Biology:αr45 RNA

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αr45 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 (Smr45C) was found in a Sinorhizobium meliloti 1021 locus located in the chromosome (C). Further homology and structure conservation analysis identified homologs in several nitrogen-fixing symbiotic rhizobia (i.e. S. medicae, S. fredii, Rhizobium 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), in Bartonella species (i.e. B. henselae, B. clarridgeiae, B. tribocorum, B. quintana, B. bacilliformis, B. grahamii), in several members of the Xanthobactereacea family (i.e. Azorhizobium caulinodans, Starkey novella, Xhantobacter autotrophicus), and in some representatives of the Beijerinckiaceae family (i.e. Methylocella silvestris, Beijerinckia indica subsp. indica). αr45C RNA species are 147-153 nt long (Table 1) and share a well defined common secondary structure (Figure 1). All of the αr45 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

Smr45C sRNA was described by del Val et al.,[1] as a result of a computational comparative genomic approach 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 smr45C locus did express a single transcript of 130-179 nt length, which accumulated differentially in free-living and endosymbiotic bacteria. TAP-based 5’-RACE experiments mapped the transcription start site (TSS) of the full-length Smr45C transcript to the 3,105,445 nt position in the S. meliloti 1021 genome (http://iant.toulouse.inra.fr/bacteria/annotation/cgi/rhime.cgi) whereas the 3’-end was initially assumed to be located at the 3,105,265 nt position matching the last residue of a short stretch of Us (Figure 2) of a putative, but low-rated, Rho-independent terminator. Recent deep sequencing-based characterization of the small RNA fraction (50-350 nt) of S. meliloti 2011 further confirmed the expression of Smr45C (here referred to as SmelC706), and mapped the full-length transcript to the same 5’ end and to the 3' end position 3,105,298.[2]

Figure 1: Covariance Model in stockholm format showing the consensus structure for the αr45 family. Each of the stems represented by the structure line #=GC SS_cons is in a different color. Covariance Model in stockholm format can be downloaded here.

The nucleotide sequence of Smr45C 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. Smr45C 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)[3] (Figure 2). This CM was used in a further search for new members of the αr45 family in the existing bacterial genomic databases.

