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User:Rcrzarg/αr7 RNA

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Introduction to αr7 sRNA

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αr7 is a family of bacterial small non-coding RNAs with representatives in a broad group of α-proteobacterial species from the order Rhizobiales. The first member of this family (Smr7C 150nt) was found in a Sinorhizobium meliloti 1021 locus located in the chromosome (C). Further homology and structure conservation analysis identified full-length 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 biobars of B. melitensis). αr7 RNA species are 134-159 nt long (Table 1) and share a well defined common secondary structure (Figure 1, Figure 2). αr7 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 4).

Discovery and Structure

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Smr7C 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 detected two RNA species expressed from the smr7C locus, which accumulated differentially in free-living and endosymbiotic bacteria. TAP-based 5’-RACE experiments mapped the transcription start site (TSS) to two close G residues. From the six independent sequences obtained, five mapped to residue 201,681 in the chromosome and one to the upstream residue 201,679. Furthermore, an additional 5′-RACE product could be obtained from this transcript in both TAP- and mock-treated RNA samples. The sequence of this second RACE product mapped the processing site of Smr7C to residue 201,723 nt in the S. meliloti 1021 genome (http://iant.toulouse.inra.fr/bacteria/annotation/cgi/rhime.cgi). The 3’-end was assumed to be located at the 201,828 nt position matching the last residue of the consecutive stretch of Us of a bona fide Rho-independent terminator. Parallel and later studies[2][3] in which Smr7C transcript is referred to as sra03 or Sm13, independently confirmed the expression this sRNA in S. melilloti and in its closely related strain 2011. Recent deep sequencing-based characterization of the small RNA fraction (50-350 nt) of S. meliloti 2021 further also confirmed the expression of Smr7C (here referred to as SmelC023), and mapped the 5’- end of the full-length transcript to the same position in the S. meliloti 1021 genome, and the 3' end to position 201,825[4].

The nucleotide sequence of Smr7C 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. Smr7C was next BLASTed with default parameters against all the currently available bacterial genomes (1,615 sequences at 20 April 2011; http://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]. This CM was used in a further search for new members of the αr7 family in the existing bacterial genomic databases (Table 1) and to create the final CM model (Figure 1).

