αr15 RNA

αr15 is a family of bacterial small non-coding RNAs with representatives in a broad group of α-proteobacteria from the order Rhizobiales. The first members of this family (smr15C1 and smrC15C2) were found tandemly arranged in the same intergenic region (IGR) of the Sinorhizobium meliloti 1021 chromosome (C).[1] Further homology and structure conservation analysis have identified full-length Smr15C1 and Smr15C2 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). The Smr15C1 (115 nt) and Smr15C2 (121 nt) homologs are also encoded in tandem within the same IGR region of Rhizobium and Agrobacterium species, whereas in Brucella species the αr15C loci are spread in the IGRs of Chromosome I. Moreover, this analysis also identified a third αr15 loci in extrachromosomal replicons of the mentioned nitrogen-fixing α-proteobacteria and in the Chromosome II of Brucella species. αr15 RNA species are 99-121 nt long (Table 1) and share a well defined common secondary structure consisting of three stem loops (Figure 1). The transcripts of the αr15 family can be catalogued as trans-acting sRNAs encoded by independent transcription units with recognizable promoter and transcription termination signatures within intergenic regions (IGRs) of the α-proteobacterial genomes (Figure 5).

Discovery and structure

Smr15C1 y Smr15C2 sRNAs were 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). Although the primary nucleotide sequence of Smr15C1 y Smr15C2 showed high similarity (84% identity), specific probes for each sRNA could be designed which detected transcripts of different size and expression profiles.[1]

TAP-based 5’-RACE experiments mapped the Smr15C1 and Smr15C2 transcription start sites (TSS) in the S. meliloti 1021 genome (http://iant.toulouse.inra.fr/bacteria/annotation/cgi/rhime.cgi). The Smr15C1 TSS was mapped to the chromosomal position 1698731 nt and the TSS of Smr15C2 to the nt 1698937. The 3’-ends were assumed to be located at the 1698617 nt and 1698817 nt respectively, matching the last residue of the consecutive Us stretch of a bona fide Rho-independent terminator (Figure 5). Parallel and later studies,[2][3] in which Smr15C1 and Smr15C2 transcripts are referred to as two copies of sra41 or Sm3/Sm3', independently confirmed the expression of these sRNAs 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 2011 also revealed the expression of Smr15C1 and Smr15C2, here referred to as SmelC411 and SmelC412 respectively, mapping the 5’- and 3´-ends of the full-length transcripts to essentially the same positions as del Val et al. in the S. meliloti 1021 chromosome. However, this study identified an additional TSS for Smr15C2 at position 1698948.[4]

The nucleotide sequences of Smr15C1 and Smr15C2 were initially used as query to search against the Rfam database (version 10.0; http://rfam.xfam.org). This search revealed partial homology of both transcripts, restricted to the second hairpin and the Rho-independent terminator, to the RF00519 family of RNAs known as suhB (http://rfam.xfam.org/family/RF00519). However, no structural homologs of the full-length sRNAs were found in this database.

Both S.melilloti αr15 sRNAs were also 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 αr15 family in the existing bacterial genomic databases.