Table 1: αr45 homologs in other symbionts and pathogens
CM model Name GI accession number begin end strand %GC length Organism
αr45 Smr45C gi|15963753|ref|NC_003047.1| 3105265 3105445 - 59 148 Sinorhizobium meliloti 1021
αr45 Smedr45C gi|150395228|ref|NC_009636.1| 2892729 2892909 - 59 148 Sinorhizobium medicae WSM419 chromosome
αr45 Sfr45C gi|227820587|ref|NC_012587.1| 3069095 3069275 - 59 148 Sinorhizobium fredii NGR234 chromosome
αr45 Atr45C gi|159185562|ref|NC_003063.2| 205601 205782 - 57 148 Agrobacterium tumefaciens str. C58 chromosome linear
αr45 ReCIATr45C gi|190889639|ref|NC_010994.1| 3953756 3953936 - 59 148 Rhizobium etli CIAT 652
αr45 Arr45CI gi|222084201|ref|NC_011985.1| 3124263 3124442 - 57 147 Agrobacterium radiobacter K84 chromosome 1
αr45 Rlt2304r45C gi|209547612|ref|NC_011369.1| 3504209 3504389 - 59 148 Rhizobium leguminosarum bv. trifolii WSM2304
αr45 Avr45CI gi|222147015|ref|NC_011989.1| 3166967 3167147 - 59 148 Agrobacterium vitis S4 chromosome 1
αr45 Rlvr45C gi|116249766|ref|NC_008380.1| 4405210 4405390 - 59 148 Rhizobium leguminosarum bv. viciae 3841
αr45 Rlt1325r45C gi|241202755|ref|NC_012850.1| 3739371 3739551 - 59 148 Rhizobium leguminosarum bv. trifolii WSM1325
αr45 ReCFNr45C gi|86355669|ref|NC_007761.1| 3840978 3841158 - 59 148 Rhizobium etli CFN 42
αr45 Mlr45C gi|57165207|ref|NC_002678.2| 2390687 2390867 - 62 147 Mesorhizobium loti MAFF303099 chromosome
αr45 Mcr45C gi|319779749|ref|NC_014923.1| 1999110 1999290 + 63 147 Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome
αr45 Bcr45CII gi|161620094|ref|NC_010104.1| 97148 97326 + 60 143 Brucella canis ATCC 23365 chromosome II
αr45 Bs23445r45CII gi|163844199|ref|NC_010167.1| 97254 97432 + 60 146 Brucella suis ATCC 23445 chromosome II
αr45 Bm16Mr45CII gi|17988344|ref|NC_003318.1| 1172651 1172829 - 60 146 Brucella melitensis bv. 1 str. 16M chromosome II
αr45 BaS19r45CII gi|189022234|ref|NC_010740.1| 96948 97126 + 60 146 Brucella abortus S19 chromosome 2
αr45 Bm23457r45CII gi|225685871|ref|NC_012442.1| 97129 97307 + 60 146 Brucella melitensis ATCC 23457 chromosome II
αr45 Bs1330r45CII gi|56968493|ref|NC_004311.2| 97128 97306 + 60 146 Brucella suis 1330 chromosome II
αr45 Ba19941r45CII gi|62316961|ref|NC_006933.1| 96885 97063 + 60 146 Brucella abortus bv. 1 str. 9-941 chromosome II
αr45 Bmar45CII gi|83268957|ref|NC_007624.1| 96950 97128 + 60 146 Brucella melitensis biovar Abortus 2308 chromosome II
αr45 Bor45CII gi|148557829|ref|NC_009504.1| 96814 96992 + 60 146 Brucella ovis ATCC 25840 chromosome II
αr45 Bmir45CII gi|256014795|ref|NC_013118.1| 97102 97280 + 60 146 Brucella microti CCM 4915 chromosome 2
αr45 Oar45CII gi|153010078|ref|NC_009668.1| 1673505 1673683 - 60 146 Brucella anthropi ATCC 49188 chromosome 2
αr45 MsBNCr45C gi|110632362|ref|NC_008254.1| 2952752 2952930 + 60 146 Mesorhizobium sp. BNC1
αr45 Bahr45C gi|49474831|ref|NC_005956.1| 1421835 1422014 - 54 147 Bartonella henselae str. Houston-1
αr45 Bacr45C gi|319898193|ref|NC_014932.1| 1277567 1277776 - 54 147 Bartonella clarridgeiae 73
αr45 Batr45C gi|163867306|ref|NC_010161.1| 1865843 1866022 - 54 147 Bartonella tribocorum CIP 105476
αr45 Baqr45C gi|49473688|ref|NC_005955.1| 1185140 1185319 - 53 147 Bartonella quintana str. Toulouse
αr45 Babr45C gi|121601635|ref|NC_008783.1| 1120052 1120229 - 56 147 Bartonella bacilliformis KC583
αr45 Bagr45C gi|240849682|ref|NC_012846.1| 1761390 1761567 - 53 147 Bartonella grahamii as4aup
αr45 Acr45C gi|158421624|ref|NC_009937.1| 385443 385629 - 64 154 Azorhizobium caulinodans ORS 571
αr45 Stnr45C gi|298290017|ref|NC_014217.1| 4175745 4175703 + 65 156 Starkeya novella DSM 506 chromosome
αr45 Xar45C gi|154243958|ref|NC_009720.1| 2404335 2404523 - 63 156 Xanthobacter autotrophicus Py2 chromosome
αr45 Mesr45C gi|217976200|ref|NC_011666.1| 1244610 1244795 - 64 155 Methylocella silvestris BL2 chromosome
αr45 Beir45C gi|182677002|ref|NC_010581.1| 1241316 1241498 - 61 153 Beijerinckia indica subsp. indica ATCC 9039 chromosome

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[4] with very similar predictions. The manual inspection of the sequences found with the CM using Infernal allowed finding 39 closer homolog sequences, all of them present as single chromosomal copies in the α-proteobacterial genomes. The rhizobial species encoding these homologs to Smr45C were: S. medicae and S. fredii, two R. leguminosarum trifolii strains (WSM304 and WSM35), 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, Brucella species (B. ovis, B. canis, B. abortus, B. microtis, and several biobars of B. melitensis), Brucella anthropi, the Mesorhizobium species loti, M. ciceri and M. BNC., Bartonella species (i.e. B. henselae, B. clarridgeiae, B. tribocorum, B. quintana, B. bacilliformis, B. grahamii). All these sequences showed significant Infernal E-values (8.93E-40 – 6.12E-36) and bit-scores. The rest of the sequences found with the model showed high E-values between (3.28E-06 and 4.56E-04) but lower bit-scores and are encoded by several members of the Xanthobactereacea family (i.e. A. caulinodans, Sa. novella, X. autotrophicus), Me. silvestris, and Be. indica subsp. indica.

