Αr9 RNA explained

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

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.

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
class=cellinside αr9class=cellinside Smr9Cclass=cellinside gi|15963753|ref|NC_003047.1|class=cellinside 1398277class=cellinside 1398425class=cellinside -class=cellinside 46class=cellinside 149class=cellinside Sinorhizobium meliloti 1021
class=cellinside αr9class=cellinside Smedr9Cclass=cellinside gi|150395228|ref|NC_009636.1|class=cellinside 979747class=cellinside 979902class=cellinside -class=cellinside 48class=cellinside 150class=cellinside Sinorhizobium medicae WSM419 chromosome
class=cellinside αr9class=cellinside Sfr9Cclass=cellinside gi|227820587|ref|NC_012587.1|class=cellinside 1130001class=cellinside 1130150class=cellinside -class=cellinside 47class=cellinside 150class=cellinside Sinorhizobium fredii NGR234 chromosome
class=cellinside αr9class=cellinside Atr9Cclass=cellinside gi|159184118|ref|NC_003062.2|class=cellinside 1275297class=cellinside 1275443class=cellinside -class=cellinside 47class=cellinside 147class=cellinside Agrobacterium tumefaciens str. C58 chromosome circular
class=cellinside αr9class=cellinside AH13r9Cclass=cellinside gi|325291453|ref|NC_015183.1|class=cellinside 1215580class=cellinside 1215726class=cellinside -class=cellinside 48class=cellinside 147class=cellinside Agrobacterium sp. H13-3 chromosome
class=cellinside αr9class=cellinside ReCIATr9Cclass=cellinside gi|190889639|ref|NC_010994.1|class=cellinside 1684929class=cellinside 1685072class=cellinside -class=cellinside 48class=cellinside 144class=cellinside Rhizobium etli CIAT 652
class=cellinside αr9class=cellinside Arr9CIclass=cellinside gi|222084201|ref|NC_011985.1|class=cellinside 1481975class=cellinside 1482119class=cellinside -class=cellinside 49class=cellinside 145class=cellinside Agrobacterium radiobacter K84 chromosome 1
class=cellinside αr9class=cellinside Rlt2304r9Cclass=cellinside gi|209547612|ref|NC_011369.1|class=cellinside 1296506class=cellinside 1296650class=cellinside -class=cellinside 48class=cellinside 145class=cellinside Rhizobium leguminosarum bv. trifolii WSM2304 chromosome
class=cellinside αr9class=cellinside Avr9CIclass=cellinside gi|222147015|ref|NC_011989.1|class=cellinside 1448510class=cellinside 1448659class=cellinside -class=cellinside 45class=cellinside 150class=cellinside Agrobacterium vitis S4 chromosome 1
class=cellinside αr9class=cellinside Rlvr9Cclass=cellinside gi|116249766|ref|NC_008380.1|class=cellinside 1802936class=cellinside 1803079class=cellinside -class=cellinside 49class=cellinside 144class=cellinside Rhizobium leguminosarum bv. viciae 3841
class=cellinside αr9class=cellinside Rlt1325r9Cclass=cellinside gi|241202755|ref|NC_012850.1|class=cellinside 1354593class=cellinside 1354736class=cellinside -class=cellinside 47class=cellinside 144class=cellinside Rhizobium leguminosarum bv. trifolii WSM1325
class=cellinside αr9class=cellinside ReCFNr9Cclass=cellinside gi|86355669|ref|NC_007761.1|class=cellinside 1703203class=cellinside 1703345class=cellinside -class=cellinside 47class=cellinside 143class=cellinside Rhizobium etli CFN 42
class=cellinside αr9class=cellinside Mlr9Cclass=cellinside gi|57165207|ref|NC_002678.2|class=cellinside 1127217class=cellinside 1127363class=cellinside +class=cellinside 54class=cellinside 145class=cellinside Mesorhizobium loti MAFF303099 chromosome
class=cellinside αr9class=cellinside Mcr9Cclass=cellinside gi|319779749|ref|NC_014923.1|class=cellinside 3449639class=cellinside 3449786class=cellinside -class=cellinside 52class=cellinside 148class=cellinside Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome
class=cellinside αr9class=cellinside Bcr9CIclass=cellinside gi|161617991|ref|NC_010103.1|class=cellinside 796281class=cellinside 796428class=cellinside -class=cellinside 49class=cellinside 148class=cellinside Brucella canis ATCC 23365 chromosome I
