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. 2010 Feb 11;2009:354649. doi: 10.1155/2009/354649

ATP-Binding Cassette Systems of Brucella

Dominic C Jenner 1,*, Elie Dassa 2, Adrian M Whatmore 3, Helen S Atkins 1
PMCID: PMC2821768  PMID: 20169092

Abstract

Brucellosis is a prevalent zoonotic disease and is endemic in the Middle East, South America, and other areas of the world. In this study, complete inventories of putative functional ABC systems of five Brucella species have been compiled and compared. ABC systems of Brucella melitensis 16M, Brucella abortus 9-941, Brucella canis RM6/66, Brucella suis 1330, and Brucella ovis 63/290 were identified and aligned. High numbers of ABC systems, particularly nutrient importers, were found in all Brucella species. However, differences in the total numbers of ABC systems were identified (B. melitensis, 79; B. suis, 72; B. abortus 64; B. canis, 74; B. ovis, 59) as well as specific differences in the functional ABC systems of the Brucella species. Since B. ovis is not known to cause human brucellosis, functional ABC systems absent in the B. ovis genome may represent virulence factors in human brucellosis.

1. Introduction

Brucella species are the causative agents of brucellosis, the world's most prevalent zoonotic disease, with high occurrences in endemic areas including the Middle East, Asia, Mexico, and the Mediterranean [1]. The bacteria are small nonmotile, Gram-negative, nonspore-forming coccobacilli that reside within the subphylum α-proteobacteria, which also includes nitrogen-fixing bacteria of the genus Nitrobacter, Rhizobium, Agrobacterium, and Rickettsia [2]. They are considered facultative intracellular pathogens.

There are six traditionally recognised Brucella species that have different host preferences: Brucella melitensis (which usually infects sheep and goats), Brucella abortus (cattle), Brucella suis (pigs), Brucella ovis (sheep), Brucella canis (dogs), and Brucella neotomae (desert wood rats). Furthermore, there are three newly identified Brucella species isolated from marine mammals: Brucella pinnipedialis (seals) [3], Brucella ceti (dolphins and porpoises) [3], and Brucella microti (voles) [4]. Although Brucella are primarily animal pathogens causing infectious abortions in females and orchitis in males [5], four of the nine species may infect humans (B. melitensis, B. abortus, B. suis, and occasionally B. canis, in order of disease severity) causing a range of flu-like symptoms including fever, sweats, malaise, and nausea [6]. Transmission to humans takes place via three recognised channels: (i) the consumption of infected animal products, (ii) direct contact with infected animal birth products, and (iii) the inhalation of aerosolised Brucella. Due to the nature of the human disease and the ability to be infectious via aerosol, Brucella species have been classified as category B threat agents by the US Centre for Disease Control and Prevention (CDC) [7].

Genome sequence analysis of B. melitensis 16M [8], B. suis 1330 [9], B. abortus 9-941 [10], B. canis RM6/66 (NCBI: NC_009504 and NC_009505, unpublished), and B. ovis 63/290 (NCBI: NC_010103 and NC_0010104, unpublished) has demonstrated the close relatedness of these organisms [11, 12]. The genomic DNA of each strain comprises two chromosomes of approximately 2.1 Mb and 1.2 Mb. DNA-DNA hybridisations between the species had previously revealed over 90% similarity between the species, leading to the suggestion that all Brucella species should be classified as B. melitensis [13, 14]. However, it is widely believed that the differences in host specificity and pathogenicity are related to Brucella genetics; although there is currently little experimental evidence to support this, a few studies have found differences between the Brucella species genomes that may support this hypothesis [10, 15, 16]. A significant proportion of the Brucella genomes appear to code for ATP-binding cassette (ABC) systems.

ABC transporters are responsible for the import and export of many different substances across cellular membranes [17]. Although ABC transporters are extremely versatile, they all contain one defining feature, the ability to hydrolyse ATP to ADP, providing the energy needed for active transport. ABCs have three main conserved motifs known as Walker A (G-X-X-G-X-G-K-S/T, where X represents any amino acid residue), Walker B (ø-ø-ø-ø-D, where ø designates a hydrophobic residue), and a signature sequence (LSGGQ) [18]. The Walker A and Walker B motifs form tertiary structure enabling ATP-binding and can be found in all ATP-binding molecules. The signature sequence is well conserved in all ABC proteins and is also known as the linker peptide or C motif [19]. Although the configuration of ABC systems varies, the majority of ABC systems comprise of two hydrophilic ABC domains associated with two hydrophobic membrane-spanning domains (inner membrane (IM) proteins). Import systems are only found in prokaryotic organisms and contain both ABC domains and IM domains, along with extra-cytoplasmic binding proteins (BPs) designed to bind the specific allocrite of that ABC system. In Gram-negative bacteria the BPs are located in the periplasm whereas, in Gram-positive bacteria, they are anchored to the outer membrane of the cell via N-terminal lipid groups [20]. ABC systems import a diverse range of substrates into the bacterial cell including peptides [21], polyamines [22], metal ions [23], amino acids [24], iron [25], and sulphates [26]. In comparison, ABC systems involved in export functions usually contain only IM and ABC domains fused together via either the N-terminus (IM-ABC) or the C-terminus (ABC-IM), which homodimerise to create a functional system [27]. Substances exported by ABC transporters include antibiotics in both producing and resistant bacteria [28, 29], fatty acids in Gram-negative bacteria [27], and toxins [30]. In addition to transporters, many ABC proteins have roles in house-keeping functions, such as regulation of gene expression [31] and DNA repair [27, 32]. These proteins do not contain IM domains but are constituted of two fused ABC domains (ABC2) [27]. There is now increasing evidence that ABC systems can play roles in bacterial virulence [33–36] and can be used as targets for vaccine development [37].

The recent sequencing of the genomes of B. melitensis 16M [8], B. abortus 9-941 [10], B. suis 1330 [9], B. ovis 63/290 (NCBI: NC_009504 and NC_009505, unpublished), and B. canis RM6/66 (NCBI: NC_010103 and NC_0010104, unpublished) has enabled the genomic comparison of different Brucella species. We report the creation and comparison of reannotated inventories of the functional ABC systems in Brucella. This improved annotation has assisted in understanding Brucella lifestyles and the identification of ABC systems that may be involved in virulence.

2. Methods

The prediction of ABC systems in sequenced bacterial genomes is based on annotation- and similarity-based homology assessment of identified or predicted ABC proteins from heterologous bacterial systems. The Artemis viewer (available from http://www.sanger.ac.uk) was used to visualise the sequenced genomes of B. melitensis 16 M, B. suis 1330, B. abortus 9-941, B. canis RM6/66, and B. ovis 63/290 [8–10]. Using the annotated genomes, ABC proteins were searched for using an array of related words, specifically “ATP-binding cassettes,” “binding protein”, or “outer membrane protein.” For completeness all proteins that were labelled as hypothetical or conserved hypothetical proteins were also checked. Hits from this search were compiled and then genes upstream and downstream were also checked to ensure that all genes from one system were found. After the genome searches were completed, protein sequences were aligned using the basic local alignment search tool (BlastP) against other ABC proteins using the ABC systems: Information on Sequence Structure and Evolution (ABCISSE) database [27, 38]. The ABCISSE database comprises 24000 proteins from 9500 annotated systems over 795 different organisms. Proteins searched against ABCISSE that scored a threshold e-value of 10−6 were assigned to an ABC family and subfamily based on the hits from the ABCISSE database. Where searches on ABCISSE were unclear or hits for multiple families were produced, proteins were aligned using BlastP searches against the Genbank protein database. Use of this larger database increased the number of positive hits and functions that could be assigned. An ABC system was defined as a series of contiguous ORFs that shared the same family, subfamily, and substrate. A complete signal sequence (LSGGQ) was identified in the majority of the ABC proteins identified, and all of the other ABC proteins contained remnants of a complete signal sequence. Walker A and Walker B sequences were not sought during these searches.

