Biology:αr14 RNA

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αr14 is a family of bacterial small non-coding RNAs with representatives in a broad group of α-proteobacteria. The first member of this family (Smr14C2) was found in a Sinorhizobium meliloti 1021 locus located in the chromosome (C). It was later renamed NfeR1 (Nodule Formation Efficiency RNA) and shown to be highly expressed in salt stress and during the symbiotic interaction on legume roots.[1] Further homology and structure conservation analysis identified 2 other chromosomal copies and 3 plasmidic ones. Moreover, full-length Smr14C homologs have been identified 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). αr14C RNA species are 115-125 nt long (Table 1) and share a well defined common secondary structure (Figure 1). Most of the αr14 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).

Table 1: αr14 homologs in other symbionts and pathogens
CM model Name GI accession number begin end strand %GC length Organism
αr14 Smr14C1 gi|15963753|ref|NC_003047.1| 206862 206980 - 63 119 Sinorhizobium meliloti 1021
αr14 Smr14C2 gi|15963753|ref|NC_003047.1| 1667491 1667613 - 65 123 Sinorhizobium meliloti 1021
αr14 Smr14C3 gi|15963753|ref|NC_003047.1| 1667769 1667891 - 62 123 Sinorhizobium meliloti 1021
αr14 Smr14A1 gi|16262453|ref|NC_003037.1| 1220690 1220808 + 62 119 Sinorhizobium meliloti 1021 plasmid pSymA
αr14 Smr14A2 gi|16262453|ref|NC_003037.1| 1328176 1328301 - 60 126 Sinorhizobium meliloti 1021 plasmid pSymA
αr14 Smr14B gi|16263748|ref|NC_003078.1| 1605826 1605943 + 64 118 Sinorhizobium meliloti 1021 plasmid pSymB
αr14 Smedr14C1 gi|150395228|ref|NC_009636.1| 1258038 1258160 - 63 123 Sinorhizobium medicae WSM419 chromosome
αr14 Smedr14C2 gi|150395228|ref|NC_009636.1| 1258311 1258431 - 65 121 Sinorhizobium medicae WSM419 chromosome
αr14 Smedr14C3 gi|150395228|ref|NC_009636.1| 3590299 3590417 - 63 119 Sinorhizobium medicae WSM419 chromosome
αr14 Smedr14p01 gi|150375726|ref|NC_009620.1| 679043 679160 - 66 118 Sinorhizobium medicae WSM419 plasmid pSMED01
αr14 Smedr14p021 gi|150377168|ref|NC_009621.1| 316304 316428 + 64 125 Sinorhizobium medicae WSM419 plasmid pSMED02
αr14 Smedr14p022 gi|150377168|ref|NC_009622.1| 338866 338990 + 63 125 Sinorhizobium medicae WSM419 plasmid pSMED02
αr14 Sfr14C1 gi|227820587|ref|NC_012587.1| 1434171 1434293 - 64 123 Sinorhizobium fredii NGR234 chromosome
αr14 Sfr14C2 gi|227820587|ref|NC_012587.1| 1434463 1434586 - 60 124 Sinorhizobium fredii NGR234 chromosome
αr14 Sfr14C3 gi|227820587|ref|NC_012587.1| 3720579 3720700 + 66 122 Sinorhizobium fredii NGR234 chromosome
αr14 Sfr14b gi|227818258|ref|NC_012586.1| 2205311 2205428 + 64 118 Sinorhizobium fredii NGR234 plasmid pNGR234b
αr14 Atr14C1 gi|159184118|ref|NC_003062.2| 109473 109601 + 59 129 Agrobacterium tumefaciens str. C58 chromosome circular
αr14 Atr14C2 gi|159185562|ref|NC_003063.2| 1230297 1230426 + 60 130 Agrobacterium tumefaciens str. C58 chromosome linear
αr14 Atr14C3 gi|159185562|ref|NC_003063.2| 1831483 1831614 + 57 132 Agrobacterium tumefaciens str. C58 chromosome linear
αr14 AH13r14C1 gi|325291453|ref|NC_015183.1| 109372 109501 + 58 130 Agrobacterium sp. H13-3 chromosome
αr14 ReCIATr14C1 gi|190889639|ref|NC_010994.1| 513993 514114 + 60 122 Rhizobium etli CIAT 652
αr14 ReCIATr14C2 gi|190889639|ref|NC_010994.1| 1173512 1173639 + 59 128 Rhizobium etli CIAT 652
αr14 ReCIATr14C3 gi|190889639|ref|NC_010994.1| 1912478 1912597 - 64 120 Rhizobium etli CIAT 652
αr14 ReCIATr14C4 gi|190889639|ref|NC_010994.1| 4444894 4445016 - 55 123 Rhizobium etli CIAT 652
αr14 ReCIATr14A gi|190895317|ref|NC_010998.1| 345900 346021 - 63 122 Rhizobium etli CIAT 652 plasmid pA
αr14 ReCIATr14B gi|190893983|ref|NC_010996.1| 112292 112425 + 61 134 Rhizobium etli CIAT 652 plasmid pB
αr14 Arr14CI1 gi|222084201|ref|NC_011985.1| 597903 598030 + 61 128 Agrobacterium radiobacter K84 chromosome 1
αr14 Arr14CI2 gi|222084201|ref|NC_011985.1| 1693278 1693409 - 60 132 Agrobacterium radiobacter K84 chromosome 1
αr14 Arr14CI3 gi|222084201|ref|NC_011985.1| 3945511 3945639 - 59 129 Agrobacterium radiobacter K84 chromosome 1
αr14 Arr14CII1 gi|222080781|ref|NC_011983.1| 957687 957817 + 58 131 Agrobacterium radiobacter K84 chromosome 2
αr14 Arr14CII2 gi|222080781|ref|NC_011983.1| 1921110 1921242 - 61 133 Agrobacterium radiobacter K84 chromosome 2
αr14 Arr14Atc gi|222101962|ref|NC_011987.1| 138495 138625 - 60 131 Agrobacterium radiobacter K84 plasmid pAtK84c
αr14 Rlt2304r14C1 gi|209547612|ref|NC_011369.1| 98050 98171 + 60 122 Rhizobium leguminosarum bv. trifolii WSM2304 chromosome
αr14 Rlt2304r14C2 gi|209547612|ref|NC_011369.1| 1534501 1534621 - 63 121 Rhizobium leguminosarum bv. trifolii WSM2304 chromosome
αr14 Rlt2304r14C3 gi|209547612|ref|NC_011369.1| 4019326 4019446 - 57 121 Rhizobium leguminosarum bv. trifolii WSM2304 chromosome
αr14 Rlt2304r14p011 gi|209546450|ref|NC_011368.1| 306339 306454 - 70 116 Rhizobium leguminosarum bv trifolii WSM2304 plasmid pRLG201
αr14 Rlt2304r14p012 gi|209546450|ref|NC_011368.1| 607636 607759 + 62 124 Rhizobium leguminosarum bv trifolii WSM2304 plasmid pRLG201
αr14 Rlt2304r14p02 gi|209545999|ref|NC_011366.1| 50814 50936 + 63 123 Rhizobium leguminosarum bv trifolii WSM2304 plasmid pRLG202
αr14 Avr14CI1 gi|222147015|ref|NC_011989.1| 115126 115257 + 58 132 Agrobacterium vitis S4 chromosome 1
αr14 Avr14CI2 gi|222147015|ref|NC_011989.1| 2043913 2044044 - 64 132 Agrobacterium vitis S4 chromosome 1
αr14 Avr14CI3 gi|222147015|ref|NC_011989.1| 2793803 2793939 + 63 137 Agrobacterium vitis S4 chromosome 1
αr14 Avr14CII1 gi|222106127|ref|NC_011988.1| 598426 598556 + 62 131 Agrobacterium vitis S4 chromosome 2
αr14 Avr14CII2 gi|222106127|ref|NC_011988.1| 901035 901159 - 63 125 Agrobacterium vitis S4 chromosome 2
αr14 Avr14Atc gi|222083145|ref|NC_011984.1| 7318 7444 + 61 127 Agrobacterium vitis S4 plasmid pAtS4c
αr14 Rlvr14C1 gi|116249766|ref|NC_008380.1| 512658 512779 + 59 122 Rhizobium leguminosarum bv. viciae 3841
αr14 Rlvr14C2 gi|116249766|ref|NC_008380.1| 2174956 2175074 - 65 119 Rhizobium leguminosarum bv. viciae 3841
αr14 Rlvr14C3 gi|116249766|ref|NC_008380.1| 4988030 4988158 - 58 129 Rhizobium leguminosarum bv. viciae 3841
αr14 Rlvr14p11 gi|116255200|ref|NC_008384.1| 574471 574593 - 59 123 Rhizobium leguminosarum bv. viciae 384 plasmid pRL11
αr14 Rlvr14p12 gi|116248676|ref|NC_008378.1| 407202 407316 + 65 115 Rhizobium leguminosarum bv. viciae 384 plasmid pRL12
αr14 Rlt1325r14C1 gi|241202755|ref|NC_012850.1| 107063 107184 + 58 122 Rhizobium leguminosarum bv. trifolii WSM1325
αr14 Rlt1325r14C2 gi|241202755|ref|NC_012850.1| 1697038 1697156 - 63 119 Rhizobium leguminosarum bv. trifolii WSM1325
αr14 Rlt1325r14C3 gi|241202755|ref|NC_012850.1| 4296632 4296749 - 58 118 Rhizobium leguminosarum bv. trifolii WSM1325
αr14 Rlt1325r14p012 gi|241113003|ref|NC_012848.1| 265945 266069 + 62 125 Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132501
αr14 Rlt1325r14p011 gi|241113003|ref|NC_012848.1| 112604 112728 + 66 125 Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132501
αr14 Rlt1325r14p02 gi|241666492|ref|NC_012858.1| 28646 28767 + 60 122 Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132502
αr14 Rlt1325r14p04 gi|241258599|ref|NC_012852.1| 119314 119443 + 59 130 Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132504
αr14 Rlt1325r14p05 gi|241554070|ref|NC_012854.1| 2286 2409 - 65 124 Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132505
αr14 ReCFNr14C1 gi|86355669|ref|NC_007761.1| 462566 462687 - 58 122 Rhizobium etli CFN 42
αr14 ReCFNr14C2 gi|86355669|ref|NC_007761.1| 1926239 1926358 + 65 120 Rhizobium etli CFN 42
αr14 ReCFNr14C3 gi|86355669|ref|NC_007761.1| 4314384 4314505 + 58 122 Rhizobium etli CFN 42
αr14 ReCFNr14e gi|86360278|ref|NC_007765.1| 443001 443129 + 64 129 Rhizobium etli CFN 42 plasmid p42e
αr14 ReCFNr14f gi|86360734|ref|NC_007766.1| 22818 22935 - 64 118 Rhizobium etli CFN 42 plasmid p42f
αr14 ReCFNr14d gi|89255298|ref|NC_004041.2| 77668 77794 - 61 127 Rhizobium etli CFN 42 symbiotic plasmid p42d
αr14 Mlr14C1 gi|57165207|ref|NC_002678.2| 890582 890702 + 68 121 Mesorhizobium loti MAFF303099 chromosome
αr14 Mlr14C2 gi|57165207|ref|NC_002678.2| 890760 890880 + 64 121 Mesorhizobium loti MAFF303099 chromosome
αr14 Mlr14C3 gi|57165207|ref|NC_002678.2| 890941 891061 + 63 121 Mesorhizobium loti MAFF303099 chromosome
αr14 Mlr14C4 gi|57165207|ref|NC_002678.2| 5350767 5350882 + 65 116 Mesorhizobium loti MAFF303099 chromosome
αr14 Mlr14C5 gi|57165207|ref|NC_002678.2| 6092423 6092540 - 64 118 Mesorhizobium loti MAFF303099 chromosome
αr14 Mcr14C1 gi|319779749|ref|NC_014923.1| 3674843 3674963 - 64 121 Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome
αr14 Mcr14C2 gi|319779749|ref|NC_014923.1| 3675022 3675142 - 67 121 Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome
αr14 Mcr14C3 gi|319779749|ref|NC_014923.1| 3675197 3675318 - 65 122 Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome
αr14 Mcr14C4 gi|319779749|ref|NC_014923.1| 2545673 2545788 + 64 116 Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome
αr14 Mcr14C5 gi|319779749|ref|NC_014923.1| 5265891 5266009 + 63 119 Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome
αr14 Mcr14p01 gi|319777789|ref|NC_014918.1| 241412 241531 - 63 120 Mesorhizobium ciceri biovar biserrulae WSM1271 plasmid pMESCI01
αr14 Bcr14CI1 gi|161617991|ref|NC_010103.1| 338021 338128 + 56 108 Brucella canis ATCC 23365 chromosome I
αr14 Bcr14CI2 gi|161617991|ref|NC_010103.1| 867217 867335 - 60 119 Brucella canis ATCC 23365 chromosome I
αr14 Bs23445r14CI1 gi|163842277|ref|NC_010169.1| 355557 355664 + 57 108 Brucella suis ATCC 23445 chromosome I
αr14 Bs23445r14CI2 gi|163842277|ref|NC_010169.1| 888713 888831 - 60 119 Brucella suis ATCC 23445 chromosome I
αr14 Bm16Mr14CI1 gi|17986284|ref|NC_003317.1| 1116661 1116787 + 59 127 Brucella melitensis bv. 1 str. 16M chromosome
αr14 Bm16Mr14CI2 gi|17986284|ref|NC_003317.1| 1644167 1644273 - 56 107 Brucella melitensis bv. 1 str. 16M chromosome
αr14 BaS19r14CI1 gi|189023268|ref|NC_010742.1| 358310 358417 + 56 108 Brucella abortus S19 chromosome 1
αr14 BaS19r14CI2 gi|189023268|ref|NC_010742.1| 888877 888995 - 59 119 Brucella abortus S19 chromosome 1
αr14 Bm23457r14CI2 gi|225851546|ref|NC_012441.1| 890343 890461 - 59 119 Brucella melitensis ATCC 23457 chromosome I
αr14 Bm23457r14CI1 gi|225851546|ref|NC_012441.1| 358976 359082 + 56 107 Brucella melitensis ATCC 23457 chromosome I
αr14 Bs1330r14CI1 gi|56968325|ref|NC_004310.3| 338032 338139 + 56 108 Brucella suis 1330 chromosome I
αr14 Bs1330r14CI2 gi|56968325|ref|NC_004310.3| 868847 868965 - 60 119 Brucella suis 1330 chromosome I
αr14 Ba19941r14CI1 gi|62288991|ref|NC_006932.1| 359925 360032 + 56 108 Brucella abortus bv. 1 str. 9-941 chromosome I
αr14 Ba19941r14CI2 gi|62288991|ref|NC_006932.1| 890576 890694 - 59 119 Brucella abortus bv. 1 str. 9-941 chromosome I
αr14 Bmar14CI2 gi|82698932|ref|NC_007618.1| 886854 886972 - 59 119 Brucella melitensis biovar Abortus 2308 chromosome I
αr14 Bmar14CI1 gi|82698932|ref|NC_007618.1| 356293 356400 + 56 108 Brucella melitensis biovar Abortus 2308 chromosome I
αr14 Bor14CI1 gi|148558820|ref|NC_009505.1| 359682 359789 + 56 108 Brucella ovis ATCC 25840 chromosome I
αr14 Bor14CI2 gi|148558820|ref|NC_009505.1| 895749 895867 - 60 119 Brucella ovis ATCC 25840 chromosome I
αr14 Bmir14CI1 gi|256368465|ref|NC_013119.1| 339699 339806 + 57 108 Brucella microti CCM 4915 chromosome 1
αr14 Bmir14CI2 gi|256368465|ref|NC_013119.1| 873049 873167 - 60 119 Brucella microti CCM 4915 chromosome 1
αr14 Oar14CII1 gi|153010078|ref|NC_009668.1| 274684 274807 + 55 124 Brucella anthropi ATCC 49188 chromosome 2
αr14 Oar14CII2 gi|153010078|ref|NC_009668.1| 1275649 1275772 + 58 124 Brucella anthropi ATCC 49188 chromosome 2
αr14 Oar14CI1 gi|153007346|ref|NC_009667.1| 448505 448614 + 58 110 Brucella anthropi ATCC 49188 chromosome 1
αr14 Oar14CI2 gi|153007346|ref|NC_009667.1| 2453973 2454100 + 56 128 Brucella anthropi ATCC 49188 chromosome 1
αr14 MsBCNr14C1 gi|110632362|ref|NC_008254.1| 1916694 1916817 + 60 124 Mesorhizobium sp. BNC1
αr14 MsBCNr14C2 gi|110632362|ref|NC_008254.1| 3977086 3977208 - 60 123 Mesorhizobium sp. BNC1
αr14 MsBCNr14p1 gi|110346917|ref|NC_008242.1| 135270 135386 - 66 117 Mesorhizobium sp. BNC1 plasmid 1