class=cellinside αr9class=cellinside Bs23445r9CIclass=cellinside gi|163842277|ref|NC_010169.1|class=cellinside 817762class=cellinside 817909class=cellinside -class=cellinside 49class=cellinside 148class=cellinside Brucella suis ATCC 23445 chromosome I
class=cellinside αr9class=cellinside Bm16Mr9CIclass=cellinside gi|17986284|ref|NC_003317.1|class=cellinside 1187596class=cellinside 1187743class=cellinside +class=cellinside 49class=cellinside 146class=cellinside Brucella melitensis bv. 1 str. 16M chromosome I
class=cellinside αr9class=cellinside BaS19r9CIclass=cellinside gi|189023268|ref|NC_010742.1|class=cellinside 817898class=cellinside 818045class=cellinside -class=cellinside 49class=cellinside 148class=cellinside Brucella abortus S19 chromosome 1
class=cellinside αr9class=cellinside Bm23457r9CIclass=cellinside gi|225851546|ref|NC_012441.1|class=cellinside 819377class=cellinside 819523class=cellinside -class=cellinside 50class=cellinside 147class=cellinside Brucella melitensis ATCC 23457 chromosome I
class=cellinside αr9class=cellinside Bs1330r9CIclass=cellinside gi|56968325|ref|NC_004310.3|class=cellinside 797917class=cellinside 798064class=cellinside -class=cellinside 49class=cellinside 148class=cellinside Brucella suis 1330 chromosome I
class=cellinside αr9class=cellinside Ba19941r9CIclass=cellinside gi|62288991|ref|NC_006932.1|class=cellinside 819597class=cellinside 819744class=cellinside -class=cellinside 49class=cellinside 148class=cellinside Brucella abortus bv. 1 str. 9-941 chromosome I
class=cellinside αr9class=cellinside Bmar9CIclass=cellinside gi|82698932|ref|NC_007618.1|class=cellinside 815875class=cellinside 816022class=cellinside -class=cellinside 49class=cellinside 148class=cellinside Brucella melitensis biovar Abortus 2308 chromosome I
class=cellinside αr9class=cellinside Bor9CIclass=cellinside gi|148558820|ref|NC_009505.1|class=cellinside 822712class=cellinside 822859class=cellinside -class=cellinside 49class=cellinside 148class=cellinside Brucella ovis ATCC 25840 chromosome I
class=cellinside αr9class=cellinside Bmir9CIclass=cellinside gi|256368465|ref|NC_013119.1|class=cellinside 802078class=cellinside 802225class=cellinside -class=cellinside 49class=cellinside 148class=cellinside Brucella microti CCM 4915 chromosome 1
class=cellinside αr9class=cellinside Oar9CIclass=cellinside gi|153007346|ref|NC_009667.1|class=cellinside 2529108class=cellinside 2529255class=cellinside +class=cellinside 48class=cellinside 146class=cellinside Brucella anthropi ATCC 49188 chromosome 1
class=cellinside αr9class=cellinside MsBCNr9Cclass=cellinside gi|110632362|ref|NC_008254.1|class=cellinside 1141776class=cellinside 1141933class=cellinside -class=cellinside 50class=cellinside 158class=cellinside Mesorhizobium sp. BNC1

Expression information

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) and high salt stress, oxidative stress and cold and hot shock stresses. 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 further revealed up-regulation of Smr9C upon salt, acidic, cold-shock and heat shock stresses.Recent co-inmuno precipitation experiments[7] corroborate that Smr9C, does bind the bacterial protein Hfq for efficient target binding.

Promoter analysis

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.[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 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 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.[12]

Genomic context

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.[13] [14] [15] 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,[16] PFAM[17] or Smart,[18] and thus, are considered here as missannotations not registered in the genomic context graph.