Figure 2: Covariance Model in stockholm format showing the consensus structure for the αr15 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.
Table 1: Smr15C1 and Smr15C2 homologs in other symbionts and pathogens
CM modelNameGI accession numberbeginendstrand%GClengthOrganism
αr15 Smr15C1 gi|15963753|ref|NC_003047.1| 1698617 1698731 - 54 115 Sinorhizobium meliloti 1021
αr15 Smr15C2 gi|15963753|ref|NC_003047.1| 1698817 1698937 - 50 121 Sinorhizobium meliloti 1021
αr15 Smr15A gi|16262453|ref|NC_003037.1| 552873 552984 + 51 112 Sinorhizobium meliloti 1021 plasmid pSymA
αr15 Smedr15C1 gi|150395228|ref|NC_009636.1| 1337011 1337126 - 53 116 Sinorhizobium medicae WSM419 chromosome
αr15 Smedr15C2 gi|150395228|ref|NC_009636.1| 1337212 1337331 - 50 120 Sinorhizobium medicae WSM419 chromosome
αr15 Smedr15p03 gi|150378263|ref|NC_009622.1| 40054 40165 - 52 112 Sinorhizobium medicae WSM419 plasmid pSMED03
αr15 Sfr15C1 gi|227820587|ref|NC_012587.1| 1612511 1612626 - 59 116 Sinorhizobium fredii NGR234 chromosome
αr15 Sfr15C2 gi|227820587|ref|NC_012587.1| 1612711 1612830 - 51 120 Sinorhizobium fredii NGR234 chromosome
αr15 Sfr15b gi|227818258|ref|NC_012586.1| 134078 134190 - 55 113 Sinorhizobium fredii NGR234 plasmid pNGR234b
αr15 Atr15C1 gi|159184118|ref|NC_003062.2| 2163254 2163370 + 53 117 Agrobacterium tumefaciens str. C58 chromosome circular
αr15 Atr15C2 gi|159184118|ref|NC_003062.2| 2163454 2163554 + 57 101 Agrobacterium tumefaciens str. C58 chromosome circular
αr15 AH13r15C1 gi|325291453|ref|NC_015183.1| 2112823 2112939 + 52 117 Agrobacterium sp. H13-3 chromosome
αr15 AH13r15C2 gi|325291453|ref|NC_015183.1| 2113023 2113121 + 54 99 Agrobacterium sp. H13-3 chromosome
αr15 AH13r15a gi|325168279|ref|NC_015184.1| 211698 211807 - 53 110 Agrobacterium sp. H13-3 plasmid pAspH13-3a
αr15 ReCIATr15C1 gi|190889639|ref|NC_010994.1| 3155217 3155332 + 51 116 Rhizobium etli CIAT 652
αr15 ReCIATr15C2 gi|190889639|ref|NC_010994.1| 3155440 3155555 + 48 116 Rhizobium etli CIAT 652
αr15 ReCIATr15pC gi|190894340|ref|NC_010997.1| 941345 941452 + 53 108 Rhizobium etli CIAT 652 plasmid pC
αr15 ReCIATr15B gi|190893983|ref|NC_010996.1| 187927 188041 - 50 115 Rhizobium etli CIAT 652 plasmid pB
αr15 Arr15CI1 gi|222084201|ref|NC_011985.1| 2506215 2506331 + 52 117 Agrobacterium radiobacter K84 chromosome 1
αr15 Arr15CI2 gi|222084201|ref|NC_011985.1| 2506418 2506534 + 54 117 Agrobacterium radiobacter K84 chromosome 1
αr15 Arr15CII gi|222080781|ref|NC_011983.1| 1011511 1011624 - 57 114 Agrobacterium radiobacter K84 chromosome 2
αr15 Rlt2304r15C1 gi|209547612|ref|NC_011369.1| 2770612 2770727 + 50 116 Rhizobium leguminosarum bv. trifolii WSM2304 chromosome
αr15 Rlt2304r15C2 gi|209547612|ref|NC_011369.1| 2770835 2770949 + 50 115 Rhizobium leguminosarum bv. trifolii WSM2304 chromosome
αr15 Avr15CI1 gi|222147015|ref|NC_011989.1| 2608532 2608647 + 54 116 Agrobacterium vitis S4 chromosome 1
αr15 Avr15CI2 gi|222147015|ref|NC_011989.1| 2608739 2608839 + 46 101 Agrobacterium vitis S4 chromosome 1
αr15 Avr15Atc gi|222083145|ref|NC_011984.1| 122624 122736 - 50 113 Agrobacterium vitis S4 plasmid pAtS4c
αr15 Avr15Ate gi|222102412|ref|NC_011981.1| 198928 199039 + 51 112 Agrobacterium vitis S4 plasmid pAtS4e
αr15 Avr15Ti gi|222080117|ref|NC_011982.1| 52286 52397 - 57 112 Agrobacterium vitis S4 plasmid pTiS4
αr15 Rlvr15C1 gi|116249766|ref|NC_008380.1| 3605490 3605605 + 51 116 Rhizobium leguminosarum bv. viciae 3841
αr15 Rlvr15C2 gi|116249766|ref|NC_008380.1| 3605714 3605829 + 48 116 Rhizobium leguminosarum bv. viciae 3841
αr15 Rlvr15p10 gi|116254467|ref|NC_008381.1| 138799 138912 + 56 114 Rhizobium leguminosarum bv. viciae 3841 plasmid pRL10
αr15 Rlvr15p11 gi|116255200|ref|NC_008384.1| 567053 567166 - 53 114 Rhizobium leguminosarum bv. viciae 3841 plasmid pRL11
αr15 Rlt1325r15C1 gi|241202755|ref|NC_012850.1| 2981275 2981390 + 50 116 Rhizobium leguminosarum bv. trifolii WSM1325
αr15 Rlt1325r15C2 gi|241202755|ref|NC_012850.1| 2981499 2981613 + 50 115 Rhizobium leguminosarum bv. trifolii WSM1325
αr15 Rlt1325r15p02 gi|241666492|ref|NC_012858.1| 36176 36289 + 51 114 Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132502
αr15 ReCFNr15C1 gi|86355669|ref|NC_007761.1| 3117667 3117782 + 50 116 Rhizobium etli CFN 42
αr15 ReCFNr15C2 gi|86355669|ref|NC_007761.1| 3117890 3118004 + 50 115 Rhizobium etli CFN 42
αr15 ReCFNr15d gi|89255298|ref|NC_004041.2| 172760 172874 - 50 115 Rhizobium etli CFN 42 symbiotic plasmid p42d
αr15 ReCFNr15a gi|86359705|ref|NC_007762.1| 157296 157409 + 56 114 Rhizobium etli CFN 42 plasmid p42a
αr15 Mlr15a gi|13488050|ref|NC_002679.1| 65044 65154 - 51 111 Mesorhizobium loti MAFF303099 plasmid pMLa
αr15 Bcr15CII gi|161620094|ref|NC_010104.1| 707465 707572 + 56 108 Brucella canis ATCC 23365 chromosome II
αr15 Bcr15CI1 gi|161617991|ref|NC_010103.1| 1379297 1379398 - 51 102 Brucella canis ATCC 23365 chromosome I
αr15 Bcr15CI2 gi|161617991|ref|NC_010103.1| 1451969 1452087 - 50 119 Brucella canis ATCC 23365 chromosome I
αr15 Bs23445r15CI1 gi|163842277|ref|NC_010169.1| 1401085 1401186 - 51 102 Brucella suis ATCC 23445 chromosome I
αr15 Bs23445r15CI2 gi|163842277|ref|NC_010169.1| 1473791 1473909 - 50 119 Brucella suis ATCC 23445 chromosome I
αr15 Bs23445r15CII gi|163844199|ref|NC_010167.1| 696081 696188 + 56 108 Brucella suis ATCC 23445 chromosome II
αr15 Bm16Mr15CI gi|17986284|ref|NC_003317.1| 607684 607785 + 51 102 Brucella melitensis bv. 1 str. 16M chromosome I
αr15 Bm16Mr15CII gi|17988344|ref|NC_003318.1| 589501 589608 - 56 108 Brucella melitensis bv. 1 str. 16M chromosome II
αr15 BaS19r15CII gi|189022234|ref|NC_010740.1| 508055 508162 - 56 108 Brucella abortus S19 chromosome 2
αr15 BaS19r15CI1 gi|189023268|ref|NC_010742.1| 1396794 1396895 - 51 102 Brucella abortus S19 chromosome 1
αr15 BaS19r15CI2 gi|189023268|ref|NC_010742.1| 1469407 1469525 - 50 119 Brucella abortus S19 chromosome 1
αr15 Bm23457r15CII gi|225685871|ref|NC_012442.1| 687290 687397 + 56 108 Brucella melitensis ATCC 23457 chromosome II
αr15 Bm23457r15CI gi|225851546|ref|NC_012441.1| 1400641 1400742 - 51 102 Brucella melitensis ATCC 23457 chromosome I
αr15 Bs1330r15CII gi|56968493|ref|NC_004311.2| 708185 708292 + 56 108 Brucella suis 1330 chromosome II
αr15 Bs1330r15CI1 gi|56968325|ref|NC_004310.3| 1380381 1380482 - 51 102 Brucella suis 1330 chromosome I
αr15 Bs1330r15CI2 gi|56968325|ref|NC_004310.3| 1453011 1453129 - 50 119 Brucella suis 1330 chromosome I
αr15 Ba19941r15CI1 gi|62288991|ref|NC_006932.1| 1398464 1398565 - 51 102 Brucella abortus bv. 1 str. 9-941 chromosome I
αr15 Ba19941r15CI2 gi|62288991|ref|NC_006932.1| 1471073 1471191 - 50 119 Brucella abortus bv. 1 str. 9-941 chromosome I
αr15 Ba19941r15CII gi|62316961|ref|NC_006933.1| 508851 508958 - 56 108 Brucella abortus bv. 1 str. 9-941 chromosome II
αr15 Bmar15CII gi|83268957|ref|NC_007624.1| 508839 508946 - 56 108 Brucella melitensis biovar Abortus 2308 chromosome II
αr15 Bmar15CI1 gi|82698932|ref|NC_007618.1| 1395614 1395715 - 51 102 Brucella melitensis biovar Abortus 2308 chromosome I
αr15 Bmar15CI2 gi|82698932|ref|NC_007618.1| 1468227 1468345 - 50 119 Brucella melitensis biovar Abortus 2308 chromosome I
αr15 Bor15CI1 gi|148558820|ref|NC_009505.1| 1387928 1388029 - 50 102 Brucella ovis ATCC 25840 chromosome I
αr15 Bor15CI2 gi|148558820|ref|NC_009505.1| 1460506 1460624 - 50 119 Brucella ovis ATCC 25840 chromosome I
αr15 Bor15CII gi|148557829|ref|NC_009504.1| 709415 709524 + 54 110 Brucella ovis ATCC 25840 chromosome II
αr15 Bmir15CII gi|256014795|ref|NC_013118.1| 709102 709209 + 56 108 Brucella microti CCM 4915 chromosome 2
αr15 Bmir15CI1 gi|256368465|ref|NC_013119.1| 1387776 1387877 - 51 102 Brucella microti CCM 4915 chromosome 1
αr15 Bmir15CI2 gi|256368465|ref|NC_013119.1| 1461298 1461416 - 50 119 Brucella microti CCM 4915 chromosome 1
αr15 Oar15CI gi|153007346|ref|NC_009667.1| 1751482 1751598 + 49 117 Ochrobactrum anthropi ATCC 49188 chromosome 1
αr15 Oar15CII gi|153010078|ref|NC_009668.1| 1270083 1270191 + 56 109 Ochrobactrum anthropi ATCC 49188 chromosome 2
αr15 Oar15p02 gi|153011934|ref|NC_009670.1| 22208 22320 + 54 113 Ochrobactrum anthropi ATCC 49188 plasmid pOANT02

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] comparing the obtained predictions. The manual inspection of the sequences found with the CM using Infernal allowed finding 38 true homologues in phylogenetically related α-proteobacterial genomes. The 26 closest αr15 family members were found as tandem in the same chromosomal IGRs for the following species besides S. melilloti:

  • Sinorhizobium species: S. medicae and S. fredii
  • Rhizobium species: 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
  • Agrobacterium species: A. vitis,A. tumefaciens, A. radiobacter and A. H13

All these sequences showed significant bit scores and Infernal E-values (1.71e-28 - 2.03e-20). However, the plasmidic copies of all mentioned α-proteobacterial genomes and those αr15 members encoded by Brucella species (B. ovis, B. canis, B. abortus, B. microtis, and several biovars of B. melitensis), Ochrobactrum anthropi and Mesorhizobium lotishowed high E-values between (1e-19 and 8e-03) but very low bit-scores.