Figure 2: Consensus secondary structure of Smr45C and the ar45 family predicted by RNA[5] and RNAalifold.[6] The color scheme of Smr45C represent the base pair probabilities. The coloring scheme for the ar45 family structure is based on 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. The gene strand is represented with the file direction.
Figure 3: Phylogenetic distribution of known and predicted αr45 genes. Gene numbers are based on computational analysis using the program Infernal. Legend: Smr45C = Sinorhizobium meliloti 1021 (NC_003047), Smedr45C = Sinorhizobium medicae WSM419 chromosome (NC_009636), Sfr45C = Sinorhizobium fredii NGR234 chromosome (NC_012587), Atr45C = Agrobacterium tumefaciens str. C58 chromosome linear (NC_003063), ReCIATr45C = Rhizobium etli CIAT 652 (NC_010994), Arr45C = Agrobacterium radiobacter K84 chromosome 1 (NC_011985), Rlt2304r45C = Rhizobium leguminosarum bv. trifolii WSM2304 (NC_011369), Avr45C = Agrobacterium vitis S4 chromosome 1 (NC_011989), Rlvr45C = Rhizobium leguminosarum bv. viciae 3841 (NC_008380), Rlt1325r45C = Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850), ReCFNr45C = Rhizobium etli CFN 42 (NC_007761), Mlr45C = Mesorhizobium loti MAFF303099 chromosome (NC_002678), Mcr45C = Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923), Bcr45CII = Brucella canis ATCC 23365 chromosome II (NC_010104), Bs23445r45CII = Brucella suis ATCC 23445 chromosome II (NC_010167), Bm16Mr45CII = Brucella melitensis bv. 1 str. 16M chromosome II (NC_003318), BaS19r45CII = Brucella abortus S19 chromosome 2 (NC_010740), Bm23457r45CII = Brucella melitensis ATCC 23457 chromosome II (NC_012442), Bs1330r45CII = Brucella suis 1330 chromosome II (NC_004311), Ba19941r45CII = Brucella abortus bv. 1 str. 9-941 chromosome II (NC_006933), Bmar45CII = Brucella melitensis biovar Abortus 2308 chromosome II (NC_007624), Bor45CII = Brucella ovis ATCC 25840 chromosome II (NC_009504), Bmir45CII = Brucella microti CCM 4915 chromosome 2 (NC_013118), Oar45C = Brucella anthropi ATCC 49188 chromosome 2 (NC_009668), MsBNCr45C = Mesorhizobium sp. BNC1 (NC_008254), Bahr45C = Bartonella henselae str. Houston-1 (NC_005956), Bacr45C = Bartonella clarridgeiae 73 (NC_014932), Batr45C = Bartonella tribocorum CIP 105476 (NC_010161), Baqr45C = Bartonella quintana str. Toulouse (NC_005955), Babr45C = Bartonella bacilliformis KC583 (NC_008783), Bagr45C = Bartonella grahamii as4aup (NC_012846), Ac571r45C = Azorhizobium caulinodans ORS 571 (NC_009937), Stnr45C = Starkeya novella DSM 506 chromosome (NC_014217), Xar45C = Xanthobacter autotrophicus Py2 chromosome (NC_009720), Mesr45C = Methylocella silvestris BL2 chromosome (NC_011666), Beir45C = Beijerinckia indica subsp. indica ATCC 9039 chromosome (NC_010581), Rhpr45C = Rhodopseudomonas palustris BisA53 chromosome (NC_008435).

Expression information

The expression of Smr45C in S. meliloti 1021 was assessed 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] The expression of Smr45C in free-living bacteria was found to be growth-dependent, being the gene strongly down-regulated when bacteria entered the stationary phase. However, luteolin moderately stimulated the expression of Smr45C (2-fold) but the gene was not detectable in endosymbiotic bacteria.

Recent co-inmuno precipitation experiments[7] corroborate that Smr45C, does bind the bacterial protein Hfq for efficient target binding.

Promoter Analysis

All the promoter regions of the αr45 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 homolog 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.[8] To identify binding sites for other known transcription factors we used the fasta sequences provided by RegPredict[9](http://regpredict.lbl.gov/regpredict/help.html), and used those position weight matrices (PSWM) provided by RegulonDB[10] (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[11] (http://meme.sdsc.edu/meme4_6_1/intro.html) and used relaxed regular expressions (i.e. pattern matching) over all Smr45C homologs promoters.

This study predicts differences in the regulation of the expression of the αr45 representatives in the different α-proteobacterial species. The Sinorhizobium, Rhizobium, and Agrobacterium groups presented a very well conserved motif that matches the consensus sequence recognized by the maltose repressor Mall. Furthermore, the promoters of the αr45 members of the . Furthermore, the promoters of the αr45 members of the Sinorhizobium group presented an additional conserved region between positions -60 and -85 (boxed in orange in Figure 4), with significant similarity to the matrix SMb21598_Rhizobiales from Reg_Predict. This binding site corresponds to a transcriptional regulator of the LacI family. The Rhizobium group, presented also a well conserved motif in this region for which no significant similarity could be found (marked in green in Figure 4). This analysis also revealed an extended conserved sequence stretch among the promoters of the Brucella and Bartonella αr45 sRNA loci, but no known transcription factor binding sites were recognizable in these motifs.

Figure 4: Alignment of the promoter region of αr45 members. All members presented putative σ70 promoters with -35 and -10 boxes marked in green and red respectively.