Table 2: Detailed Genomic context information of the αr9 sRNA members.! Family !! Feature !! Name !! Strand !! Begin !! End !! Protein name !! Annotation !! Organism
class=cellinside αr9_Smr9Cclass=cellinside geneclass=cellinside SMc01933class=cellinside Rclass=cellinside 1397889class=cellinside 1398104class=cellinside NP_385391.1class=cellinside transmembrane proteinclass=cellinside Sinorhizobium meliloti 1021 (NC_003047)
class=cellinside αr9_Smr9Cclass=cellinside sRNAclass=cellinside Smr9Cclass=cellinside Rclass=cellinside 1398277class=cellinside 1398425class=cellinside class=cellinside class=cellinside Sinorhizobium meliloti 1021 (NC_003047)
class=cellinside αr9_Smr9Cclass=cellinside geneclass=cellinside SMc01934class=cellinside Dclass=cellinside 1398815class=cellinside 1400143class=cellinside NP_385392.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Sinorhizobium meliloti 1021 (NC_003047)
class=cellinside αr9_Rlt2304r9Cclass=cellinside geneclass=cellinside Rleg2_1278class=cellinside Dclass=cellinside 1296067class=cellinside 1296342class=cellinside YP_002280798.1class=cellinside transmembrane protein function DUF146class=cellinside Rhizobium leguminosarum bv trifolii WSM2304 chromosome (NC_011369)
class=cellinside αr9_Rlt2304r9Cclass=cellinside sRNAclass=cellinside Rlt2304r9Cclass=cellinside Rclass=cellinside 1296506class=cellinside 1296650class=cellinside class=cellinside class=cellinside Rhizobium leguminosarum bv trifolii WSM2304 chromosome (NC_011369)
class=cellinside αr9_Rlt2304r9Cclass=cellinside geneclass=cellinside Rleg2_1279class=cellinside Dclass=cellinside 1296935class=cellinside 1298257class=cellinside YP_002280799.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Rhizobium leguminosarum bv trifolii WSM2304 chromosome (NC_011369)
class=cellinside αr9_Rlt1325r9Cclass=cellinside geneclass=cellinside Rleg_1370class=cellinside Dclass=cellinside 1354155class=cellinside 1354430class=cellinside YP_002975201.1class=cellinside transmembrane proteinclass=cellinside Rhizobium leguminosarum bv trifolii WSM1325 (NC_012850)
class=cellinside αr9_Rlt1325r9Cclass=cellinside sRNAclass=cellinside Rlt1325r9Cclass=cellinside Rclass=cellinside 1354593class=cellinside 1354736class=cellinside class=cellinside class=cellinside Rhizobium leguminosarum bv trifolii WSM1325 (NC_012850)
class=cellinside αr9_Rlt1325r9Cclass=cellinside geneclass=cellinside Rleg_1371class=cellinside Dclass=cellinside 1355021class=cellinside 1356343class=cellinside YP_002975202.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Rhizobium leguminosarum bv trifolii WSM1325 (NC_012850)
class=cellinside αr9_ReCFNr9Cclass=cellinside geneclass=cellinside RHE_CH01622class=cellinside Dclass=cellinside 1702700class=cellinside 1703041class=cellinside YP_469148.1class=cellinside transmembrane proteinclass=cellinside Rhizobium etli CFN 42 (NC_007761)
class=cellinside αr9_ReCFNr9Cclass=cellinside sRNAclass=cellinside ReCFNr9Cclass=cellinside Rclass=cellinside 1703203class=cellinside 1703345class=cellinside class=cellinside class=cellinside Rhizobium etli CFN 42 (NC_007761)
class=cellinside αr9_ReCFNr9Cclass=cellinside geneclass=cellinside RHE_CH01623class=cellinside Dclass=cellinside 1703629class=cellinside 1704951class=cellinside YP_469149.2class=cellinside prolyl-tRNA sybthetaseclass=cellinside Rhizobium etli CFN 42 (NC_007761)
class=cellinside αr9_Smedr9Cclass=cellinside geneclass=cellinside Smed_0907class=cellinside Dclass=cellinside 979229class=cellinside 979498class=cellinside YP_001326597.1class=cellinside transmembrane proteinclass=cellinside Sinorhizobium medicae WSM419 chromosome (NC_009636)
class=cellinside αr9_Smedr9Cclass=cellinside sRNAclass=cellinside Smedr9Cclass=cellinside Rclass=cellinside 979747class=cellinside 979753class=cellinside class=cellinside class=cellinside Sinorhizobium medicae WSM419 chromosome (NC_009636)
class=cellinside αr9_Smedr9Cclass=cellinside geneclass=cellinside Smed_0908class=cellinside Dclass=cellinside 980177class=cellinside 981469class=cellinside YP_001326598.1class=cellinside FAD-dependent pyridine nucleotide-disulfide oxidoreductasclass=cellinside Sinorhizobium medicae WSM419 chromosome (NC_009636)