Figure 1: Consensus secondary structure of Smr15C1, Smr15C2 and the αr15 family predicted by RNA[7] and RNAalifold.[8] Smr15C1 and Smr15C2 are colored with a base probability scheme. The coloring of the αr15 family structure follows a base pairs conservation scheme: Red: base pair occurring in all sequences used to generate the consensus; yellow: two types of base pairing occur; Green: three types of base pairing occur. The shading of base pairs represents: Saturated, no inconsistent sequences; Pale, one inconsistent sequence; Very pale, two inconsistent sequences.
Figure 3: Phylogenetic distribution of known and predicted αr9 genes. Gene numbers are based on computational analysis using the program Infernal. Legend: Smr15C1 = Sinorhizobium meliloti 1021 (NC_003047), Smr15C2 = Sinorhizobium meliloti 1021 (NC_003047), Smr15A = Sinorhizobium meliloti 1021 plasmid pSymA (NC_003037), Smedr15C1 = Sinorhizobium medicae WSM419 chromosome (NC_009636), Smedr15C2 = Sinorhizobium medicae WSM419chromosome (NC_009636), Smedr15p03 = Sinorhizobium medicae WSM419 plasmid pSMED03 (NC_009622), Sfr15C1 = Sinorhizobium fredii NGR234 chromosome (NC_012587), Sfr15C2 = Sinorhizobium fredii NGR234 chromosome (NC_012587), Sfr15b = Sinorhizobium fredii NGR234 plasmid pNGR234b (NC_012586), Atr15C2 = Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062), Atr15C1 = Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062), AH13r15C2 = Agrobacterium sp. H13-3 chromosome (NC_015183), AH13r15C1 = Agrobacterium sp. H13-3 chromosome (NC_015183), AH13r15a = Agrobacterium sp. H13-3 plasmid pAspH13-3a (NC_015184), ReCIATr15C2 = Rhizobium etli CIAT 652 (NC_010994), ReCIATr15C1 = Rhizobium etli CIAT 652 (NC_010994), ReCIATr15pC = Rhizobium etli CIAT 652 plasmid pC (NC_010997), ReCIATr15B = Rhizobium etli CIAT 652 plasmid pB (NC_010996), Arr15CI2 = Agrobacterium radiobacter K84 chromosome 1 (NC_011985), Arr15CI1 = Agrobacterium radiobacter K84 chromosome 1 (NC_011985), Arr15CII = Agrobacterium radiobacter K84 chromosome 2 (NC_011983), Rlt2304r15C2 = Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369), Rlt2304r15C1 = Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369), Avr15C2 = Agrobacterium vitis S4 chromosome 1 (NC_011989), Avr15C1 = Agrobacterium vitis S4 chromosome 2 (NC_011989), Avr15pAtc = Agrobacterium vitis S4 plasmid pAtS4c (NC_011984), Avr15Ate = Agrobacterium vitis S4 plasmid pAtS4e (NC_011981), Avr15Ti = Agrobacterium vitis S4 plasmid pTiS4 (NC_011982), Rlvr15C2 = Rhizobium leguminosarum bv. viciae 3841 (NC_008380), Rlvr15C1 = Rhizobium leguminosarum bv. viciae 3841 (NC_008380), Rlvr15p10 = Rhizobium leguminosarum bv. viciae 3841 plasmid pRL10 (NC_008381), Rlvr15p11 = Rhizobium leguminosarum bv. viciae 3841 plasmid pRL11 (NC_008384), Rlt1325r15C2 = Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850), Rlt1325r15C1 = Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850), Rlt1325r15p02 = Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132502 (NC_012858), ReCFNr15C2 = Rhizobium etli CFN 42 (NC_007761), ReCFNr15C1 = Rhizobium etli CFN 42 (NC_007761), ReCFNr15d = Rhizobium etli CFN 42 symbiotic plasmid p42d (NC_004041), ReCFNr15a = Rhizobium etli CFN 42 plasmid p42a (NC_007762), Mlr15a = Mesorhizobium loti MAFF303099 plasmid pMLa (NC_002679), Bcr15CII = Brucella canis ATCC 23365 chromosome II (NC_010104), Bcr15CI2 = Brucella canis ATCC 23365 chromosome I (NC_010103), Bcr15CI1 = Brucella canis ATCC 23365 chromosome I (NC_010103), Bs23445r15CI2 = Brucella suis ATCC 23445 chromosome I (NC_010169), Bs23445r15CI1 = Brucella suis ATCC 23445 chromosome I (NC_010169), Bs23445r15CII = Brucella suis ATCC 23445 chromosome II (NC_010167), Bm16MCI = Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317), Bm16Mr15CII = Brucella melitensis bv. 1 str. 16M chromosome II (NC_003318), BaS19r15CII = Brucella abortus S19 chromosome 2 (NC_010740), BaS19r15CI2 = Brucella abortus S19 chromosome 1 (NC_010742), BaS19r15CI1 = Brucella abortus S19 chromosome 1 (NC_010742), Bm23457r15CII = Brucella melitensis ATCC 23457 chromosome II (NC_012442), Bm23457r15CI = Brucella melitensis ATCC 23457 chromosome I (NC_012441), Bs1330r15CII = Brucella suis 1330 chromosome II (NC_004311), Bs1330r15CI2 = Brucella suis 1330 chromosome I (NC_004310), Bs1330r15CI1 = Brucella suis 1330 chromosomeI (NC_004310), Ba19941r15CI2 = Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932), Ba19941r15CI1 = Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932), Ba19941r15CII = Brucella abortus bv. 1 str. 9-941 chromosome II (NC_006933), Bmar15CII = Brucella melitensis biovar Abortus 2308 chromosome II (NC_007624), Bmar15CI2 = Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618), Bmar15CI1 = Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618), Bor15CI2 = Brucella ovis ATCC 25840 chromosome I (NC_009505), Bor15CI1 = Brucella ovis ATCC 25840 chromosome I (NC_009505), Bor15CII = Brucella ovis ATCC 25840 chromosome II (NC_009504), Bmir15CII = Brucella microti CCM 4915 chromosome 2 (NC_013118), Bmr15CI2 = Brucella microti CCM 4915 chromosome 1 (NC_013119), Bmir15CI1 = Brucella microti CCM 4915 chromosome 1 (NC_013119), Oar15CI = Ochrobactrum anthropi ATCC 49188 chromosome 1 (NC_009667), Oar15CII = Ochrobactrum anthropi ATCC 49188 chromosome 2 (NC_009668).

Expression and functional information

Several studies have assessed Smr15C1 and Smr15C2 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] high salt stress, oxidative stress and cold and hot shock stresses.[3] The results showed different expression profiles for both sRNAs,[1] which is consistent with their organization in independent and differentially regulated transcription units within the same IGR (Figure 4 and Figure 5).

The expression of Smr15C1 and Smr15C2 in free-living bacteria was found to be growth-dependent but in an opposite manner. While Smr15C1 is accumulated in the stationary phase Smr15C2 is The expression of Smr15C1 and Smr15C2 in free-living bacteria was found to be growth-dependent but in an opposite manner. While Smr15C1 is accumulated in the stationary phase, Smr15C2 is preferentially expressed in log bacterial cultures.[1] Additionally, Schlüter et al.[4] recently described the up-regulation of Smr15C2 under cold shock stress, while no effects of a temperature downshift were observed in the expression of Smr15C1. The growth-dependent opposite expression profiles of Smr15C1 and Smr15C2, have not been observed in their Agrobacterium tumefaciens counterparts referred to as AbcR1 and AbcR2, respectively, by Wilms et al. (Atr15C1 and Atr15C2 in this work). AbcR1 and AbcR2 are induced simultaneously and both accumulate in stationary phase.[9] This behavior agrees with the fact that AbcR1 and AbcR2 have identical promoter-like sequences, being these very similar to the one of Smr15C2, but not to the promoter sequence of Smr15C1 (see Promoter Analysis). Furthermore, a first approach to the function of the AbcR genes revealed that these sRNAs silence the GABA uptake system through the down-regulation of the corresponding ABC transporter genes in an Hfq-dependent manner.[9] GABA is one of the plants signals recognized by rhizobacteria in some plant-bacteria interactions. Thus, these results, point to the shutting off synthesis of the GABA uptake system as a way used by A. tumefaciens to subvert the plant defense mechanism.