Genomic Context

All members of the αr45 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.[12][13][14] The genomic regions of the αr45 sRNAs from Sinorhizobium, Rhizobium, A. vitis and A. radiobacter exhibited a great degree of conservation including the upstream and downstream genes which have been predicted to code for a LysR family transcriptional regulator and an ornithine descarboxilase, respectively (solo como aclaración, upstream and downstream se refieren al sentido de transcripción). Partial synteny of the αr45 genomic regions was observed in the Mesorhizobium and Brucella species where instead of aLysR family transcriptional regulator' gene an amidase coding gene was found. In Bartonella species the αr45 upstream gene was always found to code for a protein containing a rhodanase domain. In the genomic regions of the αr45 homologs in more distantly related α-proteobacteria (e.g. Starkeya, Metthylocella or Xanthobacter species) synteny was restricted to the downstream ornithine descarboxylase gene.

Figure 5: Genomic context scheme of Smr45C and its closest homologues in other organisms. The αr45 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 αr45 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: αr45_Smr45C = Sinorhizobium meliloti 1021 (NC_003047), αr45_Smedr45C = Sinorhizobium medicae WSM419 chromosome (NC_009636), αr45_Sfr45C = Sinorhizobium fredii NGR234 chromosome (NC_012587), αr45_Atr45C = Agrobacterium tumefaciens str. C58 chromosome linear (NC_003063), αr45_ReCIATr45C = Rhizobium etli CIAT 652 (NC_010994), αr45_Arr45C = Agrobacterium radiobacter K84 chromosome 1 (NC_011985), αr45_Rlt2304r45C = Rhizobium leguminosarum bv. trifolii WSM2304 (NC_011369), αr45_Avr45C = Agrobacterium vitis S4 chromosome 1 (NC_011989), αr45_Rlvr45C = Rhizobium leguminosarum bv. viciae 3841 (NC_008380), αr45_Rlt1325r45C = Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850), αr45_ReCFNr45C = Rhizobium etli CFN 42 (NC_007761), αr45_Mlr45C = Mesorhizobium loti MAFF303099 chromosome (NC_002678), αr45_Mcr45C = Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923), αr45_Bcr45CII = Brucella canis ATCC 23365 chromosome II (NC_010104), αr45_Bs23445r45CII = Brucella suis ATCC 23445 chromosome II (NC_010167), αr45_Bm16Mr45CII = Brucella melitensis bv. 1 str. 16M chromosome II (NC_003318), αr45_BaS19r45CII = Brucella abortus S19 chromosome 2 (NC_010740), αr45_Bm23457r45CII = Brucella melitensis ATCC 23457 chromosome II (NC_012442), αr45_Bs1330r45CII = Brucella suis 1330 chromosome II (NC_004311), αr45_Ba19941r45CII = Brucella abortus bv. 1 str. 9-941 chromosome II (NC_006933), αr45_Bmar45CII = Brucella melitensis biovar Abortus 2308 chromosome II (NC_007624), αr45_Bor45CII = Brucella ovis ATCC 25840 chromosome II (NC_009504), αr45_Bmir45CII = Brucella microti CCM 4915 chromosome 2 (NC_013118), αr45_Oar45C = Brucella anthropi ATCC 49188 chromosome 2 (NC_009668), αr45_MsBNCr45C = Mesorhizobium sp. BNC1 (NC_008254), αr45_Bahr45C = Bartonella henselae str. Houston-1 (NC_005956), αr45_Bacr45C = Bartonella clarridgeiae 73 (NC_014932), αr45_Batr45C = Bartonella tribocorum CIP 105476 (NC_010161), αr45_Baqr45C = Bartonella quintana str. Toulouse (NC_005955), αr45_Babr45C = Bartonella bacilliformis KC583 (NC_008783), αr45_Bagr45C = Bartonella grahamii as4aup (NC_012846), αr45_Ac571r45C = Azorhizobium caulinodans ORS 571 (NC_009937), αr45_Stnr45C = Starkeya novella DSM 506 chromosome (NC_014217), αr45_Xar45C = Xanthobacter autotrophicus Py2 chromosome (NC_009720), αr45_Mesr45C = Methylocella silvestris BL2 chromosome (NC_011666), αr45_Beir45C = Beijerinckia indica subsp. indica ATCC 9039 chromosome (NC_010581), αr45_Rhpr45C = Rhodopseudomonas palustris BisA53 chromosome (NC_008435).
Table 2: Detailed Genomic context information of the α45 sRNA members.
Family Feature Name Strand Begin End Protein name Annotation Organism
αr45 gene SMc02983 R 3103912 3105051 NP_386981.1 Ornithine or Arginine decarboxylase Sinorhizobium meliloti 1021 (NC_003047)
αr45 sRNA Smr45C R 3105265 3105445 - - Sinorhizobium meliloti 1021 (NC_003047)