class=cellinside αr9_Rlvr9Cclass=cellinside geneclass=cellinside RL1718class=cellinside Dclass=cellinside 1802432class=cellinside 1802773class=cellinside YP_767322.1class=cellinside transmembrane proteinclass=cellinside Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
class=cellinside αr9_Rlvr9Cclass=cellinside sRNAclass=cellinside Rlvr9Cclass=cellinside Rclass=cellinside 1802936class=cellinside 1803079class=cellinside class=cellinside class=cellinside Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
class=cellinside αr9_Rlvr9Cclass=cellinside geneclass=cellinside RL1719class=cellinside Dclass=cellinside 1803364class=cellinside 1804686class=cellinside YP_767323.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
class=cellinside αr9_Atr9Cclass=cellinside geneclass=cellinside Atu1286class=cellinside Dclass=cellinside 1274803class=cellinside 1275072class=cellinside NP_354296.2class=cellinside transmembrane proteinclass=cellinside Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062)
class=cellinside αr9_Atr9Cclass=cellinside sRNAclass=cellinside Atr9Cclass=cellinside Rclass=cellinside 1275297class=cellinside 1275443class=cellinside class=cellinside class=cellinside Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062)
class=cellinside αr9_Atr9Cclass=cellinside geneclass=cellinside Atu1288class=cellinside Dclass=cellinside 1275738class=cellinside 1277060class=cellinside NP_354297.2class=cellinside prolyl-tRNA sybthetaseclass=cellinside Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062)
class=cellinside αr9_ReCIATr9Cclass=cellinside geneclass=cellinside RHECIAT_CH0001694class=cellinside Dclass=cellinside 1684473class=cellinside 1684766class=cellinside YP_001977846.1class=cellinside transmembrane proteinclass=cellinside Rhizobium etli CIAT 652 (NC_010994)
class=cellinside αr9_ReCIATr9Cclass=cellinside sRNAclass=cellinside ReCIATr9Cclass=cellinside Rclass=cellinside 1684929class=cellinside 1685072class=cellinside class=cellinside class=cellinside Rhizobium etli CIAT 652 (NC_010994)
class=cellinside αr9_ReCIATr9Cclass=cellinside geneclass=cellinside RHECIAT_CH0001695class=cellinside Dclass=cellinside 1685356class=cellinside 1686678class=cellinside YP_001977847.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Rhizobium etli CIAT 652 (NC_010994)
class=cellinside αr9_Arr9CIclass=cellinside geneclass=cellinside Arad_1869class=cellinside Dclass=cellinside 1481492class=cellinside 1481770class=cellinside YP_002544124.1class=cellinside transmembrane proteinclass=cellinside Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
class=cellinside αr9_Arr9CIclass=cellinside sRNAclass=cellinside Arr9CIclass=cellinside Rclass=cellinside 1481975class=cellinside 1482119class=cellinside class=cellinside class=cellinside Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
class=cellinside αr9_Arr9CIclass=cellinside geneclass=cellinside Arad_1870class=cellinside Dclass=cellinside 1482307class=cellinside 1483734class=cellinside YP_002544125.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
class=cellinside αr9_Sfr9Cclass=cellinside geneclass=cellinside NGR_c10670class=cellinside Dclass=cellinside 1129571class=cellinside 1129840class=cellinside YP_002825606.1class=cellinside transmembrane proteinclass=cellinside Sinorhizobium fredii NGR234 chromosome (NC_012587)
class=cellinside αr9_Sfr9Cclass=cellinside sRNAclass=cellinside Sfr9Cclass=cellinside Rclass=cellinside 1130001class=cellinside 1130150class=cellinside class=cellinside class=cellinside Sinorhizobium fredii NGR234 chromosome (NC_012587)
class=cellinside αr9_Sfr9Cclass=cellinside geneclass=cellinside NGR_c10680class=cellinside Dclass=cellinside 1130367class=cellinside 1131872class=cellinside YP_002825607.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Sinorhizobium fredii NGR234 chromosome (NC_012587)
class=cellinside αr9_AH13r9Cclass=cellinside geneclass=cellinside AGROH133_05703class=cellinside Dclass=cellinside 1215032class=cellinside 1215337class=cellinside YP_004278514.1class=cellinside transmembrane proteinclass=cellinside Agrobacterium sp. H13-3 chromosome (NC_015183)