The ABC system inventories compiled in this study include systems that contain genes with predicted frame shift mutations and premature stop codons. For example, the B. melitensis 16M gene BMEII0099 is a known pseudogene with multiple premature stop codons. However, this gene is part of an ABC system that is encoded by another four genes (BMEII0098, BMEII00101, BMEII102, and BMEII0103), all of which are predicted to be functional; the mutation in BMEII0099 might render the whole system nonfunctional or it is possible that the other four genes could create a partially functional system. Due to the inability to determine the functionality of ABC systems using bioinformatic techniques, the ABC systems where one or more components were predicted to be nonfunctional were excluded from the total ABC system numbers and functions of the ABC systems. Within the genomes of all Brucella species single components of ABC systems (mainly BP) not attached to individual systems were located. These were included in ABC system inventories and termed lone components but were not included in total functional ABC system counts.

3. Results and Discussion

The genome structures of Brucella species are very similar [10–12], and although it is widely believed that the differences in Brucella species virulence and host preferences are related to their genetic composition, there is little experimental evidence to support this belief. However, there are a few studies that have uncovered differences between the genomes [10, 15, 16]. In this study we have compared the presence of putative functional ABC systems in the genomes of B. melitensis 16M (BM), B. suis 1330 (BS), B. abortus 9-941(BS), B. canis RM6/66 (BC), and B. ovis 63/290 (BO). In the original annotations of these genomes, a uniform nomenclature was not used and functional assignment of the systems varied considerably. Here we describe a reannotation of the ABC systems of these bacterial strains, leading to new predicted functions of the systems and predictions about how the individual components combine to form functional systems. Complete inventories of the ABC systems of BM, BS, BA, BC, and BO are shown in Table 1.

Table 1.

Reconstruction and comparative inventories of Brucella ABC systems.