Recent co-inmunoprecipitation experiment[10] showed that both, Smr15C1 and Smr15C2, do bind the S. meliloti RNA chaperone Hfq, supporting also a role for these transcripts in this bacterium as trans-acting antisense riboregulators.They were also shown to fine-tune nutrient uptake.[11]

Promoter analysis

All αr15 loci have recognizable σ70-dependent promoters showing a -35/-10 consensus motif CTTGAC-n17-CTATAT, which has been previously shown to be widely conserved among several other genera in the α-subgroup of proteobacteria.[12] A multiple sequence alignment of these promoter regions revealed a conserved sequence stretch extending up to 80 bp upstream of the transcription start site in all the αr15 loci with the only exceptions of the S. meliloti, S.fredii and S. medicae αr15C1 promoters.

To identify binding sites for other known transcription factors we used the fasta sequences provided by RegPredict[13](http://regpredict.lbl.gov/regpredict/help.html), and used those position weight matrices (PSWM) provided by RegulonDB[14] (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 established, (see "Thresholded consensus" in http://gps-tools2.its.yale.edu). Moreover, we searched for conserved unknown motifs using MEME[15] (http://meme.sdsc.edu/meme4_6_1/intro.html) and used relaxed regular expressions (i.e. pattern matching) over all αr15 homologs promoters.

These studies revealed a difference in regulation between S. melilloti, S.fredii and S. medicae αr15C1 sRNAs and the rest of the αr15 family members independently of their group of origin (Rhizobium or Agrobacterium ) and genomic location (αr15C1, αr15C2, αr15plasmid) (Figure 4).

The rest of the family members presented a very well conserved 30 bp long region between positions -36 and -75. This conserved region, was used to query databases of known transcription factor motifs with TomTom,[16] the best matching motif was SMb20667_Rhizobiales, motif belonging to RegTransBase (http://regtransbase.lbl.gov/cgi-bin/regtransbase?page=main). The Smb20667 correspond to the binding site for a dicarboxylate metabolism regulator in Rhizobiales that belongs to the LacI family. This motif was identified clustering genes of tartrate dehydrogenase, succinate semialdehyde dehydrogenase, 3-hydroxyisobutyrate dehydrogenase and hydroxypyruvate isomerase in S. meliloti, and several Rhizobiums and it is marked in the promoter alignment figure (Figure 5) with an orange box. Moreover, another conserved sequence was found using MEME in the promoter region of the Sinorhizobium species αr15C1. This conserved region was used to query databases of known transcription factor motifs with TomTom, and the best matching motif was SMb20537_Rhizobiales (Figure 5 in red), that identifies the binding site for a sugar utilization regulator in Rhizobiales from the LacI family as well.

Figure 5: Graphic representation of the 15C seed members' promoter region. All members presented putative σ70 promoters with -30 and -10 boxes marked in green and red respectively. Conserved motifs are marked with orange and red color boxes.

Genomic context

Most of the αr15 family members are trans-encoded sRNAs transcribed from independent promoters in chromosomal IGRs. Many of the αr15 members neighboring genes were not annotated, and thus they were further manually curated.[17][18][19] As a result, we could classify the members of the family in four subgroups according to their genomic context. In the first group are the tandem αr15C1 and αr15C2 loci of the Rhizobium, Sinorhizobium and Agrobacterium species. They exhibited a great degree of conservation in the up and downstream genes, which have been predicted to code for a LysR transcriptional regulator and an AsR transcriptional regulator protein respectively (Figure 5). The only exception in this group was found for S. fredii that presented a very different genomic context. The second group includes the αr15CI1 loci in the Brucella species (additional file 2), which presented a very well conserved genomic context (Aspartate amino transferase and LysR/unknown transcriptional regulator) with partial synteny to the first group. A very different genomic context, not even partially conserved in most cases, was present in all plasmid-borne αr15 loci (additional file 1), which integrates the defined group three, where the flanking genes corresponded to ABC transporter proteins, excisonase or transposase among others. The αr15CI2 loci in the Brucella species (additional file 3) conform the group four and presented an up and downstream conserved genomic context, coding all regions for UDP-3-O-hydroxymyristoyl N-acetylglucosamine deacetylase and GTPAse cell division protein FtsZ. To the last group correspond the αr15CII loci in the Brucella group (additional file 4) where only one of the genes could be annotated always as a glycine deshidrogenase, the other sRNA flanking position was mostly coped by a hypothethical protein conserved in the Brucella group to which no domain, motif or GO functional annotation could be assigned.

Figure 4: Genomic context scheme of Smr15 and its closest homologues in other organisms. The αr15 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 αr15 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: Legend: αr15_Smr15C = Sinorhizobium meliloti 1021 (NC_003047), αr15_Smedr15C = Sinorhizobium medicae WSM419 chromosome (NC_009636), αr15_Sfr15C = Sinorhizobium fredii NGR234 chromosome (NC_012587), αr15_Atr15C = Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062), αr15_AH13r15C = Agrobacterium sp. H13-3 chromosome (NC_015183), αr15_ReCIATr15C = Rhizobium etli CIAT 652 (NC_010994), αr15_Arr15CI = Agrobacterium radiobacter K84 chromosome 1 (NC_011985), αr15_Rlt2304r15C = Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369), αr15_Avr15C = Agrobacterium vitis S4 chromosome 1 (NC_011989), αr15_Rlvr15C = Rhizobium leguminosarum bv. viciae 3841 (NC_008380), αr15_Rlt1325r15C = Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850), αr15_ReCFNr15C = Rhizobium etli CFN 42 (NC_007761).

Additional Files:

  • Genomic context graph of the αr15 family plasmid copies Image:Smbr15 1.png
  • Genomic context graph of the αr15CI1 loci in the Brucella group Image:Smbr15 2.png
  • Genomic context graph of the αr15CI2 loci in the Brucella group Image:Smbr15 3.png
  • Genomic context graph of the αr15CII loci in the Brucella group Image:Smbr15 4.png
Table 2: Detailed Genomic context information of the αr15 sRNA seed members.
FamilyFeature typeFeature nameStrandBeginEndProtein nameAnnotationOrganism
αr15_Smr15C gene SMc01226 R 1698201 1698491 NP_385671.1 transcription regulator protein Sinorhizobium meliloti 1021 (NC_003047)
αr15_Smr15C sRNA Smr15C1 R 1698617 1698731 - sRNA Sinorhizobium meliloti 1021 (NC_003047)
αr15_Smr15C sRNA Smr15C2 R 1698817 1698937 - sRNA Sinorhizobium meliloti 1021 (NC_003047)
αr15_Smr15C gene SMc01225 R 1699144 1700052 NP_385672.1 transcription regulator protein Sinorhizobium meliloti 1021 (NC_003047)
αr15_Smed15C gene Smed_1246 R 1336608 1336898 YP_001326931.1 ArsR family transcriptional regulator Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr15_Smed15C sRNA Smedr15C1 R 1337011 1337126 - sRNA Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr15_Smed15C sRNA Smedr15C2 R 1337212 1337331 - sRNA Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr15_Smed15C gene Smed_1247 R 1337537 1338433 YP_001326932.1 LysR family transcriptional regulator Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr15_Rlt2304r15C gene Rleg2_2722 D 2769491 2770402 YP_002282219.1 LysR family transcriptional regulator Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369)
αr15_Rlt2304r15C sRNA Rlt2304r15C1 D 2770612 2770727 - sRNA Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369)
αr15_Rlt2304r15C sRNA Rlt2304r15C2 D 2770835 2770949 - sRNA Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369)
αr15_Rlt2304r15C gene Rleg2_2723 D 2771064 2771357 YP_002282220.1 ArsR family transcriptional regulator Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369)
αr15_Rlt1325r15C gene Rleg_2983 D 2980263 2981174 YP_002976781.1 LysR family transcriptional regulator Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr15_Rlt1325r15C sRNA Rlt1325r15C1 D 2981275 2981390 - sRNA Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr15_Rlt1325r15C sRNA Rlt1325r15C2 D 2981499 2981613 - sRNA Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr15_Rlt1325r15C gene Rleg_2984 D 2981728 2982021 YP_002976782.1 ArsR family transcriptional regulator Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr15_ReCFNr15C gene RHE_CH02976 D 3116670 3117566 YP_470470.1 LysR family transcriptional regulator Rhizobium etli CFN 42 (NC_007761)
αr15_ReCFNr15C sRNA ReCFNr15C1 D 3117667 3117782 - sRNA Rhizobium etli CFN 42 (NC_007761)
αr15_ReCFNr15C sRNA ReCFNr15C2 D 3117890 3118004 - sRNA Rhizobium etli CFN 42 (NC_007761)
αr15_ReCFNr15C gene RHE_CH02977 D 3118119 3118412 YP_470471.1 ArsR family transcriptional regulator Rhizobium etli CFN 42 (NC_007761)
αr15_ReCIATr15C gene RHECIAT_CH0003143 D 3154220 3155116 YP_001979269.1 LysR family transcriptional regulator Rhizobium etli CIAT 652 (NC_010994)
αr15_ReCIATr15C sRNA ReCIATr15C1 D 3155217 3155332 - sRNA Rhizobium etli CIAT 652 (NC_010994)
αr15_ReCIATr15C sRNA ReCIATr15C2 D 3155440 3155555 - sRNA Rhizobium etli CIAT 652 (NC_010994)
αr15_ReCIATr15C gene RHECIAT_CH0003144 D 3155652 3155963 YP_001979270.1 ArsR family transcriptional regulator Rhizobium etli CIAT 652 (NC_010994)
αr15_Rlvr15C gene RL3429 D 3604478 3605389 YP_769009.1 LysR family transcriptional regulator Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr15_Rlvr15C sRNA Rlvr15C1 D 3605490 3605605 - sRNA Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr15_Rlvr15C sRNA Rlvr15C2 D 3605714 3605829 - sRNA Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr15_Rlvr15C gene RL3430 D 3605944 3606237 YP_769010.1 ArsR family transcriptional regulator Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr15_Sfr15C gene NGR_c15610 R 1611431 1612354 YP_002826082.1 lytic transglycosylase catalytic Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr15_Sfr15C sRNA Sfr15C1 R 1612511 1612626 - sRNA Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr15_Sfr15C sRNA Sfr15C2 R 1612711 1612830 - sRNA Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr15_Sfr15C gene NGR_c15640 R 1612866 1612961 YP_002826083.1 hypothetical protein Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr15_Arr15CI gene Arad_3145 D 2505179 2506090 YP_002545096.1 transcription regulator protein Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr15_Arr15CI sRNA Arr15CI1 D 2506215 2506331 - sRNA Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr15_Arr15CI sRNA Arr15CI2 D 2506418 2506534 - sRNA Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr15_Arr15CI gene Arad_3147 D 2506657 2506950 YP_002545097.1 transcription regulator protein Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr15_AH13r15C gene AGROH133_07649 D 2111723 2112625 YP_004279410.1 LysR family transcriptional regulator Agrobacterium sp. H13-3 chromosome (NC_015183)
αr15_AH13r15C sRNA AH13r15C1 D 2112823 2112939 - sRNA Agrobacterium sp. H13-3 chromosome (NC_015183)
αr15_AH13r15C sRNA AH13r15C2 D 2113023 2113121 - sRNA Agrobacterium sp. H13-3 chromosome (NC_015183)
αr15_AH13r15C gene AGROH133_07651 D 2113201 2113515 YP_004279411.1 LysR family transcriptional regulator Agrobacterium sp. H13-3 chromosome (NC_015183)
αr15_Atr15C gene Atu2186 D 2162154 2163056 NP_355147.1 LysR family transcriptional regulator Agrobacterium tumefaciens C58 chromosome circular (NC_003062)
αr15_Atr15C sRNA Atr15C1 D 2163254 2163370 - sRNA Agrobacterium tumefaciens C58 chromosome circular (NC_003062)
αr15_Atr15C sRNA Atr15C2 D 2163454 2163554 - sRNA Agrobacterium tumefaciens C58 chromosome circular (NC_003062)
αr15_Atr15C gene Atu2187 D 2163657 2163947 NP_355148.2 ArsR family transcriptional regulator Agrobacterium tumefaciens C58 chromosome circular (NC_003062)
αr15_Avr15CI gene Avi_3141 D 2607436 2608350 YP_002550262.1 LysR family transcriptional regulator Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr15_Avr15CI sRNA Avr15CI1 D 2608532 2608647 - sRNA Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr15_Avr15CI sRNA Avr15CI2 D 2608739 2608839 - sRNA Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr15_Avr15CI gene Avi_3142 D 2608951 2609238 YP_002550263.1 ArsR family transcriptional regulator Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr15_ReCFNr15a gene RHE_PA00141 D 152078 157177 YP_471730.1 n-6 DNA methylase Rhizobium etli CFN 42 plasmid p42a (NC_007762)
αr15_ReCFNr15a sRNA ReCFNr15a D 157296 157409 - sRNA Rhizobium etli CFN 42 plasmid p42a (NC_007762)