Table 1: αr7 homologs in other symbionts and pathogens
CM model Name GI accession number begin end strand %GC length Organism
αr7 Smr7C gi|15963753|ref|NC_003047.1| 201679 201828 + 64 150 Sinorhizobium meliloti 1021
αr7 Smedr7C gi|150395228|ref|NC_009636.1| 3585152 3585302 + 60 151 Sinorhizobium medicae WSM419 chromosome
αr7 Sfr7C gi|227820587|ref|NC_012587.1| 3727302 3727450 - 66 149 Sinorhizobium fredii NGR234 chromosome
αr7 Atr7C gi|159184118|ref|NC_003062.2| 112535 112678 - 65 144 Agrobacterium tumefaciens str. C58 chromosome circular
αr7 AH13r7C gi|325291453|ref|NC_015183.1| 112523 112667 - 63 145 Agrobacterium sp. H13-3 chromosome
αr7 ReCIATr7C gi|190889639|ref|NC_010994.1| 205678 205811 - 61 134 Rhizobium etli CIAT 652
αr7 Arr7CI gi|222084201|ref|NC_011985.1| 243240 243377 - 62 138 Agrobacterium radiobacter K84 chromosome 1
αr7 Rlt2304r7C gi|209547612|ref|NC_011369.1| 4280520 4280653 - 63 134 Rhizobium leguminosarum bv. trifolii WSM2304 chromosome
αr7 Avr7CI gi|222147015|ref|NC_011989.1| 255869 256019 + 60 151 Agrobacterium vitis S4 chromosome 1
αr7 Rlvr7C gi|116249766|ref|NC_008380.1| 192620 192753 - 62 134 Rhizobium leguminosarum bv. viciae 3841
αr7 Rlt1325r7C gi|241202755|ref|NC_012850.1| 4553564 4553697 - 62 134 Rhizobium leguminosarum bv. trifolii WSM1325
αr7 ReCFNr7C gi|86355669|ref|NC_007761.1| 163762 163895 - 60 134 Rhizobium etli CFN 42
αr7 Mlr7C gi|57165207|ref|NC_002678.2| 2648243 2648390 - 65 148 Mesorhizobium loti MAFF303099 chromosome
αr7 MsBNCr7C gi|110632362|ref|NC_008254.1| 4251581 4251722 + 60 142 Mesorhizobium sp. BNC1
αr7 Mcr7C gi|319779749|ref|NC_014923.1| 1781903 1782047 + 68 145 Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome
αr7 Bcr7CI gi|161617991|ref|NC_010103.1| 134573 134715 - 62 143 Brucella canis ATCC 23365 chromosome I
αr7 Bs23445r7CI gi|163842277|ref|NC_010169.1| 134908 135050 - 62 143 Brucella suis ATCC 23445 chromosome I
αr7 Bm16Mr7CI gi|17986284|ref|NC_003317.1| 1868345 1868487 + 62 143 Brucella melitensis bv. 1 str. 16M chromosome I
αr7 BaS19r7CI gi|189023268|ref|NC_010742.1| 134335 134477 - 62 143 Brucella abortus S19 chromosome 1
αr7 Bm23457r7CI gi|225851546|ref|NC_012441.1| 134555 134697 - 62 143 Brucella melitensis ATCC 23457 chromosome I
αr7 Bs1330r7CI gi|56968325|ref|NC_004310.3| 134590 134732 - 62 143 Brucella suis 1330 chromosome I
αr7 Ba19941r7CI gi|62288991|ref|NC_006932.1| 135949 136091 - 62 143 Brucella abortus bv. 1 str. 9-941 chromosome I
αr7 Bmar7CI gi|82698932|ref|NC_007618.1| 132316 132458 - 62 143 Brucella melitensis biovar Abortus 2308 chromosome I
αr7 Bor7CI gi|148558820|ref|NC_009505.1| 134888 135029 - 63 142 Brucella ovis ATCC 25840 chromosome I
αr7 Bmir7CI gi|256368465|ref|NC_013119.1| 136167 136309 - 62 143 Brucella microti CCM 4915 chromosome 1
αr7 Oar7CI gi|153007346|ref|NC_009667.1| 149814 149972 - 58 159 Ochrobactrum anthropi ATCC 49188 chromosome 1


Figure 1: Covariance Model in stockholm format showing the consensus structure for the αr7 family. Each of the stems represented by the structure line #=GC SS_cons is in a different color, corresponding the red one to the rho independent terminator stem. Covariance Model in stockholm format can be downloaded 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 closer homologs to Smr7C were: S. medicae and S. fredii, two R. leguminosarum trifolii strains (WSM2304 and WSM1325), two R. etli strains CFN 42 and CIAT 652, the reference R. leguminosarum bv. viciae 3841 strain, and the Agrobacterium species A. vitis, A. tumefaciens, A. radiobacter and A. H13 and the Mesorhizobum species loti, M. ciceri and M. BNC. All these sequences showed significant Infernal E-values (3.66E-49 - 2.93E-12) and bit-scores. The rest of the sequences found with the model showed high E-values between (1.58E-10 and 2.88E-09) but lower bit-scores and are encoded by Brucella species (B. ovis, B. canis, B. abortus, B. microtis, and several biobars of B. melitensis), and Ochrobactrum anthropi.