Number Family Subfamily Substrate/Function Type B. melitensis B. abortus B.suis B. ovis B. canis
1 ART REG Involved in gene expression regulation ABC2 BMEI0288 BruAb11738 BR1753 BOV_1692 BCAN_A1791
2 ART REG Involved in gene expression regulation ABC2 BMEI0553 BruAb11451 BR1456 BOV_1411 BCAN_A1491
3 ART REG Involved in gene expression regulation ABC2 BMEI1258 BruAb10711 BR0692 BOV_0683 BCAN_A0704
4 CBY CBU Cobalt import ABC BMEI0635 BruAb11365 BR1368 BOV_1324 BCAN_A1395
CBY CBU Cobalt import IM BMEI0637 BruAb11364 BR1367 BOV_1323 BCAN_A1394, CbiQ
5 CCM Possibly heme export IM BMEI1851 BR0096, ccmC BOV_0094 BCAN_A0098, ccmC
CCM Possibly heme export IM BMEI1852 BR0095, ccmB BOV_0093 BCAN_A0097, ccmB
CCM Possibly heme export ABC BMEI1853 BR0094, ccmA BOV_0092 BCAN_A0096, ccmA
6 CDI Involved in cell division IM BMEI0073, ftsX BruAb11971 BR1996 BCAN_A2042
CDI Involved in cell division ABC BMEI0072, ftsE BruAb11972, ftsE BR1997, ftsE BCAN_A2043, ftsE
7 CLS O antigen export system ABC BMEI1416, rfbB BR0519, rfbE BOV_0523 BCAN_A0531, rfbB
CLS O antigen export system IM BMEI1415, rfbD BR0520, rfbD BOV_0524 BCAN_A0532, rfbD
8 DLM (ABCY) D-L-Methionine and derivatives import LPP BMEI1954
9 DLM (ABCY) D-L-Methionine and derivatives import IM BMEII0336 BruAb20271 BRA0962 BOV_A0903 BCAN_B0983
DLM (ABCY) D-L-Methionine and derivatives import ABC BMEII0337 BruAb20272 BRA0961 BOV_A0902 BCAN_B0982
DLM (ABCY) D-L-Methionine and derivatives import LPP BMEII0338 BruAb20273 BRA0960
10 DPL CYD Cytochrome bd biogenesis and cysteine export IM-ABC BMEII0761, cydC BruAb20713 BRA0509 BOV_A0443 BCAN_B0508
DPL CYD Cytochrome bd biogenesis and cysteine export IM-ABC BMEII0762, cydD BruAb20714, cydD BRA0508, cydD BOV_A0442 BCAN_B0507, CydD
11 DPL MDL Involved in mitochondrial export systems IM-ABC BMEI0323, msbA BruAb11700 BR1715 BOV_1657 BCAN_A1753
12 DPL HMT Involved in mitochondrial export systems IM-ABC BMEI0472 BruAb11533 BR1545 BOV_1493 BCAN_A1581
DPL HMT Involved in mitochondrial export systems IM-ABC BMEI0471 BruAb11534 BR1544 BOV_1494 BCAN_A1582
13 DPL PRT Proteases, lipase, S-layer protein export OMP BMEI1029, TolC BruAb10954 BCAN_A0957
14 DPL CHV Beta-(1–>2) glucan export IM-ABC BMEI0984 BruAb11004 BR0998 BCAN_A1015
15 DPL HMT Heavy metal tolerance protein IM-ABC BMEI1492 BruAb10321 BR0442 BOV_0449 BCAN_A0446
16 DPL HMT Involved in mitochondrial export systems IM-ABC BMEI1743
DPL HMT Involved in mitochondrial export systems IM-ABC BMEI1742 BOV_0198
17 DPL LIP Involved in lipid A or polysaccharide export IM-ABC BMEII0250 BruAb20990 BRA1050 BOV_A0988 BCAN_B1071
18 DRI YHIH Unknown IM BMEI0656 BruAb11347 BR1349 BOV_1307 BCAN_A1377
DRI YHIH Unknown IM BMEI0655
DRI YHIH Unknown ABC2 BMEI0654 BruAb11348 BR1350 (ABC2-IM) BOV_1308 BCAN_A1378
DRI YHIH Unknown MFP BMEI0653 BruAb11349 BR1351 BOV_1309 BCAN_A1379
19 DRI YHIH Unknown IM BMEII0801 BruAb20757 BRA0465 BCAN_B0467
DRI YHIH Unknown ABC BMEII0802, drrA BruAb20758 BRA0464 BOV_A0403 BCAN_B0466
DRI YHIH Unknown MFP BMEII0803 BruAb20759 BRA0463 BOV_A0404 BCAN_B0465
20 DRI NOS Nitrous oxide reduction IM BMEII0970, nosY BruAb20902, nosY BRA0278, nosY BOV_A0254 BCAN_B0280
DRI NOS Nitrous oxide reduction ABC BMEII0971, nosF BruAb20903, nosF BRA0277, nosF BOV_A0253 BCAN_B0279
DRI NOS Nitrous oxide reduction SS BMEII0972 BruAb20904, nosD BRA0276, nosD BOV_A0252 BCAN_B0278
21 FAE Fatty acid export IM-ABC BMEI0520 BruAb11484 BR1490 BCAN_A1528
22 FAE Fatty acid export IM-ABC BMEII0976 BruAb20908 BOV_A0247 BCAN_B0273
23 HAA Branched-chain amino acids IM BMIE0258, LivH BruAb11771 BR1790 BOV_1725 BCAN_A1829
HAA Branched-chain amino acids IM BMIE0259, LivM BruAb11772 BR1791 BOV_1724 BCAN_A1828
HAA Branched-chain amino acids ABC BMEI0260, braF BruAb11770 BR1788 BOV_1723 BCAN_A1827
HAA Branched-chain amino acids ABC BMEI0261, braG BruAb11769 BR1789 BOV_1722 BCAN_A1826
HAA Branched-chain amino acids BP BMEI0263 BruAb11765 BR1785 BOV_1720 BCAN_A1823
HAA Branched-chain amino acids BP BMEI0264 BruAb11767 BR1782 BCAN_A1820
HAA Branched-chain amino acids BP BMEI0265 BOV_1719
24 HAA Branched-chain amino acids BP BMEI1930 BR0014 BOV_0012 BCAN_A0014
25 HAA Branched-chain amino acids ABC BMEII0065, livF BruAb20027 BRA0028 BOV_A0025 BCAN_B0030
HAA Branched-chain amino acids ABC BMEII0066, livG BruAb20028 BRA0027 BOV_A0024 BCAN_B0029
HAA Branched-chain amino acids IM BMEII0067, livM BruAb20025 BRA0026 BOV_A0023 BCAN_B0028
HAA Branched-chain amino acids IM BMEII0068, livH BruAb20026 BRA0025 BOV_A0022 BCAN_B0027
HAA Branched-chain amino acids BP BMEII0069 BruAb20024 BRA0024 BOV_A0021 BCAN_B0026
26 HAA Branched-chain amino acids ABC BMEII0098 BruAb21132 BRA1197 BOV_A1099 BCAN_B1227
HAA Branched-chain amino acids ABC BMEII0099 BruAb21133 BRA1196 BOV_A1098 BCAN_B1226
HAA Branched-chain amino acids IM BMEII0101 BruAb21131 BRA1194 BOV_A1097 BCAN_B1225
HAA Branched-chain amino acids IM BMEII0102 BruAb21130 BRA1195 BOV_A1096 BCAN_B1224
HAA Branched-chain amino acids BP BMEII0103 BruAb21129 BRA1193 BOV_A0195 BCAN_B1223
27 HAA Branched-chain amino acids ABC BMEII0119 BruAb21111 BRA1176 BOV_A1079 BCAN_B1207
HAA Branched-chain amino acids IM-ABC BMEII0120 BruAb21112 BRA1175 BOV_A1078 BCAN_B1206
HAA Branched-chain amino acids IM BMEII0121 BruAb21110 BRA1174 BCAN_B1205
HAA Branched-chain amino acids BP BMEII0122 BruAb21109 BRA1173 BOV_A1076 BCAN_B1204
28 HAA Branched-chain amino acids IM BMEII0340 BruAb20276 BRA0957 BCAN_B0977
HAA Branched-chain amino acids IM BMEII0341 BruAb20277 BRA0956 BOV_A0897 BCAN_B0978
HAA Branched-chain amino acids ABC BMEII0342 BruAb20278 BRA0955 BOV_A0896 BCAN_B0976
HAA Branched-chain amino acids ABC BMEII0343 BruAb20279 BRA0954 BOV_A0895 BCAN_B0975
HAA Branched-chain amino acids BP BMEII0344 BruAb20280 BRA0953 BOV_A0894 BCAN_B0974
29 HAA Branched-chain amino acids ABC BMEII0628 BruAb20574 BRA0652 BOV_A0613 BCAN_B0652
HAA Branched-chain amino acids ABC BMEII0629 BruAb20575 BRA0651 BOV_A0614 BCAN_B0651
HAA Branched-chain amino acids IM BMEII0630 BruAb20577 BRA0650 BOV_A0611 BCAN_B0649
HAA Branched-chain amino acids IM BMEII0632 BruAb20576 BRA0649 BOV_A0612 BCAN_B0650
HAA Branched-chain amino acids BP BMEII0633 BruAb20578 BRA0648 BOV_A0610 BCAN_B0648
30 HAA Branched-chain amino acids BP BMEII0875 BruAb20801 BRA0392 BCAN_B0398
HAA Branched-chain amino acids BP BMEII0868 BruAb20809 BRA0400 BOV_A0343 BCAN_B0395
HAA Branched-chain amino acids ABC BMEII0874 BruAb20806 BRA0395 BOV_A0338 BCAN_B0389
HAA Branched-chain amino acids ABC BMEII0873 BruAb20807 BRA0394 BOV_A0337 BCAN_B0396
HAA Branched-chain amino acids IM BruAb20808 BRA0393 BOV_A0336 BCAN_B0397
31 ISB (ABCX) Iron/sulphur centre biogenesis CYTP BMEI1040 BruAb10941 BR0931
ISB (ABCX) Iron/sulphur centre biogenesis CYTP BMEI1042 BruAb10940 BR0933
ISB (ABCX) Iron/sulphur centre biogenesis ABC BMEI1041 BruAb10942 BR0932
32 ISVH Iron-siderophores, VB12 and Hemin import ABC BMEI0660 BruAb11342 BR1344 BOV_1302 BCAN_A1371
ISVH Iron-siderophores, VB12 and Hemin import IM BMEI0659 BruAb11343 BR1345 BOV_1304 BCAN_A1372
ISVH Iron-siderophores, VB12 and Hemin import OMR BMEI0657 BruAb11344 BR1347 BOV_1306 BCAN_A1374
ISVH Iron-siderophores, VB12 and Hemin import BP BMEI0658 BruAb11345 BR1346 BOV_1305 BCAN_A1373
33 ISVH Iron(III) dicitrate import BP BMEII0535 BruAb20476 BRA0756 BOV_A0705 BCAN_B0763
ISVH Iron(III) dicitrate import IM BMEII0536, fecD BruAb20477 BRA0755 BOV_A0704 BCAN_B0764
ISVH Iron(III) dicitrate import ABC BMEII0537, fecE BruAb20478 BRA0754 BOV_A0703 BCAN_B0762
34 ISVH Iron(III) import ABC BMEII0604 BruAb20550 BRA0678 BOV_A0635 BCAN_B0677
ISVH Iron(III) import IM BMEII0605, fatC BruAb20551 BRA0676 BOV_A0634 BCAN_B0675
ISVH Iron(III) import IM BMEII0606, fatD BruAb20552 BRA0677 BOV_A0633 BCAN_B0676
ISVH Iron(III) import BP BMEII0607 BruAb20553 BRA0675 BOV_A0632 BCAN_B0674
35 MET Zinc import IM BMEII0176, ZnuB BruAb21061, ZnuB BRA1124, ZnuB BOV_A1029 BCAN_B1152
MET Zinc import ABC BMEII0177, ZnuC BruAb21060, ZnuC BRA1123, ZnuC BOV_A1028 BCAN_B1151
MET Zinc import BP BMEII0178, ZnuA BruAb21059, ZnuA BRA1122, ZnuA BOV_A1027 BCAN_B1150
36 MKL Involved in toluene tolerance ABC BMEI0964 BruAb11025 BR1020 BOV_0987
MKL Involved in toluene tolerance IM BMEI0965, ttg2B BruAb1024 BR1019 BOV_0986
MKL Involved in toluene tolerance SS BMEI0963, ttg2C BruAb11026 BR1021 BOV_0988
37 MOI Thiamine import ABC BMEI0283, thiQ BruAb11744 BR1759 BOV_1698 BCAN_A1798
MOI Thiamine import IM BMEI0284, thiP BruAb11743, thiP BR1758, thiP BOV_1696 thiP, BCAN_A1797
MOI Thiamine import BP BMEI0285 BruAb11744, thiB BR1757, thiB BOV_1695 thiB, BCAN_A1796
38 MOI Putrescine import BP BMEI0411, potF BruAb11599 BR1612 BOV_1556 BCAN_A1649
MOI Putrescine import ABC BMEI0412 BruAb11598 BR1611 BOV_1555 BCAN_A1648
MOI Putrescine import IM BMEI0413 BruAb11596 BR1609 BOV_1554 BCAN_A1647