αr45 gene SMc02984 D 3105638 3106531 NP_386982.1 LysR family transcriptional regulator Sinorhizobium meliloti 1021 (NC_003047)
αr45 gene Smed_2772 R 2891376 2892509 YP_001328437.1 Ornithine decarboxylase Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr45 sRNA Smedr45C R 2892729 2892909 - - Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr45 gene Smed_2773 D 2893045 2893959 YP_001328438.1 LysR family transcriptional regulator Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr45 gene NGR_c29260 R 3067740 3068873 YP_002827423.1 Ornithine decarboxylase Sinorhizobium fredii NGR234 chromosome(NC_012587)
αr45 sRNA Sfr45C R 3069095 3069275 - - Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr45 gene NGR_c29280 D 3069481 3070374 YP_002827424.1 LysR family transcriptional regulator Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr45 gene RL4156 R 4403850 4404983 YP_769731.1 Lisine-Ornithine decarboxylase Rhizobium leguminosarum bv viciae 3841 (NC_008380)
αr45 sRNA Rlvr45C R 4405210 4405390 - - Rhizobium leguminosarum bv viciae 3841 (NC_008380)
αr45 gene RL4157 D 4405512 4406405 YP_769732.1 LysR family transcriptional regulator Rhizobium leguminosarum bv viciae 3841 (NC_008380)
αr45 gene RHECIAT_CH0003899 R 3952396 3953529 YP_001980014.1 Ornithine decarboxylase Rhizobium etli CIAT 652 (NC_010994)
αr45 sRNA ReCIATr45C R 3953756 3953936 - - Rhizobium etli CIAT 652 (NC_010994)
αr45 gene RHECIAT_CH0003900 D 3954059 3954952 YP_001980015.1 LysR family transcriptional regulator Rhizobium etli CIAT 652 (NC_010994)
αr45 gene Rleg2_3390 R 3502850 3503983 YP_002282883.1 Ornithine decarboxylase Rhizobium leguminosarum bv trifolii WSM2304 (NC_011369)
αr45 sRNA Rlt2304r45C R 3504209 3504389 - - Rhizobium leguminosarum bv trifolii WSM2304 (NC_011369)
αr45 gene Rleg2_3391 D 3504512 3505405 YP_002282884.1 LysR family transcriptional regulator Rhizobium leguminosarum bv trifolii WSM2304 (NC_011369)
αr45 gene Rleg_3689 R 3738011 3739144 YP_002977471.1 Ornithine decarboxylase Rhizobium leguminosarum bv trifolii WSM1325 (NC_012850)
αr45 sRNA Rlt1325r45C R 3739371 3739551 - - Rhizobium leguminosarum bv trifolii WSM1325 (NC_012850)
αr45 gene Rleg_3690 D 3739671 3740564 YP_002977472.1 LysR family transcriptional regulator Rhizobium leguminosarum bv trifolii WSM1325 (NC_012850)
αr45 gene RHE_CH03628 R 3838931 3839521 YP_471110.1 acetyltransferase Rhizobium etli CFN 42 (NC_007761)
αr45 sRNA ReCFNr45C R 3840978 3841158 - - Rhizobium etli CFN 42 (NC_007761)
αr45 gene RHE_CH03631 D 3842303 3842944 YP_471113.1 DUF1007 Rhizobium etli CFN 42 (NC_007761)
αr45 gene Avi_3806 R 3165600 3166733 YP_002550752.1 Ornithine decarboxylase Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr45 sRNA Avr45CI R 3166967 3167147 - - Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr45 gene Avi_3808 D 3167282 3168211 YP_002550753.1 LysR family transcriptional regulator Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr45 gene Arad_3911 R 3122903 3124036 YP_002545680.1 Ornithine decarboxylase Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr45 sRNA Arr45CI R 3124263 3124442 - - Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr45 gene Arad_3912 D 3124569 3125462 YP_002545681.1 LysR family transcriptional regulator Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr45 gene Atu3196 R 204249 205382 NP_357406.2 Ornithine decarboxylase Agrobacterium tumefaciens str. C58 chromosome linear (NC_003063)
αr45 sRNA Atr45C R 205601 205782 - - Agrobacterium tumefaciens str. C58 chromosome linear (NC_003063)
αr45 gene Atu3197 D 205919 206812 NP_357405.2 LysR family transcriptional regulator Agrobacterium tumefaciens str. C58 chromosome linear (NC_003063)
αr45 gene Meso_2714 R 2951455 2952642 YP_675256.1 amidase Mesorhizobium sp. BNC1 (NC_008254)
αr45 sRNA MsBNCr45C D 2952752 2952930 - - Mesorhizobium sp. BNC1 (NC_008254)
αr45 gene Meso_2715 D 2953176 2954309 YP_675257.1 Ornithine decarboxylase Mesorhizobium sp. BNC1 (NC_008254)
αr45 gene Oant_4245 R 1672055 1673188 YP_001372774.1 Ornithine decarboxylase Brucella anthropi ATCC 49188 chromosome 2 (NC_009668)