Figure 1: Consensus secondary structure of Smr7C and the ar7 family predicted by RNA[7] and RNAalifold[8]. The color scheme of Smr7C represents the base pairs probabilities. The coloring scheme for the ar7 family structure is based on the base pairs conservation: 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 αr7 genes. Gene numbers are based on computational analysis using the program Infernal. Legend: Smedr7C = Sinorhizobium medicae WSM419 chromosome (NC_009636), Smr7C = Sinorhizobium meliloti 1021 (NC_003047), Sfr7C = Sinorhizobium fredii NGR234 chromosome (NC_012587), Atr7C = Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062), AH13r7C = Agrobacterium sp. H13-3 chromosome (NC_015183), ReCIATr7C = Rhizobium etli CIAT 652 (NC_010994), Arr7CI = Agrobacterium radiobacter K84 chromosome 1 (NC_011985), Rlt2304r7C = Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369), Avr7CI = Agrobacterium vitis S4 chromosome 1 (NC_011989), Rlvr7C = Rhizobium leguminosarum bv. viciae 3841 (NC_008380), Rlt1325r7C = Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850), ReCFNr7C = Rhizobium etli CFN 42 (NC_007761), Mlr7C = Mesorhizobium loti MAFF303099 chromosome (NC_002678), Mcr7C = Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923), Bcr7CI = Brucella canis ATCC 23365 chromosome I (NC_010103), Bs23445r7CI = Brucella suis ATCC 23445 chromosome I (NC_010169), Bm16Mr7CI = Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317), BaS19r7CI = Brucella abortus S19 chromosome 1 (NC_010742), Bm23457r7CI = Brucella melitensis ATCC 23457 chromosome I (NC_012441), Bs1330r7CI = Brucella suis 1330 chromosome I (NC_004310), Ba19941r7CI = Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932), Bmar7CI = Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618), Bor7CI = Brucella ovis ATCC 25840 chromosome I (NC_009505), Bmir7CI = Brucella microti CCM 4915 chromosome 1 (NC_013119), Oar7CI = Ochrobactrum anthropi ATCC 49188 chromosome 1 (NC_009667), MsBNCr7C = Mesorhizobium sp. BNC1 (NC_008254).

Expression information

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Parallel studies assessed Smr7C 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]. Expression of Smr7C in free-living bacteria was found to be growth-dependent, being the gene strongly down-regulated when bacteria entered the stationary phase. Interestingly, expression of SmrC7 increased ~13-fold in nodules when compared with free-living bacteria (log phase TY or MM cultures), suggesting the induction of this sRNAs during bacterial infection and/or bacteroid differentiation[1]. SmrC7 expression has also been proved in parallel studies[3][2][4].

Promoter Analysis

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All the promoter regions of the αr7 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 closest homologous 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[9]. To identify binding sites for other known transcription factors we used the fasta sequences provided by RegPredict[10] (http://regpredict.lbl.gov/regpredict/help.html), and used those position weight matrices (PSWM) provided by RegulonDB[11] (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 14–30 bps a threshold average E-value < 10E-10 for each matrix was establish, (see "Thresholded consensus" in http://gps-tools2.its.yale.edu). Moreover, we searched for conserved unknown motifs using MEME[12] (http://meme.sdsc.edu/meme4_6_1/intro.html) and used relaxed regular expressions (i.e. pattern matching) over all promoters of the Smr7C homologs promoters.

This studies revealed a 20 bp conserved motif in ll promoter regions, marked in orange as MEME conserved motif, in (Figure 4), but no significant similarity to known transcription factor biding sites matrices could be establish.

Figure 4: Alignment of the promoter region of the αr7 members. All analyzed members presented putative σ70 promoters with -35 and -10 boxes marked in green and red respectively.

Genomic Context

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All identified members of the αr7 family are trans-encoded sRNAs transcribed from independent promoters in chromosomal IGRs. Most of the neighboring genes of the seed alignment’s members were not annotated and thus were further manually curated[13][14][15].

The αr7 sRNAs' genomic regions of the Sinorhizobium, Rhizobium and Agrobacterium group members exhibited a great degree of conservation with the upstream and downstream genes coding for a DNA polymerase, and a MarR family transcriptional regulator, respectively. Partial synteny of the αr7 genomic regions was observed in the Mesorhizobium and Brucella group, where instead of the MarR family transcriptional regulator gene, a peptidase encoding gene was found.