MOI Putrescine import IM BMEI0414 BruAb11597 BR1610 BOV_1553 BCAN_A1646
39 MOI Sulphate import IM BMEI0675, cysW BruAb11328, cysW2 BR1328, cysW2 BOV_1288 CysW, BCAN_A1353
MOI Sulphate import IM BMEI0674, cysT BruAb11329 BR1329 BOV_1289 CysT, BCAN_A1354
MOI Sulphate import BP BMEI0673 BruAb11330 BR1330 BOV_1290 BCAN_A1355
40 MOI Sulphate import ABC BMEI1838 cysA BruAb10107 BR0110 BOV_0107 CysA, BCAN_A0113
MOI Sulphate import IM BMEI1839, cysW BruAb10106 BR0109, cysW1 BOV_0106 CysW, BCAN_A0112
MOI Sulphate import IM BMEI1840, cyst BruAb10105, cysT BR0108 BOV_0105 CysT, BCAN_A0111
MOI Sulphate import BP BMEI1841 BruAb10104 BR0107 BOV_0104 BCAN_A0110
41 MOI Phosphate import ABC BMEI1986, pstB BruAb12116, pstB BR2141, pstB BOV_2056 BCAN_A2185, pstB
MOI Phosphate import IM BMEI1987, pstA BruAb12114, pstC BR2139, pstC BOV_2055 BCAN_A2184, pstA
MOI Phosphate import IM BMEI1988, pstC BruAb12115, pstA BR2140 BOV_2054 BCAN_A2183, pstC
MOI Phosphate import BP BMEI1989 BruAb12113 BR2138 BOV_2053 BCAN_A2128
42 MOI Molybdenum import ABC BMEII0003, modC BruAb20090 BRA0090, modC BOV_A0084 BCAN_B0093, ModC
MOI Molybdenum import IM BMEII004, modB BruAb20089 BRA0089, modB BOV_A0083 BCAN_B0092, ModB
MOI Molybdenum import BP BMEII0005 BruAb20088 BRA0088, modA BOV_A0082 BCAN_B0091
43 MOI Spermidine/putrescine import ABC BMEII0193, potA BruAb21046 BRA1107 BCAN_B1129
MOI Spermidine/putrescine import IM BMEII0194, potB BruAb21044 BRA1106 BCAN_B1128
MOI Spermidine/putrescine import IM BMEII0195, potC BruAb21045 BRA1105 BCAN_B1127
MOI Spermidine/putrescine import BP BMEII0196 BruAb21043 BRA1104 BCAN_B1126
44 MOI Unknown BP BMEII0479 BruAb20422 BRA0810 BOV_A0760 BCAN_B0824
MOI Unknown ABC BMEII0481 BruAb20423 BRA0809 BOV_A0759 BCAN_B0823
MOI Unknown IM BMEII0483 BruAb20424 BRA0807 BOV_A0758 BCAN_B0822
MOI Unknown IM BMEII0484 BruAb20425 BRA0808 BOV_A0757 BCAN_B0821
45 MOI Iron(III) import BP BMEII0565 BruAb20510 BRA0720 BOV_A0676 BCAN_B0726
MOI Iron(III) import IM2 BMEII0566 BruAb20511 BRA0719 BOV_A0675 BCAN_B0274
MOI Iron(III) import ABC BMEII0567 BruAb20512 BRA0718 BOV_A0674 BCAN_B0725
46 MOI Iron(III) import ABC BMEII0583 BruAb20529 BRA0701 BOV_A0656 BCAN_B0702
MOI Iron(III) import BP BMEII0584 BruAb20530 BRA0700 BOV_A0655 BCAN_B0703
MOI Iron(III) import IM2 BMEII0585 BruAb20531 BRA0699 BOV_A0654 BCAN_B0701
47 MOI Spermidine/putrescine import IM BMEII0920, potC BruAb20852 BRA0328 BOV_A0303 BCAN_B0331
MOI Spermidine/putrescine import IM BMEII0921, potB BruAb20853 BRA0329 BOV_A0302 BCAN_B0330
MOI Spermidine/putrescine import ABC BMEII0922, potA BruAb20855 BRA0327 BOV_A0301 BCAN_B0329
MOI Spermidine/putrescine import BP BMEII0923, potD BruAb20854 BRA0326 BOV_A0300 BCAN_B0328
48 MOI Iron(III) import BP BMEII1120 BruAb20113 BRA0115 BOV_A0105 BCAN_B0119
MOI Iron(III) import IM BMEII1121, sufB BruAb20111 BRA0114 BOV_A0104 BCAN_B0118
MOI Iron(III) import IM BMEII1122, sufB BruAb20112 BRA0113 BOV_A0103 BCAN_B0117
MOI Iron(III) import ABC BMEII1123, sufC BruAb20110 BRA0112 BOV_A0102 BCAN_B0116
49 New1 Unknown IM BMEI0013 BruAb12030 BR2055 BOV_1975 BCAN_A2101
New1 Unknown ABC BMEI0012 BruAb12031 BR2056 BCAN_A2102
New1 Unknown BP BMEI0014
New1 Unknown BP BMEI0015
50 MOS Ribose import ABC2 BMEI0391 BruAB11620, rbsA-2 BR1632, rbsA-2 BOV_1576 BCAN_A1669
MOS Ribose import IM BMEI0392 BruAB11619, rbsC-2 BR1631, rbsC-2 BOV_1575, rbsC2 BCAN_A1668
MOS Ribose import BP BMEI0393 BruAB11618 BR1630 BOV_1574 BCAN_A1667
51 MOS Ribose Import ABC BMEI0665 BruAb11337 BR1339 BOV_1299 BCAN_A1367
MOS Ribose Import IM BMEI0664 BruAb11338 BR1340 BOV_1300 BCAN_A1368
MOS Ribose Import BP BMEI0663 BruAb11340 BR1342 BOV_1301 BCAN_A1369
MOS Ribose Import BP BMEI0662 BruAb11335
52 MOS Ribose import BP BMEI1390 BruAb10566, rbsB1 BR0544, rbsB1 BOV_0546 rbsB1 BCAN_A0557
MOS Ribose import IM BMEI1391, rbsC BruAb10565, rbsC1 BR0543, rbsC1 BOV_0545 rbsC1 BCAN_A0555
MOS Ribose import ABC2 BMEI1392, rbsA BruAb10564, rbsA1 BR0542, rbsA1 BOV_0544 rbsA1 BCAN_A0554, rsbA
53 MOS Possibly galactoside BP BMEII0083 BruAb20010 BRA0010 BOV_A0007
MOS Possibly galactoside ABC2 BMEII0085, mglA BruAb20009 BRA0009 BOV_A0006
MOS Possibly galactoside IM BMEII0086, mglC BruAb20007 BRA0007 BOV_A0005
MOS Possibly galactoside IM BMEII0087 BruAb20008 BRA0008 BOV_A0004
54 MOS Xylose import IM BMEII0144, xylH BruAb21089, xylH BRA1152, xylH BOV_A1057 BCAN_B1181
MOS Xylose import ABC2 BMEII0145, xylG BruAb21088, xylG BRA1151, xylG BOV_A1056 BCAN_B1180, xylG
MOS Xylose import BP BMEII0146, xylF BruAb21087, xylF BRA1150, xylF BOV_A1055 BCAN_B1179, xylF
55 MOS Ribose import ABC2 BMEII0300, rbsA BruAb20239rbsA4 BRA0995, rbsA4 BOV_A0937 BCAN_B1014
MOS Ribose import IM BMEII0301 rbsC BruAb20240,rbsC5 BRA0993, rbsC5 BCAN_B1013
MOS Ribose import IM BMEII0302 rbsC BruAb20239, rbsC4 BRA0994, rbsC5 BOV_A0935 BCAN_B1012
MOS Ribose import BP BruAb20238 BRA0996, rbsB3 BOV_A0938 BCAN_B1015
56 MOS Monosaccharide import BP BMEII0360, chvE BruAb20296 BRA0937 BOV_A0879 BCAN_B0957
MOS Monosaccharide import ABC2 BMEII0361 BruAb20297 BRA0936 BOV_A0878 BCAN_B0956
MOS Monosaccharide import IM BMEII0362 BruAb20298 BRA0935 BOV_A0877 BCAN_B0955
57 MOS Erythritol import ABC2 BMEII0432, rbsA BruAb20371, rbsA3 BRA0860, rbsA3 BOV_A0807, rsbA3 BCAN_B0877
MOS Erythritol import IM BMEII0433, rbsC BruAb20372, rbsC3 BRA0859, rbsC3 BCAN_B0876
MOS Erythritol import BP BMEII0435 BruAb20373, rbsB2 BRA0858, rbsB2 BOV_A0805 BCAN_B0875
58 MOS Galactoside/Ribose import ABC2 BMEII0698 BruAb20654 BRA0570 BOV_A0533 BCAN_B0570
MOS Galactoside/Ribose import IM BOV_A0534 BCAN_B0567
MOS Galactoside/Ribose import IM BMEII0700 BruAb20655 BRA0568 BOV_A0535
MOS Galactoside/Ribose import IM BMEII0701 BruAb20656 BRA0569 BCAN_B0568
MOS Galactoside/Ribose import BP BMEII0702 BRA0567 BOV_A0532 BCAN_B0567
59 MOS Monosaccharide import IM BMEII0981 BruAb20913 BRA0267 BOV_A0242 BCAN_B0268
MOS Monosaccharide import ABC2 BMEII0982 BruAb20914 BRA0266 BOV_A0241 BCAN_B0267
MOS Monosaccharide import BP BMEII0983 BruAb20916 BRA0265 BOV_A0240 BCAN_B0266
60 o228 Unknown IM BMEI0361
O228 Unknown MFP BMEI0359
o228 Unknown ABC BMEI0360
61 o228 Unknown IM BruAb10085 BR0087 BOV_0085
O228 Unknown MFP BCAN_A1712
o228 Unknown ABC BruAb10084 BR0086 BOV_0084 BCAN_A1711
62 o228 Unknown MFP BruA11658 BR1671 BOV_1617
o228 Unknown IM-ABC BruA11657 BR1670 BOV_1616 BCAN_A0087
63 o228 Lipoprotein release system ABC BMEI1138, LolD BruAb10838,LolD BR0824, LolD BOV_0818 BCAN_A0839
o228 Lipoprotein release system IM BMEI1139, LolE BruAb10837, LolE BR0823, LolE BOV_0817 BCAN_A0838
64 OPN Dipeptide import ABC BMEI0438, dppF BruAb11569 BR1582 BOV_1527 BCAN_A1617
OPN Dipeptide import ABC BMEI0437, dppD BruAb11570 BR1583 BOV_1528 BCAN_A1618
OPN Dipeptide import IM BMEI0435, dppC BruAb11571 BR1584 BOV_1530 BCAN_A1620
OPN Dipeptide import IM BMEI0436, dppC BruAb11572 BR1585 BOV_1529 BCAN_A1619
OPN Dipeptide import BP BMEI0433, dppA BruAb11573 BR1586 BOV_1531 BCAN_A1621
65 OPN Oligopeptide import ABC2 BMEI1938, oppD BruAb10006 BR0006 BOV_0006 BCAN_A0006
OPN Oligopeptide import BP BMEI1934 BruAb10007 BR0007 BOV_0009 BCAN_A0010
OPN Oligopeptide import BP BMEI1935 BruAb10008 BR0008 BOV_0010 BCAN_A0009
OPN Oligopeptide import IM BMEI1936, oppB BruAb10009 BR0009 BOV_0008 BCAN_A0008
OPN Oligopeptide import IM BMEI1937, oppC BruAb10010 BR0010 BOV_0007 BCAN_A0007
66 OPN Oligopeptide import ABC BMEII0199, oppF BruAb21039 BRA1100
OPN Oligopeptide import ABC BMEII0200, oppD BruAb21040 BRA1101 BCAN_B1123
OPN Oligopeptide import IM BMEII0201, oppC BruAb21037 BRA0099 BCAN_B1122
OPN Oligopeptide import IM BMEII0202, oppB BruAb21038 BRA0098 BCAN_B1121
OPN Oligopeptide import BP BMEII01203 BruAb21036 BRA0097 BCAN_B1119
67 OPN Dipeptide import ABC BMEII0205, dppF BruAb21033 BRA1095 BOV_A0950 BCAN_B1117
OPN Dipeptide import ABC BMEII0206, dppD BruAb21034 BRA1094 BOV_A0951 BCAN_B1116
OPN Dipeptide import IM BMEII0207, dppC BruAb21031 BRA1093 BCAN_B1115, dppC
OPN Dipeptide import IM BruAb21032 BRA1092 BOV_A0952
OPN Dipeptide import IM BMEII0209, dppB BOV_A0953 BCAN_B1114
OPN Dipeptide import BP BMEII0210 BruAb21030 BRA1090 BOV_A0954 BCAN_B1113
68 OPN Dipeptide/ Oligopeptide import BP BMEII0217 BruAb21024 BRA1084 BCAN_B1107
OPN Dipeptide/ Oligopeptide import IM BMEII0220 BruAb21020 BRA1081 BCAN_B1104
OPN Dipeptide/ Oligopeptide import IM BMEII0221 BruAb21021 BRA1080 BCAN_B1103
OPN Dipeptide/ Oligopeptide import ABC BMEII0222 BruAb21018 BRA1079 BCAN_B1102
OPN Dipeptide/ Oligopeptide import ABC BMEII0223 BruAb21019 BRA1078 BCAN_B1101
69 OPN Dipeptide import BP BMEII0284 BruAb20952 BRA1012 BOV_A0504 BCAN_B1032
OPN Dipeptide import IM BMEII0285 BruAb20950 BRA1009 BOV_A0501 BCAN_B1031
OPN Dipeptide import IM BMEII0286 BruAb20951 BRA1008 BOV_A0502 BCAN_B1030
OPN Dipeptide import ABC BMEII0287 BruAb20948 BRA1011 BOV_A0500 BCAN_B1029