class=cellinside αr9_AH13r9Cclass=cellinside sRNAclass=cellinside AH13r9Cclass=cellinside Rclass=cellinside 1215580class=cellinside 1215726class=cellinside class=cellinside class=cellinside Agrobacterium sp. H13-3 chromosome (NC_015183)
class=cellinside αr9_AH13r9Cclass=cellinside geneclass=cellinside AGROH133_05706class=cellinside Dclass=cellinside 1215911class=cellinside 1217344class=cellinside YP_004278515.1class=cellinside Prolyl-tRNA sybthetaseclass=cellinside Agrobacterium sp. H13-3 chromosome (NC_015183)
class=cellinside αr9_Avr9CIclass=cellinside geneclass=cellinside Avi_1737class=cellinside Dclass=cellinside 1448181class=cellinside 1448450class=cellinside YP_002549251.1class=cellinside transmembrane proteinclass=cellinside Agrobacterium vitis S4 chromosome 1 (NC_011989)
class=cellinside αr9_Avr9CIclass=cellinside sRNAclass=cellinside Avr9CIclass=cellinside Rclass=cellinside 1448510class=cellinside 1448659class=cellinside class=cellinside class=cellinside Agrobacterium vitis S4 chromosome 1 (NC_011989)
class=cellinside αr9_Avr9CIclass=cellinside geneclass=cellinside Avi_1739class=cellinside Dclass=cellinside 1448895class=cellinside 1450391class=cellinside YP_002549252.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Agrobacterium vitis S4 chromosome 1 (NC_011989)
class=cellinside αr9_Bor9CIclass=cellinside geneclass=cellinside BOV_0814class=cellinside Dclass=cellinside 822060class=cellinside 822329class=cellinside YP_001258797.1class=cellinside transmembrane proteinclass=cellinside Brucella ovis ATCC 25840 chromosome I (NC_009505)
class=cellinside αr9_Bor9CIclass=cellinside sRNAclass=cellinside Bor9CIclass=cellinside Rclass=cellinside 822712class=cellinside 822859class=cellinside class=cellinside class=cellinside Brucella ovis ATCC 25840 chromosome I (NC_009505)
class=cellinside αr9_Bor9CIclass=cellinside geneclass=cellinside BOV_0816class=cellinside Dclass=cellinside 823177class=cellinside 824505class=cellinside YP_001258799.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Brucella ovis ATCC 25840 chromosome I (NC_009505)
class=cellinside αr9_Bcr9CIclass=cellinside geneclass=cellinside BCAN_A0834class=cellinside Dclass=cellinside 795629class=cellinside 795898class=cellinside YP_001592670.1class=cellinside transmembrane proteinclass=cellinside Brucella canis ATCC 23365 chromosome I (NC_010103)
class=cellinside αr9_Bcr9CIclass=cellinside sRNAclass=cellinside Bcr9CIclass=cellinside Rclass=cellinside 796281class=cellinside 796428class=cellinside class=cellinside class=cellinside Brucella canis ATCC 23365 chromosome I (NC_010103)
class=cellinside αr9_Bcr9CIclass=cellinside geneclass=cellinside BCAN_A0837class=cellinside Dclass=cellinside 796746class=cellinside 798074class=cellinside YP_001592673.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Brucella canis ATCC 23365 chromosome I (NC_010103)
class=cellinside αr9_Bs23445r9CIclass=cellinside geneclass=cellinside BSUIS_A0858class=cellinside Dclass=cellinside 817110class=cellinside 817379class=cellinside YP_001627496.1class=cellinside transmembrane proteinclass=cellinside Brucella suis ATCC 23445 chromosome I (NC_010169)
class=cellinside αr9_Bs23445r9CIclass=cellinside sRNAclass=cellinside Bs23445r9CIclass=cellinside Rclass=cellinside 817762class=cellinside 817909class=cellinside class=cellinside class=cellinside Brucella suis ATCC 23445 chromosome I (NC_010169)
class=cellinside αr9_Bs23445r9CIclass=cellinside geneclass=cellinside BSUIS_A0861class=cellinside Dclass=cellinside 818227class=cellinside 819555class=cellinside YP_001627499.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Brucella suis ATCC 23445 chromosome I (NC_010169)
class=cellinside αr9_Bm16Mr9CIclass=cellinside geneclass=cellinside BMEI1140class=cellinside Rclass=cellinside 1185950class=cellinside 1187287class=cellinside NP_540057.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317)
class=cellinside αr9_Bm16Mr9CIclass=cellinside sRNAclass=cellinside Bm16Mr9CIclass=cellinside Dclass=cellinside 1187596class=cellinside 1187743class=cellinside class=cellinside class=cellinside Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317)