αr45 sRNA Oar45CII R 1673505 1673683 - - Brucella anthropi ATCC 49188 chromosome 2 (NC_009668)
αr45 gene Oant_4246 D 1673866 1675053 YP_001372775.1 amidase Brucella anthropi ATCC 49188 chromosome 2 (NC_009668)
αr45 gene BOV_A0091 R 94529 95420 A5VTL3 amidase Brucella ovis ATCC 25840 chromosome II (NC_009504)
αr45 sRNA Bor45CII D 96814 96992 - - Brucella ovis ATCC 25840 chromosome II (NC_009504)
αr45 gene BOV_A0092 D 97214 98347 YP_001257169.1 Ornithine decarboxylase Brucella ovis ATCC 25840 chromosome II (NC_009504)
αr45 sRNA Bcr45CII D 97148 97326 - - Brucella canis ATCC 23365 chromosome II (NC_010104)
αr45 gene BCAN_B0102 R 95758 96963 YP_001594073.1 amidase Brucella canis ATCC 23365 chromosome II (NC_010104)
αr45 gene BCAN_B0104 D 97548 98681 YP_001594074.1 Lisine-Ornithine decarboxylase Brucella canis ATCC 23365 chromosome II (NC_010104)
αr45I sRNA Bs23445r45CII D 97254 97432 - - Brucella suis ATCC 23445 chromosome II (NC_010167)
αr45 gene BSUIS_B0104 R 95864 97069 YP_001621952.1 amidase Brucella suis ATCC 23445 chromosome II (NC_010167)
αr45 gene BSUIS_B0106 D 97654 98787 YP_001621953.1 Lisine-Ornithine decarboxylase Brucella suis ATCC 23445 chromosome II (NC_010167)
αr45 sRNA Bm16Mr45CII R 1172651 1172829 - - Brucella melitensis bv. 1 str. 16M chromosome II (NC_003318)
αr45 gene BMEII1133 R 1171296 1172429 NP_542111.1 Ornithine decarboxylase Brucella melitensis bv. 1 str. 16M chromosome II (NC_003318)
αr45 gene BMEII1134 D 1173014 1174219 NP_542112.1 amidase Brucella melitensis bv. 1 str. 16M chromosome II (NC_003318)
αr45 sRNA BaS19r45CII D 96948 97126 - - Brucella abortus S19 chromosome 2 (NC_010740)
αr45 gene BAbS19_II00900 R 95559 96764 YP_001932063.1 amidase Brucella abortus S19 chromosome 2 (NC_010740)
αr45 gene BAbS19_II00910 D 97348 98481 YP_001932064.1 Ornithine decarboxylase Brucella abortus S19 chromosome 2 (NC_010740)
αr45 sRNA Bm23457r45CII D 97129 97307 - - Brucella melitensis ATCC 23457 chromosome II (NC_012442)
αr45 gene BMEA_B0101 R 95739 96944 YP_002733935.1 amidase Brucella melitensis ATCC 23457 chromosome II (NC_012442)
αr45 gene BMEA_B0103 D 97529 98662 YP_002733936.1 Lisine-Ornithine decarboxylase Brucella melitensis ATCC 23457 chromosome II (NC_012442)
αr45 sRNA Bmir45CII D 97102 97280 - - Brucella microti CCM 4915 chromosome 2 (NC_013118)
αr45 gene BMI_II99 R 95713 96918 YP_003104900.1 amidase Brucella microti CCM 4915 chromosome 2 (NC_013118)
αr45 gene BMI_II100 D 97502 98635 YP_003104901.1 Ornithine decarboxylase Brucella microti CCM 4915 chromosome 2 (NC_013118)
αr45 sRNA Bs1330r45CII D 97128 97306 - - Brucella suis 1330 chromosome II (NC_004311)
αr45 gene BRA0099 R 95738 96943 NP_699304.1 amidase Brucella suis 1330 chromosome II (NC_004311)
αr45 gene BRA0100 D 97528 98661 NP_699305.1 Ornithine Arginine decarboxylase Brucella suis 1330 chromosome II (NC_004311)
αr45 sRNA Ba19941r45CII D 96885 97063 - - Brucella abortus bv. 1 str. 9-941 chromosome II (NC_006933)
αr45 gene BruAb2_0098 R 95495 96700 YP_222910.1 amidase Brucella abortus bv. 1 str. 9-941 chromosome II (NC_006933)
αr45 gene BruAb2_0099 D 97285 98418 YP_222911.1 Ornithine Arginine decarboxylase Brucella abortus bv. 1 str. 9-941 chromosome II (NC_006933)
αr45 sRNA Bmar45CII D 96950 97128 - - Brucella melitensis biovar Abortus 2308 chromosome II (NC_007624)
αr45 gene BAB2_0097 R 95560 96765 YP_418341.1 amidase Brucella melitensis biovar Abortus 2308 chromosome II (NC_007624)
αr45 gene BAB2_0098 D 97350 98483 YP_418342.1 Ornithine Arginine decarboxylase Brucella melitensis biovar Abortus 2308 chromosome II (NC_007624)
αr45 gene Mesci_1912 R 1997804 1999000 YP_004141115.1 amidase Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
αr45 sRNA Mcr45C D 1999110 1999290 - - Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
αr45 gene Mesci_1913 D 1999541 2000674 YP_004141116.1 Ornithine decarboxylase Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
αr45 gene mll2974 R 2389301 2390434 NP_104188.1 Ornithine decarboxylase Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr45 sRNA Mlr45C R 2390687 2390867 - - Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr45 gene mlr2975 D 2390977 2392173 NP_104189.1 amidase Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr45 gene BH12730 R 1420457 1421590 YP_034014.1 Ornithine decarboxylase Bartonella henselae str. Houston-1 (NC_005956)