Discovery and structure

Smr14C2 sRNA was described by del Val et al.,[2] as a result of a computational comparative genomic approach consisting in the integration of complementary strategies, designed to search for novel sRNA-encoding genes 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 smr14C2 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 Smr14C transcript to the 1,667,613 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 1,667,491 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[3][4] in which Smr14C2 transcript is referred to as sra38 or Sm7', independently confirmed the expression this sRNA in S. melilloti and in its closely related strain 2011. Recent deep sequencing-based characterization of the small RNA fraction (50-350 nt) of S. meliloti 2011 further confirmed the expression of Smr14C2 (here referred to as SmelC397), and mapped the 5’- and 3´-ends of the full-length transcript to the same position in the S. meliloti 1021 genome.[5]

Figure 1: Consensus secondary structure of Smr14C2 and the ar14 family predicted by RNA[6] and RNAalifold.[7] The color scheme represent the base pair probabilities.

The nucleotide sequence of Smr14C2 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. Smr14C2 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)[8] (Figure 2). This CM was used in a further search for new members of the αr9 family in the existing bacterial genomic databases and resumed in the following Table 2:

Table 2: Number of copies
Organism Nr. of αr14 chromosomal homologs Nr. of αr14 plasmids homologs Total nr Nr. of αr14 copies
Sinorhizobium meliloti 1021 3 3 6
Sinorhizobium medicae WSM419 3 3 6
Sinorhizobium fredii NGR234 3 3 6
Rhizobium etli CIAT 652 3 3 6
Rhizobium etli CFN 42 3 3 6
Rhizobium leguminosarum bv. trifolii WSM2304 3 2 5
Rhizobium leguminosarum bv. trifolii WSM1325 3 5 8
Rhizobium leguminosarum bv. viciae 3841 4 2 6
Agrobacterium sp. H13-3 2

Agrobacterium vitis S4 3 CI / 2 CII 1 6
Agrobacterium radiobacter K84 3 CI / 2 CII 1 6
Agrobacterium tumefaciens str. C58 3
3
Brucella suis ATCC 23445 2
2
Brucella microti CCM 4915 2
2
Brucella ovis ATCC 25840 2
2
Brucella canis ATCC 23365 2
2
Brucella melitensis ATCC 23457 2
2
Brucella abortus S19 2
2
Brucella abortus bv 1 str 9-941 2
2
Brucella melitensis biovar Abortus 2308 2
2
Brucella suis 1330 2
2
Mesorhizobium loti MAFF303099 5
5
Mesorhizobium sp. BNC1 2 1 3
Mesorhizobium ciceri biovar biserrulae WSM127 4 1 5
Brucella anthropi ATCC 49188 2 CI / 2 CII
4

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[9] with very similar predictions. The manual inspection of the sequences found with the CM using Infernal allowed finding 101 homolog sequences. The rhizobial species encoding the 36 closer homologs to Smr14C2 were: S. medicae and S. fredii, two R. leguminosarum trifolii strains (WSM2304 and WSM1325), two R. etli strains CFN 42 and CIAT 652, the reference R. leguminosarum bv. viciae 3841 strain, and the Agrobacterium species A. vitis,A. tumefaciens, A. radiobacter and A. H13. All these sequences showed significant Infernal E-values (5.63E-29 - 8.16E-18) and bit-scores. The rest of the sequences found with the model showed high E-values between (1.33E-17 and 8.79E-03) 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 loti, M. ciceri and M. BNC.

The model identified five additional copies in the S. meliloti genome, locating two of them in tandem in the same IGR (Smr14C2, Smr14C3). The same results were obtained for S. medicae (Smedr14C1, Smedr14C2), S. fredii (Sfr14C1, Sfr14C2), M. loti (Mlr14C1, Mlr14C2) and M. ciceri (Mcr14C1, Mcr14C2).

Concerning the additional copies found in the S. meliloti genome, the expression of four out of the five copies have been independently confirmed in recent studies:

  • Smr14C3 referred as: sra38,[3] Sm7[4] or SmelC398[5]
  • Smr14A1 referred as: sma8[4] or SmelA075[5]
  • Smr14A2 referred as: SmelA099[5]
  • Smr14B referred as: SmelB161[5]

There are no experimental evidences up to now for the predicted copy Smr14C1.