Figure 5: Genomic context scheme of Smr7C and its closest homologues in other organisms. The αr7 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 αr7 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: αr7_Smedr7C = Sinorhizobium medicae WSM419 chromosome (NC_009636), αr7_Smr7C = Sinorhizobium meliloti 1021 (NC_003047), αr7_Sfr7C = Sinorhizobium fredii NGR234 chromosome (NC_012587), αr7_Atr7C = Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062), αr7_AH13r7C = Agrobacterium sp. H13-3 chromosome (NC_015183), αr7_ReCIATr7C = Rhizobium etli CIAT 652 (NC_010994), αr7_Arr7CI = Agrobacterium radiobacter K84 chromosome 1 (NC_011985), αr7_Rlt2304r7C = Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369), αr7_Avr7CI = Agrobacterium vitis S4 chromosome 1 (NC_011989), αr7_Rlvr7C = Rhizobium leguminosarum bv. viciae 3841 (NC_008380), αr7_Rlt1325r7C = Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850), αr7_ReCFNr7C = Rhizobium etli CFN 42 (NC_007761), αr7_Mlr7C = Mesorhizobium loti MAFF303099 chromosome (NC_002678), αr7_MsBNCr7C = Mesorhizobium sp. BNC1 (NC_008254), αr7_Mcr7C = Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923), αr7_Bcr7CI = Brucella canis ATCC 23365 chromosome I (NC_010103), αr7_Bs23445r7CI = Brucella suis ATCC 23445 chromosome I (NC_010169), αr7_Bm16Mr7CI = Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317), αr7_BaS19r7CI = Brucella abortus S19 chromosome 1 (NC_010742), αr7_Bm23457r7CI = Brucella melitensis ATCC 23457 chromosome I (NC_012441), αr7_Bs1330r7CI = Brucella suis 1330 chromosome I (NC_004310), αr7_Ba19941r7CI = Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932), αr7_Bmar7CI = Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618), αr7_Bor7CI = Brucella ovis ATCC 25840 chromosome I (NC_009505), αr7_Bmir7CI = Brucella microti CCM 4915 chromosome 1 (NC_013119), αr7_Oar7CI = Ochrobactrum anthropi ATCC 49188 chromosome 1 (NC_009667).
Table 2: Detailed Genomic context information of the α7 sRNA seed members.
Family Feature Name Strand Begin End Protein name Annotation Organism
αr7 gene Smed_3381 R 3581962 3584976 YP_001329037.1 DNA polymerase Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr7 sRNA Smedr7C D 3585152 3585302 - - Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr7 gene Smed_3382 D 3585430 3585873 YP_001329038.1 MarR family transcriptional regulator Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr7 gene SMc02850 R 198469 201483 NP_384281.1 DNA polymerase Sinorhizobium meliloti 1021 (NC_003047)
αr7 sRNA Smr7C D 201679 201828 - - Sinorhizobium meliloti 1021 (NC_003047)
αr7 gene SMc02851 D 201956 202399 NP_384282.1 MarR family transcriptional regulator Sinorhizobium meliloti 1021 (NC_003047)
αr7 gene NGR_c35130 R 3725266 3726657 YP_002827990.1 peptidase M2 Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr7 sRNA Sfr7C R 3727302 3727450 - - Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr7 gene NGR_c35150 D 3727551 3730673 YP_002827992.1 DNA polymerase Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr7 gene Atu0109 R 112000 112446 NP_353144.2 MarR family transcriptional regulator Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062)
αr7 sRNA Atr7C R 112535 112678 - - Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062)
αr7 gene Atu8081 R 112724 113134 NP_353145.1 hypothetical protein Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062)
αr7 gene AGROH133_02963 R 111988 112422 YP_004277416.1 MarR family transcriptional regulator Agrobacterium sp. H13-3 chromosome (NC_015183)