αr45 sRNA Bahr45C R 1421835 1422014 - - Bartonella henselae str. Houston-1 (NC_005956)
αr45 gene BH12750 D 1422471 1423014 Pseudogen Bartonella henselae str. Houston-1 (NC_005956)
αr45 gene BARCL_1139 R 1276216 1277577 YP_004159385.1 Lisine-Ornithine decarboxylase Bartonella clarridgeiae 73 (NC_014932)
αr45 sRNA Bacr45C R 1277597 1277776 - - Bartonella clarridgeiae 73 (NC_014932)
αr45 gene BARCL_1140 R 1278001 1278918 YP_004159386.1 rhodanese domain. Bartonella clarridgeiae 73 (NC_014932)
αr45 gene Btr_1749 R 1864467 1865600 YP_001610035.1 Lisine-Ornithine decarboxylase Bartonella tribocorum CIP 105476 (NC_010161)
αr45 sRNA Batr45C R 1865843 1866022 - - Bartonella tribocorum CIP 105476 (NC_010161)
αr45 gene Btr_1751 R 1867923 1868852 YP_001610036.1 rhodanese domain. Bartonella tribocorum CIP 105476 (NC_010161)
αr45 gene BQ10050 R 1183759 1184892 YP_032587.1 Ornithine decarboxylase Bartonella quintana str. Toulouse (NC_005955)
αr45 sRNA Baqr45C R 1185140 1185319 - - Bartonella quintana str. Toulouse (NC_005955)
αr45 gene BQ10070 R 1186001 1186915 YP_032589.1 rhodanese domain. Bartonella quintana str. Toulouse (NC_005955)
αr45 sRNA Babr45C R 1120052 1120229 - - Bartonella bacilliformis KC583 (NC_008783)
αr45 gene BARBAKC583_1090 R 1118676 1119809 YP_989352.1 pyridoxal-dependent decarboxylas Bartonella bacilliformis KC583 (NC_008783)
αr45 gene BARBAKC583_1091 R 1120463 1121380 YP_989353.1 rhodanese domain. Bartonella bacilliformis KC583 (NC_008783)
αr45 sRNA Bagr45C R 1761390 1761567 - - Bartonella grahamii as4aup (NC_012846)
αr45 gene Bgr_15560 R 1760016 1761149 YP_002972413.1 Ornithine decarboxylase Bartonella grahamii as4aup (NC_012846)
αr45 gene Bgr_15590 D 1763885 1764550 YP_002972415.1 2-dehydro-3-deoxyphosphogluconate aldolase Bartonella grahamii as4aup (NC_012846)
αr45 gene AZC_0333 R 384008 385138 YP_001523249.1 Ornithine decarboxylase Azorhizobium caulinodans ORS 571 (NC_009937)
αr45 sRNA Acr45C R 385443 385629 - - Azorhizobium caulinodans ORS 571 (NC_009937)
αr45 gene AZC_0334 D 386047 387324 YP_001523250.1 5-aminolevulinate synthase Azorhizobium caulinodans ORS 571 (NC_009937)
αr45 gene Snov_3938 D 4175011 4175250 YP_003695827.1 hypothetical protein Starkeya novella DSM 506 chromosome (NC_014217)
αr45 sRNA Stnr45C D 4175515 4175703 - - Starkeya novella DSM 506 chromosome (NC_014217)
αr45 gene Snov_3939 D 4175960 4177090 YP_003695828.1 Ornithine decarboxylase Starkeya novella DSM 506 chromosome (NC_014217)
αr45 gene Xaut_2140 R 2402902 2404032 YP_001417041.1 Ornithine decarboxylase Xanthobacter autotrophicus Py2 chromosome (NC_009720)
αr45 sRNA Xar45C R 2404335 2404523 - - Xanthobacter autotrophicus Py2 chromosome (NC_009720)
αr45 gene Xaut_2141 D 2404953 2405258 YP_001417042.1 hypothetical protein Xanthobacter autotrophicus Py2 chromosome (NC_009720)
αr45 gene Msil_1157 R 1243178 1244308 YP_002361488.1 Ornithine decarboxylase Methylocella silvestris BL2 chromosome (NC_011666)
αr45 sRNA Mesr45C R 1244610 1244795 - - Methylocella silvestris BL2 chromosome (NC_011666)
αr45 gene Msil_1158 D 1245160 1246743 YP_002361489.1 glucan biosynthesis protein Methylocella silvestris BL2 chromosome (NC_011666)
αr45 gene Bind_1080 R 1239883 1241013 YP_001832212.1 Ornithine decarboxylase Beijerinckia indica subsp. indica ATCC 9039 chromosome (NC_010581)
αr45 sRNA Beir45C R 1241316 1241498 - - Beijerinckia indica subsp. indica ATCC 9039 chromosome (NC_010581)
αr45 gene Bind_1081 D 1242373 1243974 YP_001832213.1 glucan biosynthesis protein Beijerinckia indica subsp. indica ATCC 9039 chromosome (NC_010581)
αr45 gene RPE_4802 R 5380582 5381724 YP_783701.1 Ornithine decarboxylase Rhodopseudomonas palustris BisA53 chromosome (NC_008435)
αr45 sRNA Rhpr45C R 5381912 5382109 - - Rhodopseudomonas palustris BisA53 chromosome (NC_008435)
αr45 gene RPE_4803 R 5382436 5382696 YP_783702.1 hypothetical protein Rhodopseudomonas palustris BisA53 chromosome (NC_008435)