OPN Dipeptide import ABC BMEII0288 BruAb20949 BRA1010 BOV_A0501 BCAN_B1028
70 OPN Nickel import BP BMEII0487 BruAb20428 BRA0804 BOV_A0754 BCAN_B0818, NikA
OPN Nickel import IM BMEII0488, nikB BruAb20429, nikB BRA0802, nikC BOV_A0752 BCAN_B0817, NikB
OPN Nickel import IM BMEII0489, nikC BruAb20430, nikV BRA0803, nikB BOV_A0753 BCAN_B0816, NikC
OPN Nickel import ABC BMEII0490, nikD BruAb20431, nikD BRA0800, nikE BOV_A0751 BCAN_B0815, NikD
OPN Nickel import ABC BMEII0491, nikE BruAb20432, nikE BRA0801, nikD BCAN_B0814, NikE
71 OPN Oligopeptide import BP BMEII0504 BruAb20446 BRA0783 BOV_A0737 BCAN_B0800
OPN Oligopeptide import IM BMEII0505 BruAb20447 BRA0788 BOV_A0736 BCAN_B0799
OPN Oligopeptide import IM BMEII0506 BruAb20448 BRA0787 BOV_A0735 BCAN_B0798
OPN Oligopeptide import ABC BMEII0507 BruAb20449 BRA0786 BOV_A0734 BCAN_B0797
OPN Oligopeptide import ABC BMEII0508 BOV_A0733 BCAN_B0796
72 OPN Oligopeptide import BP BMEII0691 BruAb20648 BRA0576 BOV_A0542
73 OPN Oligopeptide import BP BMEII0734 BruAb20684 BRA0538 BOV_A0468 BCAN_B0538
OPN Oligopeptide import BP BMEII0735, oppA BruAb20685 BRA0537 BOV_A0467 BCAN_B0537
OPN Oligopeptide import IM BMEII0736 BruAb20686 BRA0536 BOV_A0466 BCAN_B0535
OPN Oligopeptide import IM BMEII0737 BruAb20687 BRA0535 BOV_A0465 BCAN_B0536
OPN Oligopeptide import ABC2 BMEII0738 BruAb20688 BRA0534 BOV_A0464 BCAN_B0534
74 OPN Oligopeptide import BP BMEII0859 BruAb20792 BRA0409 BOV_A0352 BCAN_B0412
OPN Oligopeptide import IM BMEII0860 BRA0408 BOV_A0351 BCAN_B0411
OPN Oligopeptide import IM BMEII0861 BruAb20794 BRA0407 BOV_A0350 BCAN_B0410
OPN Oligopeptide import ABC BMEII0863 BruAb20796 BRA0405 BOV_A0347 BCAN_B0408
OPN Oligopeptide import ABC BMEII0864 BruAb20797 BRA0404 BOV_A0348 BCAN_B0407
75 OSP Maltose import ABC BMEI1713, malK BruAb10233 BR0238 BOV_0231 BCAN_A0241
OSP Maltose import IM BMEI1714, malG BruAb10231 BR0237 BOV_0230 BCAN_A0240
OSP Maltose import IM BMEI1715, malF BruAb10232 BR0236 BOV_0229 BCAN_A0239
OSP Maltose import BP BMEI1716 BruAb10230 BR0235 BOV_0228 BCAN_A0238
76 OSP Oligosaccharide or polyol import ABC BMEII0112, ugpC BruAb21119 BRA1183 BOV_A1086 BCAN_B1214
OSP Oligosaccharide or polyol import IM BMEII0113, ugpA BruAb21118 BRA1181 BOV_A1085 BCAN_B1213
OSP Oligosaccharide or polyol import IM BMEII0114, ugpE BruAb21117 BRA1182 BOV_A1084 BCAN_B1212
OSP Oligosaccharide or polyol import BP BMEII0115 BruAb21116 BRA1180 BCAN_B1211
77 OSP Oligosaccharide or polyol import IM BMEII0541 BruAb20483 BRA0749 BOV_A0700 BCAN_B0757
OSP Oligosaccharide or polyol import IM BruAb20482 BRA0750 BOV_A0699 BCAN_B0756
OSP Oligosaccharide or polyol import BP BMEII0542 BruAb20484 BRA0748 BOV_A0698 BCAN_B0755
OSP Oligosaccharide or polyol import ABC BMEII0544 BruAb20487 BRA0745 BOV_A0696 BCAN_B0753
78 OSP Oligosaccharide or polyol import BP BMEII0590 BruAb20537 BRA0693 BOV_A0648 BCAN_B0691
OSP Oligosaccharide or polyol import IM BMEII0591 BruAb20538 BRA0691 BOV_A0647 BCAN_B0690
OSP Oligosaccharide or polyol import IM BMEII0592 BruAb20539 BRA0692 BOV_A0646 BCAN_B0689
OSP Oligosaccharide or polyol import ABC BMEII0593 BruAb20540 BRA0690 BOV_A0645 BCAN_B0688
79 OSP SN-glycerol-3-phosphate import ABC BMEII0621, ugpC BruAb20568, ugpC BRA0658, ugpC BOV_A0620 BCAN_B0658
OSP SN-glycerol-3-phosphate import IM BMEII0622, ugpE BruAb20569, ugpE BRA0657, ugpE BOV_A0619 BCAN_B0657
OSP SN-glycerol-3-phosphate import IM BMEII0623, ugpE BruAb20570, ugpA BRA0656, ugpA BOV_A0618 BCAN_B0656
OSP SN-glycerol-3-phosphate import IM BMEII0624, ugpA
OSP SN-glycerol-3-phosphate import BP BMEII0625 BruAb20571, ugpB BRA0655, ugpA BOV_A0617 BCAN_B0655
80 OSP Oligosaccharide or polyol import ABC BMEII0750 BruAb20702 BRA0521 BOV_A0454 BCAN_B0520
OSP Oligosaccharide or polyol import IM BMEII0752 BruAb20704 BRA0519 BOV_A0452 BCAN_B0518
OSP Oligosaccharide or polyol import IM BMEII0753 BruAb20705 BRA0518 BOV_A0451 BCAN_B0517
OSP Oligosaccharide or polyol import BP BMEII0754 BruAb20706 BRA0516 BOV_A0449 BCAN_B0516
OSP Oligosaccharide or polyol import BP BMEII0755
81 OSP Maltose import ABC BMEII0940 BruAb20874 BRA0307 BOV_A0282 BCAN_B0308
OSP Maltose import IM BMEII0942 BruAb20875 BRA0306 BOV_A0281 BCAN_B0307
OSP Maltose import IM BMEII0943 BruAb20876 BRA0305 BOV_A0280 BCAN_B0306
OSP Maltose import BP BMEII0944 BOV_A0279
OSP Maltose import BP BMEII0945 BruAb20877 BRA0304 BCAN_B0305
82 OTCN Glycine betaine/L-proline import ABC BMEI0439, proV BruAb11568 BR1581 BOV_1526 BCAN_A1616
OTCN Glycine betaine/L-proline import IM BMEI0440, proW BruAb11567 BR1580 BOV_1525 BCAN_A1615
OTCN Glycine betaine/L-proline import BP BMEI0441, proX BruAb11566 BR1579 BOV_1524 BCAN_A1614
83 OTCN Choline SS-dependent regulation of yehZYXW BP BMEI1725 BruAb10220 BR0225 BOV_0216 BCAN_A0228
OTCN Choline SS-dependent regulation of yehZYXW IM BMEI1726, proW BruAb10217 BR1222 BOV_0215 BCAN_A0227
OTCN Choline SS-dependent regulation of yehZYXW IM BMEI1728, proW BruAb10219 BR0224 BOV_0213 BCAN_A0225
OTCN Choline SS-dependent regulation of yehZYXW ABC BMEI1727, proV BruAb10218 BR0223 BOV_0214 BCAN_A0226
84 OTCN Osmoprotectants, Taurine, Cyanante & Nitrate BP BMEI1737 BruAb10207 BR0211 BOV_0204 BCAN_A0215
OTCN Osmoprotectants, Taurine, Cyanante & Nitrate IM BMEI1739 BruAb10206 BR0213 BOV_0202 BCAN_A0213
OTCN Osmoprotectants, Taurine, Cyanante & Nitrate ABC BruAb10208
85 OTCN Taurine import BP BMEII0109 BruAb21122 BRA1186 BOV_A1089 BCAN_B1218
OTCN Taurine import IM BMEII0107, tauC BruAb21124 BRA1188 BOV_A1091 BCAN_B1219
OTCN Taurine import ABC BMEII0108, tauB BruAb21123 BRA1187 BOV_A1090 BCAN_B1217
86 OTCN Glycine betaine/L-proline import ABC BMEII0548 BruAb20492 BRA0740 BOV_A0692 BCAN_B0748
OTCN Glycine betaine/L-proline import IM BMEII0549 BruAb20493 BRA0739 BOV_A0691 BCAN_B0747
OTCN Glycine betaine/L-proline import BP BMEII0550 BruAb20494 BRA0738 BOV_A0690 BCAN_B0746
87 OTCN Nitrate import BP BMEII0797 BruAb20753 BRA0469 BOV_A0406 BCAN_B0471
OTCN Nitrate import ABC BMEII0798, nrtC BruAb20755 BRA0467 BOV_A0407 BCAN_B0470
OTCN Nitrate import IM BMEII0799, nrtB BruAb20755 BRA0468 BOV_A0408 BCAN_B0469
88 OTCN Taurine import ABC BMEII0961 BruAb10894 BRA0286 BOV_A0262 BCAN_B0288
OTCN Taurine import IM BMEII0962 BruAb10895 BRA0285 BOV_A0261 BCAN_B0287
OTCN Taurine import BP BMEII0963 BruAb10896 BRA0284 BOV_A0260 BCAN_B0286
89 PAO Polar amino acid import ABC BMEI0108 BruAb11932 BR1959 BOV_A0336 BCAN_A2004
PAO Polar amino acid import ABC BMEI0111 BruAb11935 BR1956 BOV_1885 BCAN_A2001
PAO Polar amino acid import IM BMEI0112 BruAb11931 BR1955 BOV_1882 BCAN_A2000
PAO Polar amino acid import IM BMEI0113 BruAb11930 BR1954 BOV_1081 BCAN_A1999
PAO Polar amino acid import BP BMEI0114 BruAb11929 BR1953 BOV_1880 BCAN_A1998
PAO Polar amino acid import BP BOV_1879
90 PAO Arginine/Ornithine biding protein precursor BP BruAb20594 BOV_A0594
PAO Arginine/Ornithine biding protein precursor BP BMEI1022 BruAb20595 BRA0632 BOV_A0593
PAO Arginine/Ornithine biding protein precursor BP BruAb10874 BRA0631 BOV_0945 BCAN_A0967
91 PAO General L-amino acid import ABC BMEI1208, appP BruAb10762 BR0745 BOV_A0890 BCAN_A0760
PAO General L-amino acid import IM BMEI1209, appM BruAb10758 BR0744 BOV_0739 BCAN_A0759
PAO General L-amino acid import IM BMEI1210, appQ BruAb10760 BR0743 BOV_0737 BCAN_A0758
PAO General L-amino acid import BP BMEI1211, appJ BruAb10761 BR0741 BOV_0738 BCAN_A0756
PAO General L-amino acid import BP BMEII0349, appJ BruAb20285 BRA0948 BOV_0736 BCAN_B0969
92 PAO Arginine BP BMEI1627 BruAb10321 BR0295 BOV_0308
93 PAO Cystine import ABC BMEII0599 BruAb20545 BRA0684 BOV_A0640 BCAN_B0682
PAO Cystine import IM BMEII0600 BruAb20546 BRA0683 BOV_A0639 BCAN_B0681
PAO Cystine import BP BMEII0601 BruAb20547, fliY BRA0682, fliY BOV_A0638, fliY BCAN_B0680
94 PAO Polar amino acid import IM BR0952 BCAN_A0964
PAO Polar amino acid import IM BR0953 BCAN_A0965
PAO Polar amino acid import BP BMEI1104 BR0955 BOV_0854
95 PAO Polar amino acid import BP BR0862 BOV_A0903
96 UVR DNA repair ABC2 BMEI0878 BruAb1110, UvrA UvrA BOV_1063 BCAN_A1124
97 YHBG Possible LPS transport to outer membrane ABC BMEI1790 BruAb10153 BR157 BOV_0152 BCAN_A0162
YHBG Possible LPS transport to outer membrane SS BMEI1791 BruAb10152 BR156 BOV_0151 BCAN_A0161
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ABC: ATP-Binding Cassette; IM: Inner membrane protein; BP: Binding protein; IM-ABC: Inner membrane protein-ATP binding cassette fusion; ABC2: 2 ABC proteins fused together; OMP: Outer membrane protein; MFP: Membrane fusion protein; SS: Signal sequence; LPP: Extracytoplasmic protein with a lipoprotein type signal sequence; BM: Brucella melitensis; BA: Brucella abortus; BS: Brucella suis; Bold Text: Indicates a frame shift mutation or premature stop codon in these genes.