αr7 sRNA AH13r7C R 112523 112667 - - Agrobacterium sp. H13-3 chromosome (NC_015183)
αr7 gene AGROH133_02965 D 112837 115824 YP_004277417.1 DNA polymerase Agrobacterium sp. H13-3 chromosome (NC_015183)
αr7 gene RHECIAT_CH0000189 R 205143 205559 YP_001976363.1 MarR family transcriptional regulator Rhizobium etli CIAT 652 (NC_010994)
αr7 sRNA ReCIATr7C R 205678 205811 - - Rhizobium etli CIAT 652 (NC_010994)
αr7 gene RHECIAT_CH0000190 D 205998 208991 YP_001976364.1 DNA polymerase Rhizobium etli CIAT 652 (NC_010994)
αr7 gene Arad_0270 R 242680 243111 YP_002542926.1 MarR family transcriptional regulator Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr7 sRNA Arr7CI R 243240 243377 - - Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr7 gene Arad_0271 D 243543 246545 YP_002542927.1 DNA polymerase Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr7 gene Rleg2_4102 R 4279984 4280400 YP_002283590.1 MarR family transcriptional regulator Rhizobium leguminosarum bv trifolii WSM2304 chromosome (NC_011369)
αr7 sRNA Rlt2304r7C R 4280520 4280653 - - Rhizobium leguminosarum bv trifolii WSM2304 chromosome (NC_011369)
αr7 gene Rleg2_4103 D 4280807 4283806 YP_002283591.1 DNA polymerase Rhizobium leguminosarum bv trifolii WSM2304 chromosome (NC_011369)
αr7 gene Avi_0299 R 252729 255707 YP_002548197.1 DNA polymerase Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr7 sRNA Avr7CI D 255869 256019 - - Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr7 gene Avi_0300 D 256094 256543 YP_002548198.1 MarR family transcriptional regulator Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr7 gene RL0159 R 192083 192499 YP_765764.1 MarR family transcriptional regulator Rhizobium leguminosarum bv viciae 3841 (NC_008380)
αr7 sRNA Rlvr7C R 192620 192753 - - Rhizobium leguminosarum bv viciae 3841 (NC_008380)
αr7 gene RL0160 D 192994 196044 YP_765765.1 DNA polymerase Rhizobium leguminosarum bv viciae 3841 (NC_008380)
αr7 gene Rleg_4422 R 4553028 4553444 YP_002978199.1 MarR family transcriptional regulator Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr7 sRNA Rlt1325r7C R 4553564 4553697 - - Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr7 gene Rleg_4423 D 4553938 4556988 YP_002978200.1 DNA polymerase Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr7 gene RHE_CH00150 R 163227 163643 YP_467702.1 MarR family transcriptional regulator Rhizobium etli CFN 42 (NC_007761)
αr7 sRNA ReCFNr7C R 163762 163895 - - Rhizobium etli CFN 42 (NC_007761)
αr7 gene RHE_CH00151 D 164051 167050 YP_467703.1 DNA polymerase Rhizobium etli CFN 42 (NC_007761)
αr7 gene mll3297 R 2646732 2648117 NP_104434.1 peptidase M2 Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr7 sRNA Mlr7C R 2648243 2648390 - - Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr7 gene mlr3298 D 2648514 2651525 NP_104435.1 DNA polymerase Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr7 gene Meso_3945 R 4248490 4251426 YP_676477.1 DNA polymerase Mesorhizobium sp. BNC1 (NC_008254)
αr7 sRNA MsBNCr7C D 4251581 4251722 - - Mesorhizobium sp. BNC1 (NC_008254)
αr7 gene Meso_3946 R 4251731 4253149 YP_676478.1 6-phosphogluconate dehydrogenase Mesorhizobium sp. BNC1 (NC_008254)
αr7 gene Mesci_1702 R 1778784 1781777 YP_004140907.1 DNA polymerase Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
αr7 sRNA Mcr7C D 1781903 1782047 - - Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
αr7 gene Mesci_1703 D 1782152 1783537 YP_004140908.1 peptidase M2 Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