References

  1. ↑ 1.0 1.1 "Identification of differentially expressed small non-coding RNAs in the legume endosymbiont Sinorhizobium meliloti by comparative genomics". Mol Microbiol 66 (5): 1080–1091. 2007. doi:10.1111/j.1365-2958.2007.05978.x. PMID 17971083. 
  2. ↑ "A genome-wide survey of sRNAs in the symbiotic nitrogen-fixing alpha-proteobacterium Sinorhizobium meliloti". BMC Genomics 11 (245): 436. 2010. doi:10.1186/1471-2164-11-436. PMID 20637113. 
  3. ↑ "Infernal 1.0: inference of RNA alignments". Bioinformatics 25 (10): 1335–1337. 2009. doi:10.1093/bioinformatics/btp157. PMID 19307242. 
  4. ↑ "Inferring Noncoding RNA Families and Classes by Means of Genome-Scale Structure-Based Clustering". PLOS Comput Biol 4 (65): e65. 2007. doi:10.1371/journal.pcbi.0030065. PMID 17432929. Bibcode: 2007PLSCB...3...65W. 
  5. ↑ I. L. Hofacker, W. Fontana, P. F. Stadler, L. S. Bonhoeffer, M. Tacker and P. Schuster (1994). "Fast folding and comparison of RNA secondary structures". Monatshefte für Chemie 125 (2): 167–188. doi:10.1007/BF00818163. 
  6. ↑ Stephan H Bernhart , Ivo L Hofacker , Sebastian Will , Andreas R Gruber and Peter F Stadler (2008). "RNAalifold: improved consensus structure prediction for RNA alignments". BMC Bioinformatics 9 (474): 474. doi:10.1186/1471-2105-9-474. PMID 19014431. 
  7. ↑ "The Sinorhizobium meliloti RNA chaperone Hfq influences central carbon metabolism and the symbiotic interaction with alfalfa". BMC Microbiol 6: 71. 2010. doi:10.1186/1471-2180-10-71. PMID 20205931. 
  8. ↑ "Promoter prediction in the rhizobia". Microbiology 152 (6): 1751–1763. 2006. doi:10.1099/mic.0.28743-0. PMID 16735738. 
  9. ↑ "RegPredict: an integrated system for regulon inference in prokaryotes by comparative genomics approach". Nucleic Acids Research 38 (Web Server issue): W299–W307. 2010. doi:10.1093/nar/gkq531. PMID 20542910. 
  10. ↑ "RegulonDB version 7.0: transcriptional regulation of Escherichia coli K-12 integrated within genetic sensory response units (Gensor Units)". Nucleic Acids Research 39 (Database issue): D98–D105. 2010. doi:10.1093/nar/gkq1110. PMID 21051347. 
  11. ↑ "Fitting a mixture model by expectation maximization to discover motifs in biopolymers". Proceedings. International Conference on Intelligent Systems for Molecular Biology 2: 28–36. 1994. PMID 7584402. 
  12. ↑ "GOPET: a tool for automated predictions of Gene Ontology terms". BMC Bioinformatics 7: 171. 2006. doi:10.1186/1471-2105-7-161. PMID 16549020. 
  13. ↑ "Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research". Bioinformatics 21 (18): 3674–3676. 2005. doi:10.1093/bioinformatics/bti610. PMID 16081474. 
  14. ↑ "ProtSweep, 2Dsweep and DomainSweep: protein analysis suite at DKFZ". Nucleic Acids Res 35 (Web Server issue): W444–50. 2007. doi:10.1093/nar/gkm364. PMID 17526514. 



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