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.
Figure 3: Phylogenetic distribution of known and predicted αr14 genes. Gene numbers are based on computational analysis using the program Infernal. Shadowed in red are the closer homologs with high Infernal E-values and bit scores. Legend: αr14_Smr14C2 = Sinorhizobium meliloti 1021 (NC_003047) (NC_010994), αr14_Smr14C3 = Sinorhizobium meliloti 1021 (NC_003047) (NC_011985), αr14_Smedr14C1 = Sinorhizobium medicae WSM419 chromosome (NC_009636) (NC_011983), αr14_Smedr14C2 = Sinorhizobium medicae WSM419 chromosome (NC_009636) (NC_011369), αr14_ReCIATr14C3 = Rhizobium etli CIAT 652 (NC_010994) (NC_012850), αr14_Atr14C2 = Agrobacterium tumefaciens str. C58 chromosome linear (NC_003063) (NC_007761), αr14_Rlt1325r14C2 = Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850) (NC_012441), αr14_ReCFNr14C2 = Rhizobium etli CFN 42 (NC_007761) (NC_010994), αr14_Rlt2304r14C2 = Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369) (NC_011985), αr14_AH13r14C1 = Agrobacterium sp. H13-3 chromosome (NC_015183) (NC_011983), αr14_Sfr14C2 = Sinorhizobium fredii NGR234 chromosome (NC_012587) (NC_011369), αr14_Sfr14C1 = Sinorhizobium fredii NGR234 chromosome (NC_012587) (NC_012850), αr14_Rlt2304r14C1 = Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369) (NC_007761), αr14_Atr14C1 = Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062) (NC_012441), αr14_ReCIATr14C1 = Rhizobium etli CIAT 652 (NC_010994) (NC_010994), αr14_Rlvr14C1 = Rhizobium leguminosarum bv. viciae 3841 (NC_008380) (NC_011985), αr14_ReCFNr14C1 = Rhizobium etli CFN 42 (NC_007761) (NC_011983), αr14_Avr14CI1 = Agrobacterium vitis S4 chromosome 1 chromosome 1 (NC_011989) (NC_011369), αr14_Arr14CI2 = Agrobacterium radiobacter K84 chromosome 1 (NC_011985) (NC_012850), αr14_ReCIATr14C4 = Rhizobium etli CIAT 652 (NC_010994) (NC_007761), αr14_Rlt1325r14C1 = Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850) (NC_012441), αr14_Avr14CI2 = Agrobacterium vitis S4 chromosome 1 chromosome 1 (NC_011989) (NC_010994), αr14_Sfr14b = Sinorhizobium fredii NGR234 plasmid pNGR234b (NC_012586) (NC_011985), αr14_Arr14CI3 = Agrobacterium radiobacter K84 chromosome 1 (NC_011985) (NC_011983), αr14_ReCFNr14C3 = Rhizobium etli CFN 42 (NC_007761) (NC_011369), αr14_Rlt1325r14C3 = Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850) (NC_012850), αr14_Rlvr14C3 = Rhizobium leguminosarum bv. viciae 3841 (NC_008380) (NC_007761), αr14_Rlt2304r14C3 = Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369) (NC_012441), αr14_Arr14Atc = Agrobacterium radiobacter K84 plasmid pAtK84c (NC_011987) (NC_010994), αr14_Arr14CII1 = Agrobacterium radiobacter K84 chromosome 2 (NC_011983) (NC_011985), αr14_Smr14B = Sinorhizobium meliloti 1021 plasmid pSymB (NC_003078) (NC_011983), αr14_Avr14CII1 = Agrobacterium vitis S4 chromosome 2 (NC_011988) (NC_011369), αr14_Smedr14p01 = Sinorhizobium medicae WSM419 plasmid pSMED01 (NC_009620) (NC_012850), αr14_Rlt1325r14p05 = Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132505 (NC_012854) (NC_007761), αr14_Rlt1325r14p02 = Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132502(NC_012858) (NC_012441), αr14_Smedr14p022 = Sinorhizobium medicae WSM419 plasmid pSMED02 (NC_009621) (NC_010994), αr14_Rlvr14p11 = Rhizobium leguminosarum bv. viciae 3841 plasmid pRL11 (NC_008384) (NC_011985), αr14_Arr14CII2 = Agrobacterium radiobacter K84 chromosome 2 (NC_011983) (NC_011983), αr14_Arr14CI1 = Agrobacterium radiobacter K84 chromosome 1 (NC_011985) (NC_011369), αr14_ReCFNr14e = Rhizobium etli CFN 42 plasmid p42e (NC_007765) (NC_012850), αr14_Rlt1325r14p012 = Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132501 (NC_012848) (NC_007761), αr14_Rlt2304r14p02 = Rhizobium leguminosarum bv. trifolii WSM2304 plasmid pR132501 (NC_011366) (NC_012441), αr14_Rlt2304r14p012 = Rhizobium leguminosarum bv. trifolii WSM2304 plasmid pR132501 (NC_011368) (NC_010994), αr14_Rlt1325r14p04 = Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132504 (NC_012852) (NC_011985), αr14_Avr14CI3 = Agrobacterium vitis S4 chromosome 1 (NC_011989) (NC_011983), αr14_ReCIATr14A = Rhizobium etli CIAT 652 plasmid pA (NC_010998) (NC_011369), αr14_MsBCNr14C1 = Mesorhizobium sp. BNC1 (NC_008254) (NC_012850), αr14_Avr14CII2 = Agrobacterium vitis S4 chromosome 2 (NC_011988) (NC_007761), αr14_Avr14Atc = Agrobacterium vitis S4 plasmid pAtS4c (NC_011984) (NC_012441), αr14_ReCIATr14C2 = Rhizobium etli CIAT 652 (NC_010994) (NC_010994), αr14_Atr14C3 = Agrobacterium tumefaciens str. C58 chromosome linear (NC_003063) (NC_011985), αr14_ReCIATr14B = Rhizobium etli CIAT 652 plasmid pB (NC_010996) (NC_011983), αr14_ReCFNr14d = Rhizobium etli CFN 42 symbiotic plasmid p42d (NC_004041) (NC_011369), αr14_Sfr14C3 = Sinorhizobium fredii NGR234 chromosome (NC_012587) (NC_012850), αr14_Smedr14C3 = Sinorhizobium medicae WSM419 chromosome (NC_009636) (NC_007761), αr14_Smr14C1 = Sinorhizobium meliloti 1021 (NC_003047) (NC_012441), αr14_Mlr14C1 = Mesorhizobium loti MAFF303099 chromosome (NC_002678) (NC_010994), αr14_Mlr14C2 = Mesorhizobium loti MAFF303099 chromosome (NC_002678) (NC_011985), αr14_Smr14A1 = Sinorhizobium meliloti 1021 plasmid pSymA (NC_003037) (NC_011983), αr14_Rlvr14p12 = Rhizobium leguminosarum bv. viciae 3841 plasmid pRL12 (NC_008378) (NC_011369), αr14_Mcr14C1 = Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923) (NC_012850), αr14_Mcr14C2 = Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923) (NC_007761), αr14_Oar14CI1 = Brucella anthropi ATCC 49188 chromosome 1 (NC_009667) (NC_012441), αr14_Oar14CII1 = Brucella anthropi ATCC 49188 chromosome 2 (NC_009668) (NC_010994), αr14_Smr14A2 = Sinorhizobium meliloti 1021 plasmid pSymA (NC_003037) (NC_011985), αr14_Oar14CI2 = Brucella anthropi ATCC 49188 chromosome 1 (NC_009667) (NC_011983), αr14_Rlt1325r14p011 = Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132501 (NC_012848) (NC_011369), αr14_MsBCNr14C2 = Mesorhizobium sp. BNC1 (NC_008254) (NC_012850), αr14_Bs23445r14CI1 = Brucella suis ATCC 23445 chromosome I (NC_010169) (NC_007761), αr14_Bmir14CI1 = Brucella microti CCM 4915 chromosome I (NC_013119) (NC_012441), αr14_Bor14CI1 = Brucella ovis ATCC 25840 chromosome I (NC_009505) (NC_010994), αr14_Bcr14CI1 = Brucella canis ATCC 23365 chromosome I (NC_010103) (NC_011985), αr14_Bm23457r14CI1 = Brucella melitensis ATCC 23457 chromosome I (NC_012441) (NC_011983), αr14_BaS19r14CI1 = Brucella abortus S19 chromosome I (NC_010742) (NC_011369), αr14_Ba19941r14CI1 = Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932) (NC_012850), αr14_Bmar14CI1 = Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618) (NC_007761), αr14_Bs1330r14CI1 = Brucella suis 1330 chromosome I (NC_004310) (NC_012441), αr14_Smedr14p021 = Sinorhizobium medicae WSM419 plasmid pSMED02 (NC_009621) (NC_010994), αr14_ReCFNr14f = Rhizobium etli CFN 42 plasmid p42f (NC_007766) (NC_011985), αr14_Oar14CII2 = Brucella anthropi ATCC 49188 chromosome 2 (NC_009668) (NC_011983), αr14_Rlt2304r14p011 = Rhizobium leguminosarum bv. trifolii WSM2304 plasmid pRLG201 (NC_011368) (NC_011369), αr14_Mcr14p01 = Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome I (NC_014918) (NC_012850), αr14_Mcr14CI4 = Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome I (NC_014923) (NC_007761), αr14_Mcr14CI5 = Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome I (NC_014923) (NC_012441), αr14_Bor14CI2 = Brucella ovis ATCC 25840 chromosome I (NC_009505) (NC_010994), αr14_Bcr14CI2 = Brucella canis ATCC 23365 chromosome I (NC_010103) (NC_011985), αr14_Bs23445r14CI2 = Brucella suis ATCC 23445 chromosome I (NC_010169) (NC_011983), αr14_Bmir14CI2 = Brucella microti CCM 4915 chromosome 1 (NC_013119) (NC_011369), αr14_Bs1330r14CI2 = Brucella suis 1330 chromosome I (NC_004310) (NC_012850), αr14_Mlr14C5 = Mesorhizobium loti MAFF303099 chromosome (NC_002678) (NC_007761), αr14_Bm16Mr14CI1 = Brucella melitensis bv. 1 str. 16M chromosome (NC_003317) (NC_012441), αr14_BaS19r14CI2 = Brucella abortus S19 chromosome 1 (NC_010742) (NC_010994), αr14_Bm23457r14CI2 = Brucella melitensis ATCC 23457 chromosome I (NC_012441) (NC_011985), αr14_Ba19941r14CI2 = Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932) (NC_011983), αr14_Bmar14CI2 = Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618) (NC_011369), αr14_MsBCNr14p1 = Mesorhizobium sp. BNC1 plasmid 1 (NC_008242) (NC_012850), αr14_Mlr14C4 = Mesorhizobium loti MAFF303099 chromosome (NC_002678) (NC_007761), αr14_Rlvr14C2 = Rhizobium leguminosarum bv. viciae 3841 (NC_008380) (NC_012441).