class=cellinside αr9_Bm16Mr9CIclass=cellinside geneclass=cellinside BMEI1141class=cellinside Rclass=cellinside 1188126class=cellinside 1188395class=cellinside NP_540058.1class=cellinside transmembrane proteinclass=cellinside Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317)
class=cellinside αr9_BaS19r9CIclass=cellinside geneclass=cellinside BAbS19_I07830class=cellinside Dclass=cellinside 817246class=cellinside 817515class=cellinside YP_001934781.1class=cellinside transmembrane proteinclass=cellinside Brucella abortus S19 chromosome 1 (NC_010742)
class=cellinside αr9_BaS19r9CIclass=cellinside sRNAclass=cellinside BaS19r9CIclass=cellinside Rclass=cellinside 817898class=cellinside 818045class=cellinside class=cellinside class=cellinside Brucella abortus S19 chromosome 1 (NC_010742)
class=cellinside αr9_BaS19r9CIclass=cellinside geneclass=cellinside BAbS19_I07840class=cellinside Dclass=cellinside 818363class=cellinside 819691class=cellinside YP_001934782.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Brucella abortus S19 chromosome 1 (NC_010742)
class=cellinside αr9_Bs1330r9CIclass=cellinside geneclass=cellinside BR0819class=cellinside Dclass=cellinside 797265class=cellinside 797534class=cellinside NP_697833.1class=cellinside transmembrane proteinclass=cellinside Brucella suis 1330 chromosome I (NC_004310)
class=cellinside αr9_Bs1330r9CIclass=cellinside sRNAclass=cellinside Bs1330r9CIclass=cellinside Rclass=cellinside 797917class=cellinside 798064class=cellinside class=cellinside class=cellinside Brucella suis 1330 chromosome I (NC_004310)
class=cellinside αr9_Bs1330r9CIclass=cellinside geneclass=cellinside BR0822class=cellinside Dclass=cellinside 798382class=cellinside 799710class=cellinside NP_697836.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Brucella suis 1330 chromosome I (NC_004310)
class=cellinside αr9_Ba19941r9CIclass=cellinside geneclass=cellinside BruAb1_0833class=cellinside Dclass=cellinside 818945class=cellinside 819214class=cellinside YP_221561.1class=cellinside transmembrane proteinclass=cellinside Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
class=cellinside αr9_Ba19941r9CIclass=cellinside sRNAclass=cellinside Ba19941r9CIclass=cellinside Rclass=cellinside 819597class=cellinside 819744class=cellinside class=cellinside class=cellinside Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
class=cellinside αr9_Ba19941r9CIclass=cellinside geneclass=cellinside BruAb1_0836class=cellinside Dclass=cellinside 820062class=cellinside 821390class=cellinside YP_221564.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
class=cellinside αr9_Bmar9CIclass=cellinside geneclass=cellinside BAB1_0839class=cellinside Dclass=cellinside 815223class=cellinside 815492class=cellinside YP_414270.1class=cellinside hypothetical membrane spanning proteinclass=cellinside Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
class=cellinside αr9_Bmar9CIclass=cellinside sRNAclass=cellinside Bmar9CIclass=cellinside Rclass=cellinside 815875class=cellinside 816022class=cellinside class=cellinside class=cellinside Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
class=cellinside αr9_Bmar9CIclass=cellinside geneclass=cellinside BAB1_0842class=cellinside Dclass=cellinside 816340class=cellinside 817668class=cellinside YP_414273.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
class=cellinside αr9_Bmir9CIclass=cellinside geneclass=cellinside BMI_I820class=cellinside Dclass=cellinside 801426class=cellinside 801695class=cellinside YP_003106759.1class=cellinside transmembrane proteinclass=cellinside Brucella microti CCM 4915 chromosome 1 (NC_013119)
class=cellinside αr9_Bmir9CIclass=cellinside sRNAclass=cellinside Bmir9CIclass=cellinside Rclass=cellinside 802078class=cellinside 802225class=cellinside class=cellinside class=cellinside Brucella microti CCM 4915 chromosome 1 (NC_013119)
class=cellinside αr9_Bmir9CIclass=cellinside geneclass=cellinside BMI_I822class=cellinside Dclass=cellinside 802543class=cellinside 803871class=cellinside YP_003106761.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Brucella microti CCM 4915 chromosome 1 (NC_013119)