αr15_ReCFNr15a gene RHE_PA00143 D 157744 159486 YP_471732.1 plasmid partitioning protein Rhizobium etli CFN 42 plasmid p42a (NC_007762)
αr15_ReCIATr15B gene RHECIAT_PB0000171 R 187267 187788 YP_001984434.1 excisonase protein Rhizobium etli CIAT 652 plasmid pB (NC_010996)
αr15_ReCIATr15B sRNA ReCIATr15B R 187927 188041 - sRNA Rhizobium etli CIAT 652 plasmid pB (NC_010996)
αr15_ReCIATr15B gene RHECIAT_PB0000172 R 188226 189416 YP_001984435.1 hypothetical protein Rhizobium etli CIAT 652 plasmid pB (NC_010996)
αr15_Avr15Atc gene Avi_9155 D 121509 122600 YP_002542647.1 DNA polymerase III alpha chain Agrobacterium vitis S4 plasmid pAtS4c (NC_011984)
αr15_Avr15Atc sRNA Avr15Atc R 122624 122736 - sRNA Agrobacterium vitis S4 plasmid pAtS4c (NC_011984)
αr15_Avr15Atc gene Avi_9156 D 123011 123358 YP_002542648.1 helicase subunit of the DNA excision repair complex Agrobacterium vitis S4 plasmid pAtS4c (NC_011984)
αr15_ReCFNr15d gene RHE_PD00155 R 172105 172731 NP_659882.1 excisonase protein Rhizobium etli CFN 42 symbiotic plasmid p42d (NC_004041)
αr15_ReCFNr15d sRNA ReCFNr15d R 172760 172874 - sRNA Rhizobium etli CFN 42 symbiotic plasmid p42d (NC_004041)
αr15_ReCFNr15d gene RHE_PD00156 R 173058 174248 NP_659881.2 hypothetical protein Rhizobium etli CFN 42 symbiotic plasmid p42d (NC_004041)
αr15_Avr15Ate gene Avi_7235 D 198046 198699 YP_002539630.1 ABC transporter membrane spanning protein Agrobacterium vitis S4 plasmid pAtS4e (NC_011981)
αr15_Avr15Ate sRNA Avr15Ate D 198928 199039 - sRNA Agrobacterium vitis S4 plasmid pAtS4e (NC_011981)
αr15_Avr15Ate gene Avi_7237 D 199739 200020 YP_002539631.1 transposase Agrobacterium vitis S4 plasmid pAtS4e (NC_011981)
αr15_AH13r15a gene AGROH133_14527 R 210807 211133 YP_004280311.1 XRE family transcriptional regulator Agrobacterium sp. H13-3 plasmid pAspH13-3a (NC_015184)
αr15_AH13r15a gene AGROH133_14529 R 211195 211713 - addiction module toxin Agrobacterium sp. H13-3 plasmid pAspH13-3a (NC_015184)
αr15_AH13r15a sRNA AH13r15a R 211698 211807 - sRNA Agrobacterium sp. H13-3 plasmid pAspH13-3a (NC_015184)
αr15_AH13r15a gene AGROH133_14530 R 211828 212286 YP_004280313.1 hypothetical protein Agrobacterium sp. H13-3 plasmid pAspH13-3a (NC_015184)
αr15_Smedr15p03 gene Smed_6375 R 39464 39784 YP_001314894.1 XRE family transcriptional regulator Sinorhizobium medicae WSM419 plasmid pSMED03 (NC_009622)
αr15_Smedr15p03 sRNA Smedr15p03 R 40054 40165 - sRNA Sinorhizobium medicae WSM419 plasmid pSMED03 (NC_009622)
αr15_Smedr15p03 gene Smed_6376 D 40123 40425 - hypothetical protein Sinorhizobium medicae WSM419 plasmid pSMED03 (NC_009622)
αr15_Avr15Ti gene Avi_8074 R 51395 51682 YP_002540018.1 XRE family transcriptional regulator Agrobacterium vitis S4 plasmid pTiS4 (NC_011982)
αr15_Avr15Ti sRNA Avr15Ti R 52286 52397 - sRNA Agrobacterium vitis S4 plasmid pTiS4 (NC_011982)
αr15_Avr15Ti gene Avi_8076 D 52672 53013 YP_002540020.1 helicase subunit of the DNA excision repair complex Agrobacterium vitis S4 plasmid pTiS4 (NC_011982)
αr15_Rlt1325r15p02 gene Rleg_6607 D 35260 35928 YP_002984610.1 hypothetical protein Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pRt132502 (NC_012858)
αr15_Rlt1325r15p02 sRNA Rlt1325r15p02 D 36176 36289 - sRNA Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pRt132502 (NC_012858)
αr15_Rlt1325r15p02 gene Rleg_6608 D 36740 37528 YP_002984611.1 Exonuclease RNase T and DNA polymerase II Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pRt132502 (NC_012858)
αr15_Sfr15b gene NGR_b01430 D 133718 133900 YP_002822362.1 hypothetical protein Sinorhizobium fredii NGR234 plasmid pNGR234b (NC_012586)
αr15_Sfr15b sRNA Sfr15b R 134078 134190 - sRNA Sinorhizobium fredii NGR234 plasmid pNGR234b (NC_012586)
αr15_Sfr15b gene NGR_b01450 R 134349 136811 YP_002822364.1 diguanylate cyclase phosphodiesterase with pas pac sensor Sinorhizobium fredii NGR234 plasmid pNGR234b (NC_012586)
αr15_Rlvr15p11 gene pRL110525 R 566752 566955 YP_771559.1 hypothetical protein Rhizobium leguminosarum bv. viciae 3841 plasmid pRL11 (NC_008384)
αr15_Rlvr15p11 sRNA Rlvr15p11 R 567053 567166 - sRNA Rhizobium leguminosarum bv. viciae 3841 plasmid pRL11 (NC_008384)
αr15_Rlvr15p11 gene pRL110526 R 567397 568065 YP_771560.1 hypothetical protein Rhizobium leguminosarum bv. viciae 3841 plasmid pRL11 (NC_008384)
αr15_Oar15p02 gene Oant_4749 D 21546 21971 YP_001373166.1 PilT domain-containing protein Ochrobactrum anthropi ATCC 49188 plasmid pOANT02 (NC_009670)
αr15_Oar15p02 sRNA Oar15p02 D 22208 22320 - sRNA Ochrobactrum anthropi ATCC 49188 plasmid pOANT02 (NC_009670)
αr15_Oar15p02 gene Oant_4750 D 22661 24454 YP_001373167.1 plasmid partitioning protein Ochrobactrum anthropi ATCC 49188 plasmid pOANT02 (NC_009670)
αr15_Mlr15a gene msl9071 R 64650 64817 NP_085644.1 hypothetical protein Mesorhizobium loti MAFF303099 plasmid pMLa (NC_002679)
αr15_Mlr15a sRNA Mlr15a R 65044 65154 - sRNA Mesorhizobium loti MAFF303099 plasmid pMLa (NC_002679)
αr15_Mlr15a gene msl9074 R 65712 66008 NP_085645.1 hypothetical protein Mesorhizobium loti MAFF303099 plasmid pMLa (NC_002679)
αr15_Smr15A gene SMa0995 R 551249 552481 NP_435782.1 transposase Sinorhizobium meliloti 1021 plasmid pSymA (NC_003037)
αr15_Smr15A sRNA Smr15A D 552873 552984 - sRNA Sinorhizobium meliloti 1021 plasmid pSymA (NC_003037)
αr15_Smr15A gene SMa0997 D 553196 553492 NP_435783.1 transposase Sinorhizobium meliloti 1021 plasmid pSymA (NC_003037)
αr15_Arr15CII gene Arad_8155 D 1010459 1011472 YP_002541089.1 hypothetical protein Agrobacterium radiobacter K84 chromosome 2 (NC_011983)
αr15_Arr15CII sRNA Arr15CII R 1011511 1011624 - sRNA Agrobacterium radiobacter K84 hromosome 2 (NC_011983)
αr15_Arr15CII gene Arad_8157 D 1012367 1013791 YP_002541091.1 monooxygenase protein Agrobacterium radiobacter K84 hromosome 2 (NC_011983)
αr15_Oar15CI gene Oant_1670 R 1750252 1751097 YP_001370215.1 metallophosphoesterase Ochrobactrum anthropi ATCC 49188 chromosome 1 (NC_009667)
αr15_Oar15CI sRNA Oar15CI D 1751482 1751598 - sRNA Ochrobactrum anthropi ATCC 49188 chromosome 1 (NC_009667)
αr15_Oar15CI gene Oant_1671 D 1752063 1753466 YP_001370216.1 RNA-directed DNA polymerase Ochrobactrum anthropi ATCC 49188 chromosome 1 (NC_009667)
αr15_ReCIATr15pC gene RHECIAT_PC0000855 R 938497 939639 YP_001985475.1 acyltransferase 3 Rhizobium etli CIAT 652 plasmid pC (NC_010997)
αr15_ReCIATr15pC sRNA ReCIATr15pC D 941345 941452 - sRNA Rhizobium etli CIAT 652 plasmid pC (NC_010997)
αr15_ReCIATr15pC gene RHECIAT_PC0000856 R 941811 945572 YP_001985476.1 hemolysin-type calcium-binding protein Rhizobium etli CIAT 652 plasmid pC (NC_010997)
αr15_Oar15CII gene Oant_3861 R 1269354 1269818 YP_001372395.1 hypothetical protein Ochrobactrum anthropi ATCC 49188 chromosome 2 (NC_009668)