Expression information

Parallel studies assessed Smr14C 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)[2] and high salt stress, oxidative stress and cold and hot shock stresses.[4] Expression of Smr14C2 in free-living bacteria was found to be growth-dependent, being the gene strongly down-regulated when bacteria entered the stationary phase. Expression of Smr14C2 increased ~5-fold in nodules when compared with free-living bacteria (log phase TY or MM cultures), suggesting the induction of these sRNAs during bacterial infection and/or bacteroid differentiation.[2] Recent deep sequencing data[5] found differential expression of the plasmic copies. Smr14A1 showed differential expression conditions, with a very low expression level in complex medium and in the same medium at decreased temperature. However, it was strongly up-regulated by heat-shock stress.[5] Smr14B showed an increase of its expression in the stationary phase greater that 8 fold. Moreover, also showed a week upregulation (<8 fold) upon acidic, basic and oxidative stress[5]

Promoter analysis

All the promoter regions of the αr14 family members examined so far are very conserved in a sequence stretch extending up to 120 bp upstream of the transcription start site of the sRNA. All closest homolog loci have recognizable σ70-dependent promoters showing a -35/-10 consensus motif CTTAGAC-n17-CTATAT, which has been previously shown to be widely conserved among several other genera in the α-subgroup of proteobacteria.[10] To identify binding sites for other known transcription factors we used the fasta sequences provided by RegPredict[11](http://regpredict.lbl.gov/regpredict/help.html), and used those position weight matrices (PSWM) provided by RegulonDB[12] (http://regulondb.ccg.unam.mx). We built PSWM for each transcription factor from the RegPredict sequences using the Consensus/Patser program, choosing the best final matrix for motif lengths between 14 and 30 bps a threshold average E-value < 10E-10 for each matrix was established, (see "Thresholded consensus" in http://gps-tools2.its.yale.edu). Moreover, we searched for conserved unknown motifs using MEME[13] (http://meme.sdsc.edu/meme4_6_1/intro.html) and used relaxed regular expressions (i.e. pattern matching) over all Smr14C2 homologs promoters. This studies revealed two well defined groups of loci, the first one represented by the closest homologs (Figure 5) that presented a 26 bp long region very conserved between positions -40 and -75, marked as conserved MEME motif in (Figure 5), but no significant similarity to known transcription factor binding sites matrices could be established. A group of not so closely related members of the αr14 family constituted the second group of conserved promoters (Figure6). They presented a different promoter region, very well conserved across all members and an additional unknown 20 bp motif.

Figure 5: Graphic representation of the αr14 seed members' promoter region. All members presented putative σ70 promoters with -30 and -10 boxes marked in green and red respectively.
Figure 6: Graphic representation of the αr14 further related members' promoter region.

Genomic context

Most of the members of the αr14 family are trans-encoded sRNAs transcribed from independent promoters in chromosomal IGRs. Many of the neighboring genes of the seed alignment's members were not annotated and thus were further manually curated.[14][15][16] The tandem copies in the Sinorhizobium group's genomes (Smr14C2, Smr14C3, Smedr14C1, Smedr14C2, Sfr14C1, Sfr14C2) presented a conserved genomic context. The gene upstream coded for an unknown protein containing the domain DUF1127 and the gene downstream coded for a trigger factor.

Partially conserved genomic context, DUF1127 protein upstream and 5-keto-4-deoxyuronate isomerase downstream, was found for the plasmidic copies of the Rhizobium group Rlt1325r14p02, Rlvr14p11, Rlt2304r14p02, and ReCIATr14A.

A similar case of partial genomic conservation, DUF1127 protein upstream and tRNA (uracil-5-)-methyltransferase downstream, was found in the case of the Mesorhizobium species, which also presented tandem copies M. loti (Mlr14C1, Mlr14C2) and M. ciceri (Mcr14C1, Mcr14C2). The same context was found for the second copy in the chromosome II of Brucella anthropi (Oar14CII2) and the second copy in chromosome I in the Brucella group (Bor14CI2, Bcr14CI2, Bmir14CI2, Bs1330r14CI2, Bm16Mr14CI1, BaS19r14CI2, Bm23457r14CI1, BMEA_A0934, BruAb1_0906, Ba19941r14CI2). In all these cases the sRNAs did appear as single copy in their IGR. Bs23445r14CI2, Bmar14CI2, and Rlvr14C2 shared the gene coding for tRNA (uracil-5-)-methyltransferase downstream, but did not share the genes coding upstream.

The results showed two other well-conserved genomic contexts. One with a gene coding for nicotinic acid mononucleotide adenylyltransferase upstream and a gene coding for a molybdenum ABC transporter downstream, which is shared by the third copy of ar14 family in the A. radiobacter genome (Arr14CI3) and in the Rhizobium group genomes (ReCFNr14C3, Rlt1325r14C3, Rlvr14C3, Rlt2304r14C3). The second group is formed by the first copy in the Chromosome I in the Brucellas genomes that share the gene upstream coding for an LrgB membrane protein and the gene downstream a coding for an alpha/beta hydrolase.

Figure 5: Group I according to the genomic context of the αr14 family.. The αr14 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 αr14 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: αr14_Smedr14C1 = Sinorhizobium medicae WSM419 chromosome (NC_009636), αr14_Smr14C2 = Sinorhizobium meliloti 1021 (NC_003047), αr14_Sfr14C1 = Sinorhizobium fredii NGR234 chromosome (NC_012587), αr14_ReCIATr14A = Rhizobium etli CIAT 65 plasmid pA (NC_010998), αr14_Rlt2304r14p02 = Rhizobium leguminosarum bv trifolii WSM2304 plasmid pRLG202 (NC_011366), αr14_Rlvr14p11 = Rhizobium leguminosarum bv viciae 384 plasmid pRL11 (NC_008384), αr14_Rlt1325r14p02 = Rhizobium leguminosarum bv trifolii WSM1325 plasmid pR132502 (NC_012858).
Figure 6: Group II according to the genomic context of the αr14 family.. The αr14 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 αr14 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: αr14_Arr14CI3 = Agrobacterium radiobacter K84 chromosome 1 (NC_011985), αr14_Rlt2304r14C3 = Rhizobium leguminosarum bv trifolii WSM2304 (NC_011369), αr14_Rlvr14C3 = Rhizobium leguminosarum bv viciae 3841 (NC_008380), αr14_Rlt1325r14C3 = Rhizobium leguminosarum bv trifolii WSM1325 (NC_012850), αr14_ReCFNr14C3 = Rhizobium etli CFN 42 (NC_007761).
Figure 7: Group III according to the genomic context of the αr14 family. The αr14 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 αr14 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: αr14_Rlvr14C2 = Rhizobium leguminosarum bv viciae 3841 (NC_008380), αr14_Mlr14C1 = Mesorhizobium loti MAFF303099 chromosome (NC_002678), αr14_Mcr14C1 = Mesorhizobium ciceri biovar biserrulae WSM127 chromosome (NC_014923), αr14_Bcr14CI2 = Brucella canis ATCC 23365 chromosome I (NC_010103), αr14_Bs23445r14CI2 = Brucella suis ATCC 23445 chromosome I (NC_010169), αr14_Bm16Mr14CI1 = Brucella melitensis bv str 16M chromosome I (NC_003317), αr14_BaS19r14CI2 = Brucella abortus S19 chromosome 2 (NC_010742), αr14_Bm23457r14CI1 = Brucella melitensis ATCC 23457 chromosome II (NC_012441), αr14_Bs1330r14CI2 = Brucella suis 1330 chromosome I (NC_004310), αr14_Ba19941r14CI2 = Brucella abortus bv str 9-94chromosome I (NC_006932), αr14_Bmar14CI2 = Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618), αr14_Bor14CI2 = Brucella ovis ATCC 25840 chromosome I (NC_009505), αr14_Bmir14CI2 = Brucella microti CCM 4915 chromosome 2 (NC_013119), αr14_Oar14CI2 = Brucella anthropi ATCC 49188 chromosome 1 (NC_009667).
Figure 8: Group IV according to the genomic context of the αr14 family.. The αr14 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 αr14 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: αr14_Bcr14CI1 = Brucella canis ATCC 23365 chromosome I (NC_010103), αr14_Bs23445r14CI1 = Brucella suis ATCC 23445 chromosome I (NC_010169), αr14_BaS19r14CI1 = Brucella abortus S19 chromosome 1 (NC_010742), αr14_Bs1330r14CI1 = Brucella suis 1330 chromosome I (NC_004310), αr14_Ba19941r14CI1 = Brucella abortus bv str 9-94chromosome I (NC_006932), αr14_Bor14CI1 = Brucella ovis ATCC 25840 chromosome I (NC_009505), αr14_Bmir14CI1 = Brucella microti CCM 4915 chromosome 1 (NC_013119).

Additional files:

Table 3: Detailed Genomic context information of the α14 sRNA seed members.
Family Feature Name Strand Begin End Protein name Annotation Organism
αr14 gene SMc02051 R 1666735 1666878 NP_385651.1 DUF1127 Sinorhizobium meliloti 1021 (NC_003047)
αr14 sRNA Smr14C2 R 1667491 1667613 - sRNA Sinorhizobium meliloti 1021 (NC_003047)
αr14 sRNA Smr14C3 R 1667769 1667891 - sRNA Sinorhizobium meliloti 1021 (NC_003047)
αr14 gene SMc02050 D 1668357 1668441 YP_001326866.1 trigger factor Sinorhizobium meliloti 1021 (NC_003047)
αr14 gene Smed_1180 R 1257614 1257814 YP_001326866.1 DUF1127 Sinorhizobium medicae WSM419 (NC_009636)
αr14 sRNA Smedr14C1 R 1258038 1258160 - sRNA Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr14 sRNA Smedr14C2 R 1258311 1258431 - sRNA Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr14 gene Smed_1181 D 1258759 1258843 YP_001326867.1 trigger factor Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr14 gene RHECIAT_CH0001925 D 1911937 1912446 YP_001978070.1 hypothetical protein Rhizobium etli CIAT 652 (NC_010994)
αr14 sRNA ReCIATr14C3 R 1912478 1912597 - sRNA Rhizobium etli CIAT 652 (NC_010994)
αr14 gene RHECIAT_CH0001926 D 1912923 1914026 YP_001978071.1 membrane protein Rhizobium etli CIAT 652 (NC_010994)
αr14 gene Atu4110 D 1229427 1230176 NP_356536.1 serine dehydrogenase Agrobacterium tumefaciens str. C58 chromosome linear (NC_003063)
αr14 sRNA Atr14C2 D 1230297 1230426 - sRNA Agrobacterium tumefaciens str. C58 chromosome linear (NC_003063)
αr14 gene Atu4112 D 1230719 1231906 NP_356534.2 proline dipeptidase-metalloexopeptidase Agrobacterium tumefaciens str. C58 chromosome linear (NC_003063)
αr14 gene Rleg_1700 R 1696657 1696803 YP_002975526.1 DUF1127 Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr14 sRNA Rlt1325r14C2 R 1697038 1697156 - sRNA Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr14 gene Rleg_1701 D 1697482 1698585 YP_002975527.1 membrane protein Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr14 gene RHE_CH01838 D 1925699 1926187 YP_469358.1 hypothetical protein Rhizobium etli CFN 42 (NC_007761)
αr14 sRNA ReCFNr14C2 R 1926239 1926358 - sRNA Rhizobium etli CFN 42 (NC_007761)
αr14 gene RHE_CH01839 D 1926684 1927778 YP_469359.1 membrane protein Rhizobium etli CFN 42 (NC_007761)
αr14 gene Rleg2_1502 R 1533929 1534075 YP_002281020.1 DUF1127 Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369)
αr14 sRNA Rlt2304r14C2 R 1534501 1534621 - sRNA Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369)
αr14 gene Rleg2_1503 D 1534947 1536050 YP_002281021.1 membrane protein Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369)
αr14 gene AGROH133_02958 R 108794 109252 YP_004277412.1 aminoacyl-tRNA ligase Agrobacterium sp. H13-3 chromosome (NC_015183)
αr14 sRNA AH13r14C1 D 109372 109501 - sRNA Agrobacterium sp. H13-3 chromosome (NC_015183)
αr14 gene AGROH133_02961 D 109733 109942 YP_004277414.1 cold shock protein Agrobacterium sp. H13-3 chromosome (NC_015183)
αr14 gene NGR_c13890 R 1433785 1433985 YP_002825922.1 DUF1127 Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr14 sRNA Sfr14C2 R 1434463 1434586 - sRNA Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr14 sRNA Sfr14C1 R 1434171 1434293 - sRNA Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr14 gene NGR_c13920 R 1434843 1434925 YP_002825924.1 trigger factor Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr14 gene Rleg2_0104 D 96796 97677 YP_002279632.1 aldo/keto reductase Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369)
αr14 sRNA Rlt2304r14C1 D 98050 98171 - sRNA Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369)
αr14 gene Rleg2_0105 D 98282 99559 YP_002279633.1 DUF900, alpha/beta hydrolase Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369)
αr14 gene Atu0104 R 108895 109353 NP_353139.1 aminoacyl-tRNA ligase Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062)
αr14 sRNA Atr14C1 D 109473 109601 - sRNA Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062)
αr14 gene Atu0106 D 109823 110032 NP_353140.2 cold shock protein Agrobacterium tumefaciens str. C58 chromosome circular (NC_003062)
αr14 gene RHECIAT_CH0000515 D 512732 513613 YP_001976686.1 oxidoreductase Rhizobium etli CIAT 652 (NC_010994)
αr14 sRNA ReCIATr14C1 D 513993 514114 - sRNA Rhizobium etli CIAT 652 (NC_010994)
αr14 gene RHECIAT_CH0000517 D 514221 515498 YP_001976688.1 DUF900, alpha/beta hydrolase Rhizobium etli CIAT 652 (NC_010994)
αr14 gene RL0474 D 511376 512272 YP_766083.1 aldo/keto reductase Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr14 sRNA Rlvr14C1 D 512658 512779 - sRNA Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr14 gene RL0475 R 512816 513202 YP_766084.1 hypothetical protein Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr14 gene RHE_CH00449 D 461301 462182 YP_467997.1 oxidoreductase Rhizobium etli CFN 42 (NC_007761)
αr14 sRNA ReCFNr14C1 D 462566 462687 - sRNA Rhizobium etli CFN 42 (NC_007761)
αr14 gene RHE_CH00450 D 462794 464071 YP_467998.1 DUF900, alpha/beta hydrolase Rhizobium etli CFN 42 (NC_007761)
αr14 gene Avi_0122 R 113190 114716 YP_002548072.1 sulfatase Agrobacterium vitis S4 chromosome 1 chromosome 1 (NC_011989)
αr14 sRNA Avr14CI1 D 115126 115257 - sRNA Agrobacterium vitis S4 chromosome 1 chromosome 1 (NC_011989)
αr14 gene Avi_0126 D 115395 116840 YP_002548074.1 phosphomannomutase Agrobacterium vitis S4 chromosome 1 chromosome 1 (NC_011989)
αr14 gene Arad_2144 R 1692677 1692823 YP_002544330.1 DUF1127 Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr14 sRNA Arr14CI2 R 1693278 1693409 - sRNA Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr14 gene Arad_2145 D 1693731 1694870 YP_002544331.1 membrane protein Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr14 gene RHECIAT_CH0004359 D 4444289 4444867 YP_001980464.1 nicotinic acid mononucleotide adenylyltransferase Rhizobium etli CIAT 652 (NC_010994)
αr14 sRNA ReCIATr14C4 R 4444894 4445016 - sRNA Rhizobium etli CIAT 652 (NC_010994)
αr14 gene RHECIAT_CH0004360 R 4445118 4445327 YP_001980465.1 hypothetical protein Rhizobium etli CIAT 652 (NC_010994)
αr14 gene Rleg_0114 D 105825 106706 YP_002973964.1 aldo/keto reductase Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr14 sRNA Rlt1325r14C1 D 107063 107184 - sRNA Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr14 gene Rleg_0115 D 107377 108654 YP_002973965.1 DUF900, alpha/beta hydrolase Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr14 gene Avi_2480 R 2042548 2043660 YP_002549780.1 membrane protein Agrobacterium vitis S4 chromosome 1 chromosome 1 (NC_011989)
αr14 sRNA Avr14CI2 D 2043913 2044044 - sRNA Agrobacterium vitis S4 chromosome 1 chromosome 1 (NC_011989)
αr14 gene Avi_2481 D 2044292 2044441 YP_002549781.1 DUF1127 Agrobacterium vitis S4 chromosome 1 chromosome 1 (NC_011989)
αr14 gene NGR_b21490 R 2204845 2205168 YP_002824347.1 acylphosphatase Sinorhizobium fredii NGR234 plasmid pNGR234b (NC_012586)
αr14 sRNA Sfr14b D 2205311 2205428 - sRNA Sinorhizobium fredii NGR234 plasmid pNGR234b (NC_012586)
αr14 gene NGR_b21500 D 2205588 2206316 YP_002824348.1 RNA polymerase sigma factor Sinorhizobium fredii NGR234 plasmid pNGR234b (NC_012586)
αr14 gene Arad_4880 D 3944888 3945469 YP_002546417.1 nicotinic acid mononucleotide adenylyltransferase Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr14 sRNA Arr14CI3 R 3945511 3945639 - sRNA Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr14 gene Arad_4883 D 3946044 3946844 YP_002546419.1 molybdenum ABC transporter Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr14 gene RHE_CH04070 D 4313781 4314359 YP_471540.1 nicotinic acid mononucleotide adenylyltransferase Rhizobium etli CFN 42 (NC_007761)
αr14 sRNA ReCFNr14C3 R 4314384 4314505 - sRNA Rhizobium etli CFN 42 (NC_007761)
αr14 gene RHE_CH04071 D 4314798 4315589 YP_471541.1 molybdenum ABC transporter Rhizobium etli CFN 42 (NC_007761)
αr14 gene Rleg_4201 D 4295976 4296575 YP_002977981.1 nicotinic acid mononucleotide adenylyltransferase Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr14 sRNA Rlt1325r14C3 R 4296632 4296749 - sRNA Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr14 gene Rleg_4202 D 4297098 4297889 YP_002977982.1 molybdenum ABC transporter Rhizobium leguminosarum bv. trifolii WSM1325 (NC_012850)
αr14 gene RL4684 D 4987413 4988012 YP_770246.1 nicotinic acid mononucleotide adenylyltransferase Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr14 sRNA Rlvr14C3 R 4988030 4988158 - sRNA Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr14 gene RL4685 D 4988507 4989298 YP_770247.1 molybdenum ABC transporter Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr14 gene Rleg2_3877 D 4018721 4019299 YP_002283365.1 nicotinic acid mononucleotide adenylyltransferase Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369)
αr14 sRNA Rlt2304r14C3 R 4019326 4019446 - sRNA Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369)
αr14 gene Rleg2_3878 D 4019781 4020572 YP_002283366.1 molybdenum ABC transporter Rhizobium leguminosarum bv. trifolii WSM2304 chromosome (NC_011369)
αr14 gene Arad_12190 D 137950 138255 YP_002546688.1 FAD dependent oxidoreductase Agrobacterium radiobacter K84 plasmid pAtK84c (NC_011987)
αr14 sRNA Arr14Atc R 138495 138625 - sRNA Agrobacterium radiobacter K84 plasmid pAtK84c (NC_011987)
αr14 gene Arad_12193 R 139226 140683 YP_002546689.1 Cytochrome c2C mono- and diheme oxidoreductase Agrobacterium radiobacter K84 plasmid pAtK84c (NC_011987)
αr14 gene Arad_8084 D 957315 957461 YP_002541036.1 DUF1127 Agrobacterium radiobacter K84 chromosome 2 (NC_011983)
αr14 sRNA Arr14CII1 D 957686 957817 - sRNA Agrobacterium radiobacter K84 chromosome 2 (NC_011983)
αr14 gene Arad_8086 R 957909 958754 YP_002541037.1 DUF900, alpha/beta hydrolase Agrobacterium radiobacter K84 chromosome 2 (NC_011983)
αr14 gene SM_b20590 R 1605382 1605705 NP_438042.1 acylphosphatase Sinorhizobium meliloti 1021 plasmid pSymB (NC_003078)
αr14 sRNA Smr14B D 1605826 1605943 - sRNA Sinorhizobium meliloti 1021 plasmid pSymB (NC_003078)
αr14 gene SM_b20592 D 1606089 1606772 NP_438044.1 RNA polymerase sigma factor Sinorhizobium meliloti 1021 plasmid pSymB (NC_003078)
αr14 gene Avi_5586 D 597555 598229 YP_002547399.1 hypothetical protein Agrobacterium vitis S4 chromosome 2 (NC_011988)
αr14 sRNA Avr14CII1 R 598426 598556 - sRNA Agrobacterium vitis S4 chromosome 2 (NC_011988)
αr14 gene Avi_5587 R 598779 598925 YP_002547400.1 DUF1127 Agrobacterium vitis S4 chromosome 2 (NC_011988)
αr14 gene Smed_4197 R 678214 678885 YP_001312935.1 RNA polymerase sigma factor Sinorhizobium medicae WSM419 plasmid pSMED01 (NC_009620)
αr14 sRNA Smedr14p01 R 679043 679160 - sRNA Sinorhizobium medicae WSM419 plasmid pSMED01 (NC_009620)
αr14 gene Smed_4198 D 679315 679599 YP_001312936.1 acylphosphatase Sinorhizobium medicae WSM419 plasmid pSMED01 (NC_009620)
αr14 gene Rleg_6288 D 1484 2256 YP_002979285.1 hypothetical protein Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132505 (NC_012854)
αr14 sRNA Rlt1325r14p05 R 2286 2409 - sRNA Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132505 (NC_012854)
αr14 gene Rleg_6290 D 3237 3734 YP_002979286.1 hypothetical protein Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132505 (NC_012854)