The Brucella strains investigated in this study all have approximately 3.3 Mb genomes comprising two chromosomes of approximately 2.1 Mb and 1.2 Mb. The total number of predicted functional ABC systems encoded by the genomes of the Brucella strains is similar but does show some variability (BM = 79, BS = 72, BA = 64, BC = 74, BO = 59). Our evaluation of the Brucella genomes confirms that these species encode a relatively high proportion of ABC system genes when compared to other bacteria [39], with an average of 8.8% of their genomes dedicated to predicted functional ABC system genes (if lone components and mutated genes are included this figure increases to 9.3%). This may reflect their relatedness to environmental α-proteobacteria such as Nitrobacter and Agrobacterium which also encode high numbers of ABC systems [39] that may assist in their survival in diverse conditions.

This work reports the first full inventories of ABC systems within five genome-sequenced Brucella strains. There are a number of specific ABC systems/genes that have previously been identified in the published literature. For example, Paulsen et al. describe two ABC systems that are present in B. suis and absent in B. melitensis. The first of these is an ABC importer encoded by BR0952 (IM), BR0953 (IM), and BR0955 (BP) [9]. Although this particular system is listed in the inventory, the ABC protein component of the system was not located in the BS genome and so this system was deemed incomplete and unlikely to be functional. The system was almost completely missing from the BM genome which is consistent with the findings of Paulsen et al. [9]. The second reported system is encoded by BRA0630, BRA0631, BRA0632, BRA0633, BRA0634, and BRA0635. However, when these genes were assessed using ABCISSE, only two of the five genes were predicted to be ABC transporter binding proteins (BRA0631 and BRA0632) and no other ABC components were located. Thus we deem this system also likely to be nonfunctional. Other genes that have been identified in the literature are BRA1080 (a dipeptide ABC transporter protein indentified in BS), BMEI1742 (a mitochondrial export ABC transporter identified in BM), and BRA0749-BRA0750 (involved in oligopeptide import) [10], all of which are present in our inventories.