αr15_Oar15CII sRNA Oar15CII D 1270083 1270191 - sRNA Ochrobactrum anthropi ATCC 49188 chromosome 2 (NC_009668)
αr15_Oar15CII gene Oant_3862 R 1270409 1273222 YP_001372396.1 glycine dehydrogenase Ochrobactrum anthropi ATCC 49188 chromosome 2 (NC_009668)
αr15_Bm23445r15CII gene BSUIS_B0713 R 695738 695851 YP_001622510.1 hypothetical protein Brucella suis ATCC 23445 chromosome II (NC_010167)
αr15_Bm23445r15CII sRNA Bm23445r15CII D 696081 696188 - sRNA Brucella suis ATCC 23445 chromosome II (NC_010167)
αr15_Bm23445r15CII gene BSUIS_B0714 D 696129 696196 - unknown Brucella suis ATCC 23445 chromosome II (NC_010167)
αr15_Bm23445r15CII gene BSUIS_B0715 R 696787 699585 YP_001622511.1 glycine dehydrogenase Brucella suis ATCC 23445 chromosome II (NC_010167)
αr15_Bm16Mr15CII gene BMEII0561 D 586104 588902 NP_541539.1 glycine dehydrogenase Brucella melitensis bv. 1 str. 16M chromosome II (NC_003318)
αr15_Bm16Mr15CII sRNA Bm16Mr15CII R 589501 589608 - sRNA Brucella melitensis bv. 1 str. 16M chromosome II (NC_003318)
αr15_Bm16Mr15CII gene BMEII0562 D 589690 589950 NP_541540.1 hypothetical protein Brucella melitensis bv. 1 str. 16M chromosome II (NC_003318)
αr15_BaS19r15CII gene BAbS19_II04850 D 504658 507456 YP_001932428.1 glycine dehydrogenase Brucella abortus S19 chromosome 2 (NC_010740)
αr15_BaS19r15CII sRNA BaS19r15CII R 508055 508162 - sRNA Brucella abortus S19 chromosome 2 (NC_010740)
αr15_BaS19r15CII gene BAbS19_II04860 D 508392 508505 YP_001932429.1 hypothetical protein Brucella abortus S19 chromosome 2 (NC_010740)
αr15_Bm23457r15CII gene BMEA_B0698 D 686472 686966 YP_002734467.1 proline dehydrogenase transcriptional activator Brucella melitensis ATCC 23457 chromosome II (NC_012442)
αr15_Bm23457r15CII sRNA Bm23457r15CII D 687290 687397 - sRNA Brucella melitensis ATCC 23457 chromosome II (NC_012442)
αr15_Bm23457r15CII gene BMEA_B0701 R 687996 690794 YP_002734468.1 glycine dehydrogenase Brucella melitensis ATCC 23457 chromosome II (NC_012442)
αr15_Bmir15CII gene BMI_II717 R 708784 709020 YP_003105497.1 hypothetical protein Brucella microti CCM 4915 chromosome 2 (NC_013118)
αr15_Bmir15CII sRNA Bmir15CII D 709102 709209 - sRNA Brucella microti CCM 4915 chromosome 2 (NC_013118)
αr15_Bmir15CII gene BMI_II718 R 709832 712630 YP_003105498.1 glycine dehydrogenase Brucella microti CCM 4915 chromosome 2 (NC_013118)
αr15_Bs1330r15CII gene BRA0724 R 707842 707955 NP_699901.1 hypothetical protein Brucella suis 1330 chromosome II (NC_004311)
αr15_Bs1330r15CII sRNA Bs1330r15CII D 708185 708292 - sRNA Brucella suis 1330 chromosome II (NC_004311)
αr15_Bs1330r15CII gene BRA0725 R 708891 711689 NP_699902.1 glycine dehydrogenase Brucella suis 1330 chromosome II (NC_004311)
αr15_Ba19941r15CII gene BruAb2_0506 D 505454 508252 YP_223286.1 glycine dehydrogenase Brucella abortus bv. 1 str. 9-941 chromosome II (NC_006933)
αr15_Ba19941r15CII sRNA Ba19941r15CII R 508851 508958 - sRNA Brucella abortus bv. 1 str. 9-941 chromosome II (NC_006933)
αr15_Ba19941r15CII gene BruAb2_0507 D 509188 509301 YP_223287.1 hypothetical protein Brucella abortus bv. 1 str. 9-941 chromosome II (NC_006933)
αr15_Bmαr15CII gene BAB2_0515 D 505442 508240 YP_418705.1 glycine dehydrogenase Brucella melitensis biovar Abortus 2308 chromosome II (NC_007624)
αr15_Bmαr15CII sRNA Bmαr15CII R 508839 508946 - sRNA Brucella melitensis biovar Abortus 2308 chromosome II (NC_007624)
αr15_Bmαr15CII gene BAB2_0516 D 509028 509264 YP_418706.1 hypothetical protein Brucella melitensis biovar Abortus 2308 chromosome II (NC_007624)
αr15_Bcr15CII gene BCAN_B0729 D 706646 707140 YP_001594668.1 proline dehydrogenase transcriptional activator Brucella canis ATCC 23365 chromosome II (NC_010104)
αr15_Bcr15CII sRNA Bcr15CII D 707465 707572 - sRNA Brucella canis ATCC 23365 chromosome II (NC_010104)
αr15_Bcr15CII gene BCAN_B0730 R 708171 710969 YP_001594669.1 glycine dehydrogenase Brucella canis ATCC 23365 chromosome II (NC_010104)
αr15_Bor15CI2 gene BOV_1448 D 1459218 1460420 YP_001259376.1 aspartate aminotransferase Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr15_Bor15CI2 sRNA Bor15CI2 R 1460506 1460624 - sRNA Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr15_Bor15CI2 gene BOV_1449 R 1460890 1461795 YP_001259377.1 LysR family transcriptional regulator Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr15_Bcr15CI2 gene BCAN_A1532 D 1450681 1451883 YP_001593329.1 aspartate aminotransferase Brucella canis ATCC 23365 chromosome I (NC_010103)
αr15_Bcr15CI2 sRNA Bcr15CI2 R 1451969 1452087 - sRNA Brucella canis ATCC 23365 chromosome I (NC_010103)
αr15_Bcr15CI2 gene BCAN_A1535 R 1452353 1453258 YP_001593332.1 transcription regulator protein Brucella canis ATCC 23365 chromosome I (NC_010103)
αr15_Bmir15CI2 gene BMI_I1510 D 1460010 1461212 YP_003107423.1 aspartate aminotransferase Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr15_Bmir15CI2 sRNA Bmir15CI2 R 1461298 1461416 - sRNA Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr15_Bmir15CI2 gene BMI_I1512 R 1461682 1462587 YP_003107425.1 LysR family transcriptional regulator Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr15_Bs1330r15CI2 gene BR1495 D 1451723 1452925 NP_698491.1 aspartate aminotransferase Brucella suis 1330 chromosome I (NC_004310)
αr15_Bs1330r15CI2 sRNA Bs1330r15CI2 R 1453011 1453129 - sRNA Brucella suis 1330 chromosome I (NC_004310)
αr15_Bs1330r15CI2 gene BR1498 R 1453395 1454300 NP_698494.1 LysR family transcriptional regulator Brucella suis 1330 chromosome I (NC_004310)
αr15_Bor15CII sRNA Bor15CII D 709415 709524 - sRNA Brucella ovis ATCC 25840 chromosome II (NC_009504)
αr15_Bor15CII gene BOV_A0677 R 704750 708432 - proline dehydrogenase transcriptional activator Brucella ovis ATCC 25840 chromosome II (NC_009504)
αr15_Bor15CII gene BOV_A0679 R 710122 712920 YP_001257680.1 glycine dehydrogenas Brucella ovis ATCC 25840 chromosome II (NC_009504)
αr15_Bm23445r15CI2 gene BSUIS_A1552 D 1472504 1473706 YP_001628154.1 aspartate aminotransferase Brucella suis ATCC 23445 chromosome I (NC_010169)
αr15_Bm23445r15CI2 sRNA Bm23445r15CI2 R 1473791 1473909 - sRNA Brucella suis ATCC 23445 chromosome I (NC_010169)
αr15_Bm23445r15CI2 gene BSUIS_A1554 R 1474175 1475080 YP_001628156.1 hypothetical protein Brucella suis ATCC 23445 chromosome I (NC_010169)
αr15_BaS19r15CI2 gene BAbS19_I14120 D 1468120 1469322 YP_001935379.1 aspartate aminotransferase Brucella abortus S19 chromosome 1 (NC_010742)
αr15_BaS19r15CI2 sRNA BaS19r15CI2 R 1469407 1469525 - sRNA Brucella abortus S19 chromosome 1 (NC_010742)
αr15_BaS19r15CI2 gene BAbS19_I14130 D 1469632 1469739 YP_001935380.1 hypothetical protein Brucella abortus S19 chromosome 1 (NC_010742)