class=cellinside αr9_Bm23457r9CIclass=cellinside geneclass=cellinside BMEA_A0861class=cellinside Dclass=cellinside 818725class=cellinside 818994class=cellinside YP_002732568.1class=cellinside transmembrane proteinclass=cellinside Brucella melitensis ATCC 23457 chromosome I (NC_012441)
class=cellinside αr9_Bm23457r9CIclass=cellinside sRNAclass=cellinside Bm23457r9CIclass=cellinside Rclass=cellinside 819377class=cellinside 819523class=cellinside class=cellinside class=cellinside Brucella melitensis ATCC 23457 chromosome I (NC_012441)
class=cellinside αr9_Bm23457r9CIclass=cellinside geneclass=cellinside BMEA_A0862class=cellinside Dclass=cellinside 819842class=cellinside 821170class=cellinside YP_002732569.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Brucella melitensis ATCC 23457 chromosome I (NC_012441)
class=cellinside αr9_Mlr9Cclass=cellinside geneclass=cellinside mll1344class=cellinside Rclass=cellinside 1125520class=cellinside 1126848class=cellinside NP_102953.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Mesorhizobium loti MAFF303099 chromosome (NC_002678)
class=cellinside αr9_Mlr9Cclass=cellinside sRNAclass=cellinside Mlr9Cclass=cellinside Dclass=cellinside 1127217class=cellinside 1127363class=cellinside class=cellinside class=cellinside Mesorhizobium loti MAFF303099 chromosome (NC_002678)
class=cellinside αr9_Mlr9Cclass=cellinside geneclass=cellinside msl1345class=cellinside Rclass=cellinside 1127503class=cellinside 1127787class=cellinside NP_102954.1class=cellinside hypothetical membrane spanning proteinclass=cellinside Mesorhizobium loti MAFF303099 chromosome (NC_002678)
class=cellinside αr9_Oar9CIclass=cellinside geneclass=cellinside Oant_2405class=cellinside Rclass=cellinside 2527462class=cellinside 2528790class=cellinside YP_001370948.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Brucella anthropi ATCC 49188 chromosome 1 (NC_009667)
class=cellinside αr9_Oar9CIclass=cellinside sRNAclass=cellinside Oar9CIclass=cellinside Dclass=cellinside 2529108class=cellinside 2529255class=cellinside class=cellinside class=cellinside Brucella anthropi ATCC 49188 chromosome 1 (NC_009667)
class=cellinside αr9_Oar9CIclass=cellinside geneclass=cellinside Oant_2406class=cellinside Rclass=cellinside 2529594class=cellinside 2529863class=cellinside YP_001370949.1class=cellinside transmembrane proteinclass=cellinside Brucella anthropi ATCC 49188 chromosome 1 (NC_009667)
class=cellinside αr9_Mcr9Cclass=cellinside geneclass=cellinside Mesci_3302class=cellinside Dclass=cellinside 3449215class=cellinside 3449499class=cellinside YP_004142475.1class=cellinside transmembrane proteinclass=cellinside Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
class=cellinside αr9_Mcr9Cclass=cellinside sRNAclass=cellinside Mcr9Cclass=cellinside Rclass=cellinside 3449639class=cellinside 3449786class=cellinside class=cellinside class=cellinside Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
class=cellinside αr9_Mcr9Cclass=cellinside geneclass=cellinside Mesci_3303class=cellinside Dclass=cellinside 3450133class=cellinside 3451461class=cellinside YP_004142476.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
class=cellinside αr9_MsBCNr9Cclass=cellinside geneclass=cellinside Meso_1039class=cellinside Dclass=cellinside 1141489class=cellinside 1141758class=cellinside YP_673601.1class=cellinside transmembrane proteinclass=cellinside Mesorhizobium sp. BNC1 (NC_008254)
class=cellinside αr9_MsBCNr9Cclass=cellinside sRNAclass=cellinside MsBCNr9Cclass=cellinside Rclass=cellinside 1141776class=cellinside 1141933class=cellinside class=cellinside class=cellinside Mesorhizobium sp. BNC1 (NC_008254)
class=cellinside αr9_MsBCNr9Cclass=cellinside geneclass=cellinside Meso_1040class=cellinside Dclass=cellinside 1142139class=cellinside 1143467class=cellinside YP_673602.1class=cellinside prolyl-tRNA sybthetaseclass=cellinside Mesorhizobium sp. BNC1 (NC_008254)

Notes and References

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  2. Vincent M Ulvé . Emeric W Sevin . Angélique Chéron. Frédérique Barloy-Hubler. amp . Identification of chromosomal alpha-proteobacterial small RNAs by comparative genome analysis and detection in Sinorhizobium meliloti strain 1021. BMC Genomics. 8. 467. 467 . 2007. 10.1186/1471-2164-8-467. 18093320. 2245857 . free .