4. ABC System Functions

In this study, we have classified the ABC systems of BM, BS, BA, BC, and BO into classes, families, and subfamilies according to the functional classification system described by Dassa and Bouige [27] (Table 2). The Brucella strains encode 8–12 class 1 systems, characterised by an ABC-IM domain fusion and comprising predicted export systems, and 5 class 2 systems, characterised by a duplicated fused ABC and with predicted functions in antibiotic resistance and house-keeping functions. However, we have found that most of the ABC systems of Brucella species belong to class 3 with roles predicted in import processes. The further classification of Brucella ABC systems into families and subfamilies shows that there are a high number of ABC systems of specific importer families, particularly the MOI (minerals and organic ions), MOS (monosaccharide), OPN (oligopeptides and nickel), OSP (oligosaccharides and polyols), and OTCN (osmoprotectants taurine cyanate and nitrate) families, all of which primarily function to acquire nutrients.

Table 2.

ABC system families/subfamilies.

Name Description and Function
Family Subfamily
Exporters (predicted and experimental)
DPL, Drugs, Peptides, HMT Mitochondrial and bacterial transporters II
Lipids CHV Beta(1–2) Glucan export
MDL Mitochondrial and bacterial transporters I
LIP Lipid A or glycerophospholipid export
PRT Proteases, Lipases, S-Layer protein export
CYD Cytochrome bd biogenesis
CCM Cytochrome C biogenesis
CLS Capsular polysaccharide, lipopolysaccharide and teichoic acids
FAE Fatty Acid Export
Importers
DLM D- L-Methionine and derivatives
CBY CBU Cobalt uptake, putative
MKL Related to MOI family but unknown substrate
YHBG Related to HAA family, but unknown substrate
CDI Cell division
MET Metals
MOS Monosaccharides
MOI Mineral and Organic ions
PAO Polar amino acids and Opines
HAA Hydrophobic amino acids and amides
OSP Oligosaccharides and polyols
OPN Oligopeptides and Nickel
OTCN Osmoprotectants Taurine Cyanate and Nitrate
ISVH Iron-Siderophores VitaminB-12 and Hemin
cellular process (experimental)
ISB Iron-sulphur centre biogenesis
ART, Antibiotic resistance and translation regulation REG Translation regulation
UVR DNA repair and drug resistance
Unknown
DRI, Drug resistance, bacteriocin, and lantibiotic immunity YHIH Drug resistance, putative
NOS Possible nitrous oxide reduction
NO Unclassified Systems
o228 Unknown
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The predicted functionality of the ABC systems within the Brucella genomes is dominated by ABC systems involved in the import of nutrients (Figure 1), and although this is not uncommon amongst bacteria, it is probable that Brucella species utilise ABC transporters to provide most of the nutrients they require [8, 39]. In support of the findings of Paulsen et al. [9], the 2.1 Mb chromosome encodes a large proportion of the ABC systems involved in molecular export and cellular process whereas the ABC systems located on the smaller chromosome are largely biased toward nutrient acquisition, leading to the idea that this second chromosome is important in the acquisition and processing of nutrients in Brucella.

Figure 1.

Figure 1

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ABC system class/family-subfamily.

Since the ABC systems were identified by homology searches, it is possible to assign each ABC importer with a predicted substrate that it imports, providing an overview of the ABC system-based import ability of the Brucella species. Table 3 shows the range of predicted substrates imported via ABC transporters within the Brucella genomes. Overall, our results show that there is little difference in the import ability between strains of the four species of Brucella that are pathogenic to humans (BM, BS, BA, and BC). However, BO lacks the ability to import 8 of the 26 listed nutrients via ABC systems. In fact, all of the 29 pseudogenes that are present within the BO ABC system inventory occur within nutrient importers. The nutrients that BO appears to be unable to import using ABC systems include polyamines (specifically spermidine and putrescine), nickel, thiamine, glycine betaine, erythritol, xylose, and molybdenum. It is possible that the defective uptake of one or more of these substrates by B. ovis may contribute to its likely lack of virulence in humans. For example, polyamines have recently been associated with bacterial virulence and pathogenicity in human pathogens [40] and polyamine transporters have therefore been targeted as novel vaccine candidate targets for human pathogens [41, 42].

Table 3.

Brucella ABC import ability.

