sfr9C sRNA Sfr9C R 1130001 1130150 Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr9_Sfr9C gene NGR_c10680 D 1130367 1131872 YP_002825607.1 prolyl-tRNA sybthetase Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr9_AH13r9C gene AGROH133_05703 D 1215032 1215337 YP_004278514.1 transmembrane protein Agrobacterium sp. H13-3 chromosome (NC_015183)
αr9_AH13r9C sRNA AH13r9C R 1215580 1215726 Agrobacterium sp. H13-3 chromosome (NC_015183)
αr9_AH13r9C gene AGROH133_05706 D 1215911 1217344 YP_004278515.1 Prolyl-tRNA sybthetase Agrobacterium sp. H13-3 chromosome (NC_015183)
αr9_Avr9CI gene Avi_1737 D 1448181 1448450 YP_002549251.1 transmembrane protein Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr9_Avr9CI sRNA Avr9CI R 1448510 1448659 Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr9_Avr9CI gene Avi_1739 D 1448895 1450391 YP_002549252.1 prolyl-tRNA sybthetase Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr9_Bor9CI gene BOV_0814 D 822060 822329 YP_001258797.1 transmembrane protein Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr9_Bor9CI sRNA Bor9CI R 822712 822859 Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr9_Bor9CI gene BOV_0816 D 823177 824505 YP_001258799.1 prolyl-tRNA sybthetase Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr9_Bcr9CI gene BCAN_A0834 D 795629 795898 YP_001592670.1 transmembrane protein Brucella canis ATCC 23365 chromosome I (NC_010103)
αr9_Bcr9CI sRNA Bcr9CI R 796281 796428 Brucella canis ATCC 23365 chromosome I (NC_010103)
αr9_Bcr9CI gene BCAN_A0837 D 796746 798074 YP_001592673.1 prolyl-tRNA sybthetase Brucella canis ATCC 23365 chromosome I (NC_010103)
αr9_Bs23445r9CI gene BSUIS_A0858 D 817110 817379 YP_001627496.1 transmembrane protein Brucella suis ATCC 23445 chromosome I (NC_010169)
αr9_Bs23445r9CI sRNA Bs23445r9CI R 817762 817909 Brucella suis ATCC 23445 chromosome I (NC_010169)
αr9_Bs23445r9CI gene BSUIS_A0861 D 818227 819555 YP_001627499.1 prolyl-tRNA sybthetase Brucella suis ATCC 23445 chromosome I (NC_010169)
αr9_Bm16Mr9CI gene BMEI1140 R 1185950 1187287 NP_540057.1 prolyl-tRNA sybthetase Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317)
αr9_Bm16Mr9CI sRNA Bm16Mr9CI D 1187596 1187743 Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317)
αr9_Bm16Mr9CI gene BMEI1141 R 1188126 1188395 NP_540058.1 transmembrane protein Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317)
αr9_BaS19r9CI gene BAbS19_I07830 D 817246 817515 YP_001934781.1 transmembrane protein Brucella abortus S19 chromosome 1 (NC_010742)
αr9_BaS19r9CI sRNA BaS19r9CI R 817898 818045 Brucella abortus S19 chromosome 1 (NC_010742)
αr9_BaS19r9CI gene BAbS19_I07840 D 818363 819691 YP_001934782.1 prolyl-tRNA sybthetase Brucella abortus S19 chromosome 1 (NC_010742)
αr9_Bs1330r9CI gene BR0819 D 797265 797534 NP_697833.1 transmembrane protein Brucella suis 1330 chromosome I (NC_004310)
αr9_Bs1330r9CI sRNA Bs1330r9CI R 797917 798064 Brucella suis 1330 chromosome I (NC_004310)
αr9_Bs1330r9CI gene BR0822 D 798382 799710 NP_697836.1 prolyl-tRNA sybthetase Brucella suis 1330 chromosome I (NC_004310)
αr9_Ba19941r9CI gene BruAb1_0833 D 818945 819214 YP_221561.1 transmembrane protein Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr9_Ba19941r9CI sRNA Ba19941r9CI R 819597 819744 Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr9_Ba19941r9CI gene BruAb1_0836 D 820062 821390 YP_221564.1 prolyl-tRNA sybthetase Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr9_Bmar9CI gene BAB1_0839 D 815223 815492 YP_414270.1 hypothetical membrane spanning protein Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr9_Bmar9CI sRNA Bmar9CI R 815875 816022 Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr9_Bmar9CI gene BAB1_0842 D 816340 817668 YP_414273.1 prolyl-tRNA sybthetase Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr9_Bmir9CI gene BMI_I820 D 801426 801695 YP_003106759.1 transmembrane protein Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr9_Bmir9CI sRNA Bmir9CI R 802078 802225 Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr9_Bmir9CI gene BMI_I822 D 802543 803871 YP_003106761.1 prolyl-tRNA sybthetase Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr9_Bm23457r9CI gene BMEA_A0861 D 818725 818994 YP_002732568.1 transmembrane protein Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr9_Bm23457r9CI sRNA Bm23457r9CI R 819377 819523 Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr9_Bm23457r9CI gene BMEA_A0862 D 819842 821170 YP_002732569.1 prolyl-tRNA sybthetase Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr9_Mlr9C gene mll1344 R 1125520 1126848 NP_102953.1 prolyl-tRNA sybthetase Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr9_Mlr9C sRNA Mlr9C D 1127217 1127363 Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr9_Mlr9C gene msl1345 R 1127503 1127787 NP_102954.1 hypothetical membrane spanning protein Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr9_Oar9CI gene Oant_2405 R 2527462 2528790 YP_001370948.1 prolyl-tRNA sybthetase Brucella anthropi ATCC 49188 chromosome 1 (NC_009667)
αr9_Oar9CI sRNA Oar9CI D 2529108 2529255 Brucella anthropi ATCC 49188 chromosome 1 (NC_009667)
αr9_Oar9CI gene Oant_2406 R 2529594 2529863 YP_001370949.1 transmembrane protein Brucella anthropi ATCC 49188 chromosome 1 (NC_009667)
αr9_Mcr9C gene Mesci_3302 D 3449215 3449499 YP_004142475.1 transmembrane protein Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
αr9_Mcr9C sRNA Mcr9C R 3449639 3449786 Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
αr9_Mcr9C gene Mesci_3303 D 3450133 3451461 YP_004142476.1 prolyl-tRNA sybthetase Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
αr9_MsBCNr9C gene Meso_1039 D 1141489 1141758 YP_673601.1 transmembrane protein Mesorhizobium sp. BNC1 (NC_008254)
αr9_MsBCNr9C sRNA MsBCNr9C R 1141776 1141933 Mesorhizobium sp. BNC1 (NC_008254)
αr9_MsBCNr9C gene Meso_1040 D 1142139 1143467 YP_673602.1 prolyl-tRNA sybthetase Mesorhizobium sp. BNC1 (NC_008254)

References

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