  3. Claudio Valverde . Jonathan Livny . Jan-Philip Schlüter . Jan Reinkensmeier . Anke Becker. Gustavo Parisi. amp. rediction of Sinorhizobium meliloti sRNA genes and experimental detection in strain 2011 . BMC Genomics. 9. 406. 2009. 10.1186/1471-2164-9-416. 18793445 . 2573895 . 416 . free .
  4. Schlüter JP, Reinkensmeier J, Daschkey S, Evguenieva-Hackenberg E, Janssen S, Jänicke S, Becker JD, Giegerich R, Becker A . A genome-wide survey of sRNAs in the symbiotic nitrogen-fixing alpha-proteobacterium Sinorhizobium meliloti. BMC Genomics. 11. 245. 2010. 10.1186/1471-2164-11-436. 20637113. 436. 3091635 . free .
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  6. Will S, Reiche K, Hofacker IL, Stadler PF, Backofen R. Inferring Noncoding RNA Families and Classes by Means of Genome-Scale Structure-Based Clustering. PLOS Comput Biol. 4. 65. e65. 10.1371/journal.pcbi.0030065. 17432929. 1851984. 2007. 2007PLSCB...3...65W . free .
  7. Torres-Quesada O, Oruezabal RI, Peregrina A, Jofre E, Lloret J, Rivilla R, Toro N, Jiménez-Zurdo JI . The Sinorhizobium meliloti RNA chaperone Hfq influences central carbon metabolism and the symbiotic interaction with alfalfa . BMC Microbiol. 6. 2010.
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  10. Gama-Castro S, Salgado H, Peralta-Gil M, Santos-Zavaleta A, Muniz-Rascado L, Solano-Lira H, Jimenez-Jacinto V, Weiss V, Garcia-Sotelo JS, Lopez-Fuentes A, Porron-Sotelo L, Alquicira-Hernandez S, Medina-Rivera A, Martinez-Flores I, Alquicira-Hernandez K, Martinez-Adame R, Bonavides-Martinez C, Miranda-Rios J, Huerta AM, Mendoza-Vargas A, Collado-Torres L, Taboada B, Vega-Alvarado L, Olvera M, Olvera L, Grande R, Morett E, Collado-Vides J . 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. 10.1093/nar/gkq1110. 21051347. 3013702.
  11. Bailey TL, Elkan C . Proceedings. International Conference on Intelligent Systems for Molecular Biology . Fitting a mixture model by expectation maximization to discover motifs in biopolymers. 28–36. AAAI Press, Menlo Park, California. 1994. 2. 7584402.
  12. Goethals K, Van Montagu M, Holsters M . Conserved motifs in a divergent nod box of Azorhizobium caulinodans ORS571 reveal a common structure in promoters regulated by LysR-type proteins. Proc Natl Acad Sci U S A. 1992. 89. 5. 1646–1650. 10.1073/pnas.89.5.1646. 1542656. 48509. 1992PNAS...89.1646G. free.
  13. Vinayagam A, del Val C, Schubert F, Eils R, Glatting KH, Suhai S, König R . GOPET: a tool for automated predictions of Gene Ontology terms . BMC Bioinformatics . 7. 171 . 2006 . 16549020. 10.1186/1471-2105-7-161 . 1434778 . free .
  14. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M . Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005. 21. 18. 3674–3676. 16081474. 10.1093/bioinformatics/bti610. free.
  15. del Val C, Ernst P, Falkenhahn M, Fladerer C, Glatting KH, Suhai S, Hotz-Wagenblatt A . ProtSweep, 2Dsweep and DomainSweep: protein analysis suite at DKFZ. Nucleic Acids Res. 35. Web Server issue. W444–50. 17526514. 10.1093/nar/gkm364. 1933246. 2007.
  16. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D, Bork P, Das U, Daugherty L, Duquenne L, Finn RD, Gough J, Haft D, Hulo N, Kahn D, Kelly E, Laugraud A, Letunic I, Lonsdale D, Lopez R, Madera M, Maslen J, McAnulla C, McDowall J, Mistry J, Mitchell A, Mulder N, Natale D, Orengo C, Quinn AF, Selengut JD, Sigrist CJ, Thimma M, Thomas PD, Valentin F, Wilson D, Wu CH, Yeats C . InterPro: the integrative protein signature database. Nucleic Acids Res. 37. Database issue. D224–228. 2009. 10.1093/nar/gkn785. 18940856. 2686546.
  17. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A . The Pfam protein families database. Nucleic Acids Res. 38. Database issue. D211–222. 2010. 10.1093/nar/gkp985. 19920124. 2808889.
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