αr14 gene Rleg_6602 D 28280 28426 YP_002984605.1 DUF1127 Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132502 (NC_012858)
αr14 sRNA Rlt1325r14p02 D 28646 28767 - sRNA Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132502(NC_012858)
αr14 gene Rleg_6603 D 29055 29891 YP_002984606.1 5-keto-4-deoxyuronate isomerase Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132502 (NC_012858)
αr14 gene Smed_5370 D 338535 338681 YP_001314073.1 DUF1127 Sinorhizobium medicae WSM419 plasmid pSMED02 (NC_009621)
αr14 sRNA Smedr14p022 D 338866 338990 - sRNA Sinorhizobium medicae WSM419 plasmid pSMED02 (NC_009621)
αr14 gene Smed_5371 R 339017 339226 YP_001314074.1 hypothetical protein Sinorhizobium medicae WSM419 plasmid pSMED02 (NC_009621)
αr14 gene pRL110530 R 573348 574184 YP_771564.1 5-keto-4-deoxyuronate isomerase Rhizobium leguminosarum bv. viciae 3841 plasmid pRL11 (NC_008384)
αr14 sRNA Rlvr14p11 R 574471 574593 - sRNA Rhizobium leguminosarum bv. viciae 3841 plasmid pRL11 (NC_008384)
αr14 gene pRL110532 R 574811 574957 YP_771566.1 DUF1127 Rhizobium leguminosarum bv. viciae 3841 plasmid pRL11 (NC_008384)
αr14 gene Arad_9216 R 1920052 1920927 YP_002541901.1 glutathione S-transferase Ygh Agrobacterium radiobacter K84 chromosome 2 (NC_011983)
αr14 sRNA Arr14CII2 R 1921110 1921242 - sRNA Agrobacterium radiobacter K84 chromosome 2 (NC_011983)
αr14 gene Arad_9217 R 1921485 1921631 YP_002541902.1 DUF1127 Agrobacterium radiobacter K84 chromosome 2 (NC_011983)
αr14 gene Arad_0725 D 596785 597666 YP_002543276.1 oxidoreductase Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr14 sRNA Arr14CI1 D 597903 598030 - sRNA Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr14 gene Arad_0727 D 598187 599503 YP_002543277.1 DUF900, alpha/beta hydrolase Agrobacterium radiobacter K84 chromosome 1 (NC_011985)
αr14 gene RHE_PE00400 R 441962 442798 YP_472562.1 5-keto-4-deoxyuronate isomerase Rhizobium etli CFN 42 plasmid p42e (NC_007765)
αr14 sRNA ReCFNr14e R 443001 443129 - sRNA Rhizobium etli CFN 42 plasmid p42e (NC_007765)
αr14 gene RHE_PE00401 R 443336 443482 YP_472563.1 hypothetical protein Rhizobium etli CFN 42 plasmid p42e (NC_007765)
αr14 gene Rleg_4483 D 265481 265806 - pseudogen Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132501 (NC_012848)
αr14 sRNA Rlt1325r14p012 D 265945 266069 - sRNA Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132501 (NC_012848)
αr14 gene Rleg_4484 R 266933 267917 - pseudogen Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132501 (NC_012848)
αr14 gene Rleg2_5661 D 50447 50593 YP_002277936.1 DUF1127 Rhizobium leguminosarum bv. trifolii WSM2304 plasmid pR132501 (NC_011366)
αr14 sRNA Rlt2304r14p02 D 50814 50936 - sRNA Rhizobium leguminosarum bv. trifolii WSM2304 plasmid pR132501 (NC_011366)
αr14 gene Rleg2_5662 D 51199 52035 YP_002277937.1 5-keto-4-deoxyuronate isomerase Rhizobium leguminosarum bv. trifolii WSM2304 plasmid pR132501 (NC_011366)
αr14 gene Rleg2_4962 R 606812 607117 YP_002278931.1 hypothetical protein Rhizobium leguminosarum bv. trifolii WSM2304 plasmid pR132501 (NC_011368)
αr14 sRNA Rlt2304r14p012 D 607636 607759 - sRNA Rhizobium leguminosarum bv. trifolii WSM2304 plasmid pR132501 (NC_011368)
αr14 gene Rleg2_4963 R 607786 608067 - pseudogen Rhizobium leguminosarum bv. trifolii WSM2304 plasmid pR132501 (NC_011368)
αr14 gene Rleg_6084 D 118943 119089 YP_002978590.1 DUF1127 Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132504 (NC_012852)
αr14 sRNA Rlt1325r14p04 D 119314 119443 - sRNA Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132504 (NC_012852)
αr14 gene Rleg_6085 R 119664 120056 YP_002978591.1 Cell wall assembly/cell proliferation coordinating protein, KNR4-like Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132504 (NC_012852)
αr14 gene Avi_3374 D 2792636 2793793 YP_002550427.1 DNA polymerase I Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr14 sRNA Avr14CI3 R 2793803 2793939 - sRNA Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr14 gene Avi_3375 R 2794154 2794300 YP_002550428.1 DUF1127 Agrobacterium vitis S4 chromosome 1 (NC_011989)
αr14 gene RHECIAT_PA0000319 R 344808 345644 YP_001985926.1 5-keto-4-deoxyuronate isomerase Rhizobium etli CIAT 652 plasmid pA (NC_010998)
αr14 sRNA ReCIATr14A R 345900 346021 - sRNA Rhizobium etli CIAT 652 plasmid pA (NC_010998)
αr14 gene RHECIAT_PA0000320 R 346130 346366 YP_001985927.1 DUF1127 Rhizobium etli CIAT 652 plasmid pA (NC_010998)
αr14 gene Meso_1791 D 1916546 1916686 YP_674350.1 DUF1127 Mesorhizobium sp. BNC1 (NC_008254)
αr14 sRNA MsBCNr14C1 D 1916694 1916817 - sRNA Mesorhizobium sp. BNC1 (NC_008254)
αr14 gene Meso_1793 R 1918307 1920064 YP_674352.1 hypothetical protein Mesorhizobium sp. BNC1 (NC_008254)
αr14 gene Avi_5890 D 899428 900909 YP_002547646.1 sulfate permease Agrobacterium vitis S4 chromosome 2 (NC_011988)
αr14 sRNA Avr14CII2 D 901035 901159 - sRNA Agrobacterium vitis S4 chromosome 2 (NC_011988)
αr14 gene Avi_5891 R 901178 902659 YP_002547647.1 siroheme synthase Agrobacterium vitis S4 chromosome 2 (NC_011988)
αr14 gene Avi_9007 D 6113 7192 YP_002542553.1 two component sensor kinase Agrobacterium vitis S4 plasmid pAtS4c (NC_011984)
αr14 sRNA Avr14Atc D 7318 7444 - sRNA Agrobacterium vitis S4 plasmid pAtS4c (NC_011984)
αr14 gene Avi_9008 R 7500 8633 YP_002542554.1 phage integrase family protein Agrobacterium vitis S4 plasmid pAtS4c (NC_011984)
αr14 gene RHECIAT_CH0001166 R 1172125 1173279 YP_001977325.1 polyhydroxybutyrate depolymerase protein Rhizobium etli CIAT 652 (NC_010994)
αr14 sRNA ReCIATr14C2 D 1173512 1173639 - sRNA Rhizobium etli CIAT 652 (NC_010994)
αr14 gene RHECIAT_CH0001168 D 1173948 1174214 YP_001977327.1 DUF2277 Rhizobium etli CIAT 652 (NC_010994)
αr14 gene Atu4670 R 1831052 1831294 NP_535148.1 hypothetical protein Agrobacterium tumefaciens str. C58 chromosome linear (NC_003063)
αr14 sRNA Atr14C3 D 1831483 1831614 - sRNA Agrobacterium tumefaciens str. C58 chromosome linear (NC_003063)
αr14 gene Atu4671 R 1831642 1832085 NP_355992.2 response regulator Agrobacterium tumefaciens str. C58 chromosome linear (NC_003063)
αr14 gene RHECIAT_PB0000101 R 111975 112217 YP_001984364.1 hypothetical protein Rhizobium etli CIAT 652 plasmid pB (NC_010996)
αr14 sRNA ReCIATr14B D 112292 112425 - sRNA Rhizobium etli CIAT 652 plasmid pB (NC_010996)
αr14 gene RHECIAT_PB0000102 D 112536 113108 YP_001984365.1 hypothetical protein Rhizobium etli CIAT 652 plasmid pB (NC_010996)
αr14 gene RHE_PD00068 D 76637 77354 NP_659968.2 hypothetical protein Rhizobium etli CFN 42 symbiotic plasmid p42d (NC_004041)
αr14 sRNA ReCFNr14d D 77668 77794 - sRNA Rhizobium etli CFN 42 symbiotic plasmid p42d (NC_004041)
αr14 gene RHE_PD00069 D 77912 78484 NP_659967.1 hydrolase Rhizobium etli CFN 42 symbiotic plasmid p42d (NC_004041)
αr14 gene NGR_c35080 R 3718015 3720336 YP_002827985.1 penicillin-binding Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr14 sRNA Sfr14C3 D 3720579 3720700 - sRNA Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr14 gene NGR_c35100 D 3721900 3722382 YP_002827987.1 hypothetical protein Sinorhizobium fredii NGR234 chromosome (NC_012587)
αr14 gene Smed_3386 R 3589318 3590205 YP_001329042.1 membrane protein Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr14 sRNA Smedr14C3 R 3590299 3590417 - sRNA Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr14 gene Smed_3387 R 3590494 3590925 YP_001329043.1 pyrimidine dimer DNA glycosylase Sinorhizobium medicae WSM419 chromosome (NC_009636)
αr14 gene SMc02855 R 205860 206783 NP_384286.1 membrane protein Sinorhizobium meliloti 1021 (NC_003047)
αr14 sRNA Smr14C1 R 206862 206980 - sRNA Sinorhizobium meliloti 1021 (NC_003047)
αr14 gene SMc02856 D 207244 209547 NP_384287.1 penicillin-binding protein Sinorhizobium meliloti 1021 (NC_003047)
αr14 gene msr1062 D 890180 890389 NP_102735.1 DUF1127 Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr14 sRNA Mlr14C1 D 890582 890702 - sRNA Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr14 sRNA Mlr14C2 D 890760 890880 - sRNA Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr14 gene mlr1064 D 891150 892568 NP_102736.1 tRNA (uracil-5-)-methyltransferase Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr14 gene SMa2165 D 1219615 1220355 NP_436422.1 oxidoreductase Sinorhizobium meliloti 1021 plasmid pSymA (NC_003037)
αr14 sRNA Smr14A1 D 1220690 1220808 - sRNA Sinorhizobium meliloti 1021 plasmid pSymA (NC_003037)
αr14 gene SMa2167 D 1221480 1221947 NP_436423.1 transcription factor regulator Sinorhizobium meliloti 1021 plasmid pSymA (NC_003037)
αr14 gene pRL120374 R 403573 404652 YP_764884.1 ribonuclease domain-containing protein Rhizobium leguminosarum bv. viciae 3841 plasmid pRL12 (NC_008378)
αr14 sRNA Rlvr14p12 D 407202 407316 - sRNA Rhizobium leguminosarum bv. viciae 3841 plasmid pRL12 (NC_008378)
αr14 gene pRL120378 R 408099 409010 YP_764885.1 L-isoaspartate O-methyltransferase Rhizobium leguminosarum bv. viciae 3841 plasmid pRL12 (NC_008378)
αr14 gene Mesci_3513 R 3673344 3674753 YP_004142683.1 tRNA (uracil-5-)-methyltransferase Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
αr14 sRNA Mcr14C1 R 3674843 3674963 - sRNA Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
αr14 sRNA Mcr14C2 R 3675022 3675142 - sRNA Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
αr14 gene Mesci_3514 R 3675321 3675461 YP_004142684.1 DUF1127 Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome (NC_014923)
αr14 gene Oant_0422 D 447656 448351 YP_001368982.1 LrgB membrane protein /hydrolase Brucella anthropi ATCC 49188 chromosome 1 (NC_009667)
αr14 sRNA Oar14CI1 D 448505 448614 - sRNA Brucella anthropi ATCC 49188 chromosome 1 (NC_009667)
αr14 gene Oant_0423 D 448748 450301 YP_001368983.1 glyoxalase bleomycin resistance protein dioxygenase/hydrolase Brucella anthropi ATCC 49188 chromosome 1 (NC_009667)
αr14 gene Oant_2969 R 272174 273850 YP_001371506.1 hypothetical protein Brucella anthropi ATCC 49188 chromosome 2 (NC_009668)
αr14 sRNA Oar14CII1 D 274684 274807 - sRNA Brucella anthropi ATCC 49188 chromosome 2 (NC_009668)
αr14 gene Oant_2970 D 275652 276380 YP_001371507.1 septum formation inhibitor Brucella anthropi ATCC 49188 chromosome 2 (NC_009668)
αr14 gene SMa2355 D 1327042 1328151 NP_436520.4 DNA polymerase I Sinorhizobium meliloti 1021 plasmid pSymA (NC_003037)
αr14 sRNA Smr14A2 R 1328176 1328301 - sRNA Sinorhizobium meliloti 1021 plasmid pSymA (NC_003037)
αr14 gene SMa2357 D 1329978 1330670 NP_436521.2 adenylate guanylate cyclase Sinorhizobium meliloti 1021 plasmid pSymA (NC_003037)
αr14 gene Oant_2332 D 2453758 2453904 YP_001370875.1 DUF1127 Brucella anthropi ATCC 49188 chromosome 1 (NC_009667)
αr14 sRNA Oar14CI2 D 2453973 2454100 - sRNA Brucella anthropi ATCC 49188 chromosome 1 (NC_009667)
αr14 gene Oant_2333 D 2454171 2455601 YP_001370876.1 tRNA (uracil-5-)-methyltransferase Brucella anthropi ATCC 49188 chromosome 1 (NC_009667)
αr14 gene Rleg_4742 D 111695 112336 YP_002972933.1 hypothetical protein Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132501 (NC_012848)