αr15_Ba19941r15CI2 gene BruAb1_1488 D 1469786 1470988 YP_222177.1 aspartate aminotransferase Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr15_Ba19941r15CI2 sRNA Ba19941r15CI2 R 1471073 1471191 - sRNA Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr15_Ba19941r15CI2 gene BruAb1_1490 D 1471190 1471405 YP_222179.1 hypothetical protein Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr15_Bmαr15CI2 gene BAB1_1514 D 1466940 1468142 YP_414880.1 aspartate aminotransferase Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr15_Bmαr15CI2 sRNA Bmαr15CI2 R 1468227 1468345 - sRNA Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr15_Bmαr15CI2 gene BAB1_1516 D 1468344 1468559 YP_414882.1 hypothetical protein Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr15_Bcr15CI1 gene BCAN_A1457 R 1377955 1378815 YP_001593259.1 UDP-3-O-[3-hydroxymyristoyl] N-acetylglucosamine deacetylase Brucella canis ATCC 23365 chromosome I (NC_010103)
αr15_Bcr15CI1 sRNA Bcr15CI1 R 1379297 1379398 - sRNA Brucella canis ATCC 23365 chromosome I (NC_010103)
αr15_Bcr15CI1 sRNA BCAN_A1458 R 1379355 1381055 YP_001593260.1 cell division protein Fts Brucella canis ATCC 23365 chromosome I (NC_010103)
αr15_Bcr15CI1 gene BCAN_A1459 R 1381152 1382474 YP_001593261.1 cell division protein Fts Brucella canis ATCC 23365 chromosome I (NC_010103)
αr15_Bm23445r15CI1 gene BSUIS_A1476 D 1400706 1400831 YP_001628084.1 hypothetical protein Brucella suis ATCC 23445 chromosome I (NC_010169)
αr15_Bm23445r15CI1 sRNA Bm23445r15CI1 R 1401085 1401186 - sRNA Brucella suis ATCC 23445 chromosome I (NC_010169)
αr15_Bm23445r15CI1 gene BSUIS_A1477 R 1401143 1402843 YP_001628085.1 cell division protein Fts Brucella suis ATCC 23445 chromosome I (NC_010169)
αr15_Bm23445r15CI1 gene BSUIS_A1478 R 1402940 1404262 YP_001628086.1 cell division protein Fts Brucella suis ATCC 23445 chromosome I (NC_010169)
αr15_Bm16Mr15CI gene BMEI0585 D 606025 607641 NP_539502.1 cell division protein Fts Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317)
αr15_Bm16Mr15CI sRNA Bm16Mr15CI D 607684 607785 - sRNA Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317)
αr15_Bm16Mr15CI gene BMEI0586 D 608267 609127 NP_539503.1 UDP-3-O-[3-hydroxymyristoyl] N-acetylglucosamine deacetylase Brucella melitensis bv. 1 str. 16M chromosome I (NC_003317)
αr15_BaS19r15CI1 gene BAbS19_I13490 R 1395452 1396312 YP_001935318.1 UDP-3-O-[3-hydroxymyristoyl] N-acetylglucosamine deacetylase Brucella abortus S19 chromosome 1 (NC_010742)
αr15_BaS19r15CI1 gene BAbS19_I13500 R 1396852 1398552 YP_001935319.1 cell division protein Fts Brucella abortus S19 chromosome 1 (NC_010742)
αr15_BaS19r15CI1 sRNA BaS19r15CI1 R 1396794 1396895 - sRNA Brucella abortus S19 chromosome 1 (NC_010742)
αr15_BaS19r15CI1 gene BAbS19_I13510 R 1398649 1399971 YP_001935320.1 heat shock protein Hsp7 Brucella abortus S19 chromosome 1 (NC_010742)
αr15_Bm23457r15CI gene BMEA_A1472 R 1399299 1400159 YP_002733139.1 UDP-3-O-[3-hydroxymyristoyl] N-acetylglucosamine deacetylase Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr15_Bm23457r15CI sRNA Bm23457r15CI R 1400641 1400742 - sRNA Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr15_Bm23457r15CI gene BMEA_A1473 R 1400699 1402399 YP_002733140.1 cell division protein Fts Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr15_Bm23457r15CI gene BMEA_A1474 R 1402496 1403818 YP_002733141.1 cell division protein Fts Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr15_Bmir15CI1 gene BMI_I1436 R 1386434 1387294 YP_003107351.1 UDP-3-O-[3-hydroxymyristoyl] N-acetylglucosamine deacetylase Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr15_Bmir15CI1 sRNA Bmir15CI1 R 1387776 1387877 - sRNA Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr15_Bmir15CI1 gene BMI_I1437 R 1387834 1389534 YP_003107352.1 cell division protein Fts Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr15_Bmir15CI1 gene BMI_I1438 R 1389631 1390953 YP_003107353.1 cell division protein Fts Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr15_Bs1330r15CI1 gene BR1424 R 1379039 1379899 NP_698422.1 UDP-3-O-[3-hydroxymyristoyl] N-acetylglucosamine deacetylase Brucella suis 1330 chromosome I (NC_004310)
αr15_Bs1330r15CI1 sRNA Bs1330r15CI1 R 1380381 1380482 - sRNA Brucella suis 1330 chromosome I (NC_004310)
αr15_Bs1330r15CI1 gene BR1425 R 1380439 1382139 NP_698423.1 cell division protein Fts Brucella suis 1330 chromosome I (NC_004310)
αr15_Bs1330r15CI1 gene BR1426 R 1382236 1383558 NP_698424.1 cell division protein Fts Brucella suis 1330 chromosome I (NC_004310)
αr15_Ba19941r15CI1 gene BruAb1_1419 R 1397122 1397982 YP_222110.1 UDP-3-O-[3-hydroxymyristoyl] N-acetylglucosamine deacetylase Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr15_Ba19941r15CI1 sRNA Ba19941r15CI1 R 1398464 1398565 - sRNA Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr15_Ba19941r15CI1 gene BruAb1_1420 R 1398522 1400222 YP_222111.1 cell division protein Fts Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr15_Ba19941r15CI1 gene BruAb1_1421 R 1400319 1401641 YP_222112.1 cell division protein Fts Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr15_Bmαr15CI1 gene BAB1_1443 R 1394272 1395132 YP_414815.1 UDP-3-O-[3-hydroxymyristoyl] N-acetylglucosamine deacetylase Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr15_Bmαr15CI1 sRNA Bmαr15CI1 R 1395614 1395715 - sRNA Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr15_Bmαr15CI1 gene BAB1_1444 R 1395672 1397372 YP_414816.1 cell division protein Fts Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr15_Bmαr15CI1 gene BAB1_1445 R 1397469 1398791 YP_414817.1 heat shock protein Hsp7 Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr15_Jspr15C gene mma_2445 R 2769080 2769601 YP_001354135.1 phosphinothricin N-acetyltransferas Janthinobacterium sp. Marseille (NC_009659)
αr15_Jspr15C sRNA Jspr15C R 2769681 2769776 - sRNA Janthinobacterium sp. Marseille (NC_009659)
αr15_Jspr15C gene mma_2446 R 2769784 2770767 YP_001354136.1 tricarboxylate binding receptor Janthinobacterium sp. Marseille (NC_009659)
αr15_Bor15CI1 gene BOV_1381 D 1387334 1387726 YP_001259317.1 transposase Orf Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr15_Bor15CI1 sRNA Bor15CI1 R 1387928 1388029 - sRNA Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr15_Bor15CI1 gene BOV_1382 R 1387986 1389686 YP_001259318.1 cell division protein Fts Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr15_Bor15CI1 gene BOV_1383 R 1389783 1391105 YP_001259319.1 cell division protein Fts Brucella ovis ATCC 25840 chromosome I (NC_009505)
gollark: - leaves (non-tree)
gollark: - space filling curves- leaves (tree)
gollark: - electromagnetism- electromagentism- the strong nuclear force- chicken (animal)- armchair (infinite)
gollark: - orange (color)
gollark: - orange (fruit)

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