αr7 gene BCAN_A0124 R 132964 134379 YP_001591996.1 peptidase M2 Brucella canis ATCC 23365 chromosome I (NC_010103)
αr7 sRNA Bcr7CI R 134573 134715 - - Brucella canis ATCC 23365 chromosome I (NC_010103)
αr7 gene BCAN_A0126 D 134940 137879 YP_001591998.1 DNA polymerase Brucella canis ATCC 23365 chromosome I (NC_010103)
αr7 gene BSUIS_A0126 R 133299 134714 YP_001626800.1 peptidase M2 Brucella suis ATCC 23445 chromosome I (NC_010169)
αr7 sRNA Bs23445r7CI R 134908 135050 - - Brucella suis ATCC 23445 chromosome I (NC_010169)
αr7 gene BSUIS_A0128 D 135275 138211 YP_001626802.1 DNA polymerase Brucella suis ATCC 23445 chromosome I (NC_010169)
αr7 gene BMEI1825 R 1865184 1868168 NP_540742.1 DNA polymerase Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317)
αr7 sRNA Bm16Mr7CI D 1868345 1868487 - - Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317)
αr7 gene BMEI1827 D 1868645 1870096 NP_540744.1 peptidase M2 Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317)
αr7 gene BAbS19_I01130 R 132726 134141 YP_001934145.1 peptidase M2 Brucella abortus S19 chromosome 1 (NC_010742)
αr7 sRNA BaS19r7CI R 134335 134477 - - Brucella abortus S19 chromosome 1 (NC_010742)
αr7 gene BAbS19_I01140 D 134702 137638 YP_001934146.1 DNA polymerase Brucella abortus S19 chromosome 1 (NC_010742)
αr7 gene BMEA_A0128 R 132946 134361 YP_002731894.1 peptidase M2 Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr7 sRNA Bm23457r7CI R 134555 134697 - - Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr7 gene BMEA_A0130 D 134922 137858 YP_002731896.1 DNA polymerase Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr7 gene BR0121 R 132981 134396 NP_697162.1 peptidase M2 Brucella suis 1330 chromosome I (NC_004310)
αr7 sRNA Bs1330r7CI R 134590 134732 - - Brucella suis 1330 chromosome I (NC_004310)
αr7 gene BR0123 D 134957 137896 NP_697164.1 DNA polymerase Brucella suis 1330 chromosome I (NC_004310)
αr7 gene BruAb1_0118 R 134340 135755 YP_220895.1 peptidase M2 Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr7 sRNA Ba19941r7CI R 135949 136091 - - Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr7 gene BruAb1_0120 D 136316 139252 YP_220897.1 DNA polymerase Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr7 gene BAB1_0118 R 130707 132122 YP_413614.1 peptidase M2 Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr7 sRNA Bmar7CI R 132316 132458 - - Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr7 gene BAB1_0120 D 132683 135619 YP_413616.1 DNA polymerase Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr7 gene BOV_0118 R 133280 134695 YP_001258159.1 peptidase M2 Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr7 sRNA Bor7CI R 134888 135029 - - Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr7 gene BOV_0119 D 135254 138190 YP_001258160.1 DNA polymerase Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr7 gene BMI_I124 R 134558 135973 YP_003106091.1 peptidase M2 Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr7 sRNA Bmir7CI R 136167 136309 - - Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr7 gene BMI_I126 D 136534 139470 YP_003106093.1 DNA polymerase Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr7 gene Oant_0136 R 148306 149715 YP_001368696.1 peptidase M2 Ochrobactrum anthropi ATCC 49188 chromosome 1 (NC_009667)
αr7 sRNA Oar7CI R 149814 149972 - - Ochrobactrum anthropi ATCC 49188 chromosome 1 (NC_009667)
αr7 gene Oant_0137 D 150127 153057 YP_001368697.1 DNA polymerase Ochrobactrum anthropi ATCC 49188 chromosome 1 (NC_009667)

References

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