αr14 sRNA Rlt1325r14p011 D 112604 112728 - sRNA Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132501 (NC_012848)
αr14 gene Rleg_4743 R 112925 113309 - hypothetical protein Rhizobium leguminosarum bv. trifolii WSM1325 plasmid pR132501 (NC_012848)
αr14 gene Meso_3687 R 3975340 3976962 YP_676220.1 alpha amylase-C hydrolase Mesorhizobium sp. BNC1 (NC_008254)
αr14 sRNA MsBCNr14C2 R 3977086 3977208 - sRNA Mesorhizobium sp. BNC1 (NC_008254)
αr14 gene Meso_3688 D 3977363 3978682 YP_676221.1 homoserine dehydrogenase-C NAD-binding Mesorhizobium sp. BNC1 (NC_008254)
αr14 gene BSUIS_A0355 D 354629 355336 YP_001627017.1 LrgB membrane protein /hydrolase Brucella suis ATCC 23445 chromosome I (NC_010169)
αr14 sRNA Bs23445r14CI1 D 355557 355664 - sRNA Brucella suis ATCC 23445 chromosome I (NC_010169)
αr14 gene BSUIS_A0356 D 355877 357124 YP_001627018.1 hypothetical protein Brucella suis ATCC 23445 chromosome I (NC_010169)
αr14 gene BMI_I332 D 338771 339478 YP_003106291.1 LrgB membrane protein /hydrolase Brucella microti CCM 4915 chromosome I (NC_013119)
αr14 sRNA Bmir14CI1 D 339699 339806 - sRNA Brucella microti CCM 4915 chromosome I (NC_013119)
αr14 gene BMI_I334 D 340025 341266 YP_003106293.1 DUF900, alpha/beta hydrolase Brucella microti CCM 4915 chromosome I (NC_013119)
αr14 gene BOV_0342 D 358754 359461 YP_001258364.1 hydrolase Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr14 sRNA Bor14CI1 D 359682 359789 - sRNA Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr14 gene BOV_0343 D 360008 361250 - pseudogen Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr14 gene BCAN_A0335 D 337093 337800 YP_001592196.1 LrgB membrane protein /hydrolase Brucella canis ATCC 23365 chromosome I (NC_010103)
αr14 sRNA Bcr14CI1 D 338021 338128 - sRNA Brucella canis ATCC 23365 chromosome I (NC_010103)
αr14 gene BCAN_A0337 D 338347 339588 YP_001592198.1 DUF900, alpha/beta hydrolase Brucella canis ATCC 23365 chromosome I (NC_010103)
αr14 gene BMEA_A0364 D 358048 358755 YP_002732104.1 LrgB membrane protein /hydrolase Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr14 sRNA Bm23457r14CI1 D 358976 359082 - sRNA Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr14 gene BMEA_A0366 D 359302 360543 YP_002732106.1 DUF900, alpha/beta hydrolase Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr14 gene BAbS19_I03260 D 357382 358089 YP_001934341.1 LrgB membrane protein /hydrolase Brucella abortus S19 chromosome I (NC_010742)
αr14 sRNA BaS19r14CI1 D 358310 358417 - sRNA Brucella abortus S19 chromosome I (NC_010742)
αr14 gene BAbS19_I03270 D 358635 359876 YP_001934342.1 DUF900, alpha/beta hydrolase Brucella abortus S19 chromosome I (NC_010742)
αr14 gene BruAb1_0352 D 358997 359704 YP_221113.1 membrane protein Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr14 sRNA Ba19941r14CI1 D 359925 360032 - sRNA Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr14 gene BruAb1_0355 D 361578 362459 YP_221115.1 pantoate—beta-alanine ligase Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr14 gene BAB1_0356 D 355365 356072 YP_413824.1 LrgB membrane protein /hydrolase Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr14 sRNA Bmar14CI1 D 356293 356400 - sRNA Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr14 gene BAB1_0358 D 356618 357859 YP_413825.1 DUF900, alpha/beta hydrolase Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr14 gene BR0326 D 337104 337811 NP_697360.1 DUF900, alpha/beta hydrolase Brucella suis 1330 chromosome I (NC_004310)
αr14 sRNA Bs1330r14CI1 D 338032 338139 - sRNA Brucella suis 1330 chromosome I (NC_004310)
αr14 gene BR0328 D 338358 339599 NP_697362.1 tRNA (uracil-5-)-methyltransferase Brucella suis 1330 chromosome I (NC_004310)
αr14 gene Smed_5352 R 313859 314596 YP_001314057.1 adenylate guanylate cyclase Sinorhizobium medicae WSM419 plasmid pSMED02 (NC_009621)
αr14 sRNA Smedr14p021 D 316304 316428 - sRNA Sinorhizobium medicae WSM419 plasmid pSMED02 (NC_009621)
αr14 gene Smed_5353 R 316485 317621 YP_001314058.1 DNA polymerase I Sinorhizobium medicae WSM419 plasmid pSMED02 (NC_009621)
αr14 gene RHE_PF00022 R 22159 22494 YP_472643.1 hypothetical protein Rhizobium etli CFN 42 plasmid p42f (NC_007766)
αr14 sRNA ReCFNr14f D 22818 22935 - sRNA Rhizobium etli CFN 42 plasmid p42f (NC_007766)
αr14 gene RHE_PF00023 D 23286 23726 YP_472644.1 carbon-sulfur lyase Rhizobium etli CFN 42 plasmid p42f (NC_007766)
αr14 gene Oant_3865 D 1275426 1275572 YP_001372399.1 DUF1127 Brucella anthropi ATCC 49188 chromosome 2 (NC_009668)
αr14 sRNA Oar14CII2 D 1275649 1275772 - sRNA Brucella anthropi ATCC 49188 chromosome 2 (NC_009668)
αr14 gene Oant_3866 R 1275787 1277010 YP_001372400.1 membrane protein Brucella anthropi ATCC 49188 chromosome 2 (NC_009668)
αr14 gene Rleg2_4668 D 305380 306273 YP_002278660.1 L-isoaspartate O-methyltransferase Rhizobium leguminosarum bv. trifolii WSM2304 plasmid pRLG201 (NC_011368)
αr14 sRNA Rlt2304r14p011 R 306339 306454 - sRNA Rhizobium leguminosarum bv. trifolii WSM2304 plasmid pRLG201 (NC_011368)
αr14 gene Rleg2_4670 R 306976 307923 YP_002278662.1 transposase IS110 family protein Rhizobium leguminosarum bv. trifolii WSM2304 plasmid pRLG201 (NC_011368)
αr14 gene Mesci_6302 D 240660 240910 YP_004134462.1 hypothetical protein Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome I (NC_014918)
αr14 sRNA Mcr14p01 R 241412 241531 - sRNA Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome I (NC_014918)
αr14 gene Mesci_6303 R 241784 242047 YP_004134463.1 hypothetical protein Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome I (NC_014918)
αr14 gene Mesci_2426 D 2545134 2545592 YP_004141622.1 phasin Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome I (NC_014923)
αr14 sRNA Mcr14CI4 D 2545673 2545788 - sRNA Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome I (NC_014923)
αr14 gene Mesci_2427 D 2545962 2546038 YP_004141623 FAD dependent oxidoreductase Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome I (NC_014923)
αr14 gene Mesci_5119 D 5264750 5265772 YP_004144269.1 LacI family transcription regulator Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome I (NC_014923)
αr14 sRNA Mcr14CI5 D 5265891 5266009 - sRNA Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome I (NC_014923)
αr14 gene Mesci_5121 R 5266103 5266693 YP_004144271.1 TetR family transcription regulator Mesorhizobium ciceri biovar biserrulae WSM1271 chromosome I (NC_014923)
αr14 gene BOV_0890 R 894271 895671 YP_001258873.1 tRNA (uracil-5-)-methyltransferase Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr14 sRNA Bor14CI2 R 895749 895867 - sRNA Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr14 gene BOV_0891 R 895931 896077 YP_001258874.1 DUF1127 Brucella ovis ATCC 25840 chromosome I (NC_009505)
αr14 gene BCAN_A0908 R 865739 867139 YP_001592741.1 tRNA (uracil-5-)-methyltransferase Brucella canis ATCC 23365 chromosome I (NC_010103)
αr14 sRNA Bcr14CI2 R 867217 867335 - sRNA Brucella canis ATCC 23365 chromosome I (NC_010103)
αr14 gene BCAN_A0909 R 867399 867545 YP_001592742.1 DUF1127 Brucella canis ATCC 23365 chromosome I (NC_010103)
αr14 gene BSUIS_A0933 R 887235 888635 YP_001627570.1 tRNA (uracil-5-)-methyltransferase Brucella suis ATCC 23445 chromosome I (NC_010169)
αr14 sRNA Bs23445r14CI2 R 888713 888831 - sRNA Brucella suis ATCC 23445 chromosome I (NC_010169)
αr14 gene BSUIS_A0934 R 888895 889041 YP_001627571.1 hypothetical protein Brucella suis ATCC 23445 chromosome I (NC_010169)
αr14 gene BMI_I892 R 871571 872971 YP_003106830.1 tRNA (uracil-5-)-methyltransferase Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr14 sRNA Bmir14CI2 R 873049 873167 - sRNA Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr14 gene BMI_I893 R 873231 873377 YP_003106831.1 DUF1127 Brucella microti CCM 4915 chromosome 1 (NC_013119)
αr14 gene BR0894 R 867369 868769 NP_697907.1 tRNA (uracil-5-)-methyltransferase Brucella suis 1330 chromosome I (NC_004310)
αr14 sRNA Bs1330r14CI2 R 868847 868965 - sRNA Brucella suis 1330 chromosome I (NC_004310)
αr14 gene BR0895 R 869029 869175 NP_697908.1 DUF1127 Brucella suis 1330 chromosome I (NC_004310)
αr14 gene mlr7359 D 6091731 6092324 NP_107697.1 transcription factor regulator Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr14 sRNA Mlr14C5 R 6092423 6092540 - sRNA Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr14 gene mll7360 R 6092659 6093681 NP_107698.1 transcription factor regulator Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr14 gene BMEI1072 D 1116469 1116615 NP_539989.1 DUF1127 Brucella melitensis bv. 1 str. 16M chromosome (NC_003317)
αr14 sRNA Bm16Mr14CI1 D 1116661 1116787 - sRNA Brucella melitensis bv. 1 str. 16M chromosome (NC_003317)
αr14 gene BMEI1073 D 1116821 1118257 NP_539990.1 tRNA (uracil-5-)-methyltransferase Brucella melitensis bv. 1 str. 16M chromosome (NC_003317)
αr14 gene BAbS19_I08530 R 887399 888799 YP_001934848.1 tRNA (uracil-5-)-methyltransferase Brucella abortus S19 chromosome 1 (NC_010742)
αr14 sRNA BaS19r14CI2 R 888877 888995 - sRNA Brucella abortus S19 chromosome 1 (NC_010742)
αr14 gene BAbS19_I08540 R 889041 889187 YP_001934849.1 DUF1127 Brucella abortus S19 chromosome 1 (NC_010742)
αr14 gene BMEA_A0933 R 888865 890265 YP_002732640.1 tRNA (uracil-5-)-methyltransferase Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr14 sRNA Bm23457r14CI2 R 890343 890461 - sRNA Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr14 gene BMEA_A0934 R 890507 890653 YP_002732641.1 DUF1127 Brucella melitensis ATCC 23457 chromosome I (NC_012441)
αr14 gene BruAb1_0906 R 889098 890498 YP_221632.1 tRNA (uracil-5-)-methyltransferase Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr14 sRNA Ba19941r14CI2 R 890576 890694 - sRNA Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr14 gene BruAb1_0907 R 890740 890886 YP_221633.1 DUF1127 Brucella abortus bv. 1 str. 9-941 chromosome I (NC_006932)
αr14 gene BAB1_0913 R 885376 886776 YP_414338.1 tRNA (uracil-5-)-methyltransferase Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr14 sRNA Bmar14CI2 R 886854 886972 - sRNA Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr14 gene BAB1_0914 R 887018 887164 YP_414339.1 oxidoreductase Brucella melitensis biovar Abortus 2308 chromosome I (NC_007618)
αr14 gene Meso_4235 R 134555 135097 YP_665858.1 hypothetical protein Mesorhizobium sp. BNC1 plasmid 1 (NC_008242)
αr14 sRNA MsBCNr14p1 R 135270 135386 - sRNA Mesorhizobium sp. BNC1 plasmid 1 (NC_008242)
αr14 gene Meso_4236 R 135539 136099 YP_665859.1 hypothetical protein Mesorhizobium sp. BNC1 plasmid 1 (NC_008242)
αr14 gene mlr6541 D 5350228 5350686 NP_107027.1 phasin Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr14 sRNA Mlr14C4 D 5350767 5350882 - sRNA Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr14 gene mlr6543 D 5351042 5351115 - two component regulator Mesorhizobium loti MAFF303099 chromosome (NC_002678)
αr14 gene RL2059 R 2172416 2173849 YP_767657.1 tRNA (uracil-5-)-methyltransferase Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr14 sRNA Rlvr14C2 R 2174956 2175074 - sRNA Rhizobium leguminosarum bv. viciae 3841 (NC_008380)
αr14 gene RL2060 D 2175400 2176503 YP_767658.1 membrane protein Rhizobium leguminosarum bv. viciae 3841 (NC_008380)

References

  1. ↑ "A conserved α-proteobacterial small RNA contributes to osmoadaptation and symbiotic efficiency of rhizobia on legume roots". Environmental Microbiology 19 (7): 2661–2680. July 2017. doi:10.1111/1462-2920.13757. PMID 28401641. 
  2. ↑ 2.0 2.1 2.2 "Identification of differentially expressed small non-coding RNAs in the legume endosymbiont Sinorhizobium meliloti by comparative genomics". Molecular Microbiology 66 (5): 1080–91. December 2007. doi:10.1111/j.1365-2958.2007.05978.x. PMID 17971083. 
  3. ↑ 3.0 3.1 "Identification of chromosomal alpha-proteobacterial small RNAs by comparative genome analysis and detection in Sinorhizobium meliloti strain 1021". BMC Genomics 8 (467): 467. December 2007. doi:10.1186/1471-2164-8-467. PMID 18093320. 
  4. ↑ 4.0 4.1 4.2 4.3 "Prediction of Sinorhizobium meliloti sRNA genes and experimental detection in strain 2011". BMC Genomics 9 (406): 416. September 2008. doi:10.1186/1471-2164-9-416. PMID 18793445. 
  5. ↑ 5.0 5.1 5.2 5.3 5.4 5.5 5.6 5.7 "Integration of physical and genetic maps of common bean through BAC-derived microsatellite markers". BMC Genomics 11 (245): 436. July 2010. doi:10.1186/1471-2164-11-436. PMID 20637113. 
  6. ↑ I. L. Hofacker, W. Fontana, P. F. Stadler, L. S. Bonhoeffer, M. Tacker and P. Schuster (1994). "Fast folding and comparison of RNA secondary structures". Monatshefte für Chemie 125 (2): 167–188. doi:10.1007/BF00818163. 
  7. ↑ "RNAalifold: improved consensus structure prediction for RNA alignments". BMC Bioinformatics 9 (474): 474. November 2008. doi:10.1186/1471-2105-9-474. PMID 19014431. 
  8. ↑ "Infernal 1.0: inference of RNA alignments". Bioinformatics 25 (10): 1335–7. May 2009. doi:10.1093/bioinformatics/btp157. PMID 19307242. 
  9. ↑ "Inferring Noncoding RNA Families and Classes by Means of Genome-Scale Structure-Based Clustering". PLOS Comput Biol 4 (65): e65. 2007. doi:10.1371/journal.pcbi.0030065. PMID 17432929. Bibcode: 2007PLSCB...3...65W. 
  10. ↑ "Promoter prediction in the rhizobia". Microbiology 152 (Pt 6): 1751–63. June 2006. doi:10.1099/mic.0.28743-0. PMID 16735738. 
  11. ↑ "RegPredict: an integrated system for regulon inference in prokaryotes by comparative genomics approach". Nucleic Acids Research 38 (Web Server issue): W299–307. July 2010. doi:10.1093/nar/gkq531. PMID 20542910. 
  12. ↑ "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): D98–105. January 2011. doi:10.1093/nar/gkq1110. PMID 21051347. 
  13. ↑ "Fitting a mixture model by expectation maximization to discover motifs in biopolymers". Proceedings. International Conference on Intelligent Systems for Molecular Biology (AAAI Press, Menlo Park, California) 2: 28–36. 1994. PMID 7584402. 
  14. ↑ "GOPET: a tool for automated predictions of Gene Ontology terms". BMC Bioinformatics 7: 161. March 2006. doi:10.1186/1471-2105-7-161. PMID 16549020. 
  15. ↑ "Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research". Bioinformatics 21 (18): 3674–6. September 2005. doi:10.1093/bioinformatics/bti610. PMID 16081474. https://hal.archives-ouvertes.fr/hal-01238282/file/Rokitta_2014_BMC%20Genomics.pdf. 
  16. ↑ "ProtSweep, 2Dsweep and DomainSweep: protein analysis suite at DKFZ". Nucleic Acids Research 35 (Web Server issue): W444–50. July 2007. doi:10.1093/nar/gkm364. PMID 17526514. 



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