Substrate B. melitensis B. abortus B. suis B. ovis B. canis
Branch chain amino acids ∗∗∗∗ ∗∗∗ ∗∗∗ ∗∗ ∗∗∗
Iron (III) ∗∗∗∗ ∗∗∗∗ ∗∗∗∗ ∗∗∗∗ ∗∗∗∗
Cobalt — ∗ ∗ ∗ ∗
Zinc ∗ ∗ ∗ ∗ ∗
Thiamine ∗ ∗ ∗ — ∗
Putrescine ∗∗∗ ∗∗ ∗∗ — ∗∗
Sulphate ∗∗ ∗∗ ∗∗ ∗∗ ∗∗
Phosphate ∗ ∗ ∗ ∗ ∗
Molybdenum ∗ ∗ ∗ — ∗
Spermidine ∗∗ ∗∗ ∗ — ∗
Ribose ∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗
Galactoside — ∗∗ ∗∗ ∗∗ ∗
Xylose ∗ ∗ ∗ — ∗
Erythritol ∗ ∗ ∗ — ∗
Dipeptides ∗∗ ∗∗ ∗∗ ∗∗ ∗∗∗
Oligopeptides ∗∗∗∗ ∗∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗∗
Nickel ∗ — ∗ — ∗
Maltose ∗ ∗ ∗ ∗ ∗
Oligosaccharide or polyol ∗∗∗ ∗ ∗∗ ∗∗ ∗∗∗
SN-glycerol-3-phosphate ∗ ∗ ∗ ∗ —
Taurine ∗∗∗ ∗∗∗ ∗∗∗ ∗ ∗∗∗
Glycine betaine ∗ — ∗ — ∗
Nitrate ∗ ∗ ∗ ∗ ∗
Polar amino acids — — — ∗ ∗
Cystine ∗ ∗ ∗ ∗ ∗
General L amino acids ∗ — ∗ ∗ ∗
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This table does not include any ABC system with pseudogenes present. ****>5 functional systems, ***3 or 4 functional systems, **2 functional systems, *1 functional system, — No functional systems.

Two predicted erythritol transport systems have been reported that have yet to be confirmed by experimental data [8, 43]. Although the erythritol transporter identified in this study has also been identified by Crasta et al. [43], it should be noted that B. abortus S19 has this transport system inactivated by pseudogenes and yet it is still able to incorporate erythritol [43], indicating that this ABC system might not be wholly responsible for erythritol transport. Another study has demonstrated that B. ovis does not utilise erythritol as readily as other sugars [44].

In this study we have identified one ABC system in BM that we have categorised within a new ABC system family (currently labelled NEW1; See Table 1). This system includes BP and IM proteins related to those of the MOS family and ABC proteins that are different to those from the MOS family. We previously identified a similar ABC system in the genomes of Burkholderia pseudomallei and Burkholderia mallei strains [45]. Clearly, experimental data is required to define the function of this system.

5. Differences between Brucella Species

Although there is similarity between the ABC system inventories of the Brucella strains studied in this work, we have identified systems that are absent in one or several Brucella species (Table 4). The systems that are absent from species are not critical for bacterial survival but could contribute to differences in the lifestyles or virulence of the Brucella species. Our data shows that there are ABC systems absent from all of the Brucella strains studied. In particular, BO (5 systems), BC (4 systems), and BA (4 systems) lack systems that are present in BM and/or BS. The absence of the ISB (formally ABCX) system from BO and BC is an interesting observation since the ISB systems are soluble complexes involved in labile [Fe-S] biogenesis, which is important in resistance to oxidative stresses. This could indicate that B. ovis and B. canis reside in environments that are low in oxygen or high in oxygen reducatants, or that they lack enzymes that need labile [Fe-S] centres [46, 47]. Furthermore, this difference may be a factor contributing to the reduced virulence for humans of B. ovis and B. canis when compared to B. melitensis, B. suis, and B. abortus. The CDI system absent from B.ovis is comprised of two proteins, FtsE (ABC protein) and FtsX (IM protein) [48], and has been studied in E. coli and other bacteria including Bacillus subtilis [49] and Mycobacterium tuberculosis [50]. This CDI system is involved in cell division. E. coli mutants of ftsE show a reduced growth capacity [51]. The MKL system absent from BC may play a role in toluene tolerance, since Tn5 insertions within the ttgA2 gene coding for the MKL ABC protein in Pseudomonas putida elicited a toluene-sensitive phenotype [52].

Table 4.

ABC system genes absent in at least one species when compared to B. melitensis.

Number Family Subfamily Substrate/ Function Type B. melitensis B. abortus B. suis B. ovis B. canis
IM BMEI1851 − + + +
5 CCM Possibly heme export IM BMEI1852 − + + +
ABC BMEI1853 − + + +
6 CDI Involved in cell division IM BMEI0073, ftsX + + − +
ABC BMEI0072, ftsE + + − +
7 CLS O antigen export system ABC BMEI1416, rfbB − + + +
IM BMEI1415, rfbD − + + +
13 DPL PRT Proteases, lipase, S-layer protein export OMP BMEI1029 + − − +
14 DPL CHV Beta-(1→2) glucan export IM-ABC BMEI0984 + + − +
16 DPL HMT Involved in mitochondrial export systems IM-ABC BMEI1743 − − − −
IM-ABC BMEI1742 − − + −
22 FAE Fatty acid export IM-ABC BMEII0976 + − + +
CYTP BMEI1040 + + − −
31 ISB (ABCX) Iron/sulphur centre biogenesis CYTP BMEI1042 + + − −
ABC BMEI1041 + + − −
ABC BMEI0964 + + + −
36 MKL Involved in toluene tolerance IM BMEI0965, ttg2B + + + −
SS BMEI0963, ttg2C + + + −
IM BMEII0087 + + + −
IM BMEI0361 − − − −
60 o228 Unknown MFP BMEI0359 − − − −
ABC BMEI0360 − − − −
IM − BruAb10085 + + −
61 o228 Unknown MFP − − − − BCAN_A1712
ABC − BruAb10084 + + +
62 o228 Unknown MFP − $ $ BOV_1617 −
IM-ABC − $ $ + BCAN_A0087
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Excludes ABC systems involved in import; −: gene absent in the Brucella species; +: gene present in the Brucella species; $: pseudogene present in the Brucella species; Number: refers to ABC system number in the full inventories/alignments of Brucella ABC systems

6. Conclusions

In this study the ABC systems of B. melitensis strain 16 M, B. suis strain 1330, B. abortus 9-941, B. canis strain RM6/66, and B. ovis strain 63/290 have been reannotated using the ABCISSE database in order to provide a new and improved set of annotated Brucella ABC systems for the strains studied. The information obtained and the uniform annotation and classification of ABC systems in these closely related species has enabled a more detailed analysis of the roles of ABC systems in Brucella species, contributing to an improved understanding of Brucella lifestyle and pathogenicity. Previous analysis of the Brucella genomes has shown that there is over 90% genome similarity between the Brucella species [13, 14]. Similarly, the ABC system inventory compiled in this work reflects the close similarities of the Brucella species. However, despite the high genetic homology of Brucella, this work highlighted differences in the predicted numbers and functions of the ABC systems encoded by each Brucella species. It is widely accepted that the three species that may cause the most human brucellosis are B. melitensis, B. suis, and B. abortus (and occasionally B. canis). This study has shown that these four species of Brucella have a larger set of ABC systems encoded within their genomes than B. ovis, which is not known to cause human disease. Although it is difficult to ascertain the exact effect of the loss of these ABC systems on B. ovis, it is possible to hypothesise that, along with other genetic differences observed [15], they contribute to its overall reduced virulence in humans. It should also be noted there that four further Brucella strains have been genome sequenced since this work was completed: B. melitensis 63/9, B. abortus 2308, B. abortus S19, and B. suis Thomsen. Compiling ABC systems inventories of these strains may identify further differences between strains that may have biological relevance. Among the newly sequenced strains are B. suis Thomsen, a strain which is not known to cause disease in humans, and B. abortus S19, a vaccine strain. ABC system inventories of these strains would be of particular interest since they are considered less pathogenic than the wild-type strains and yet the reasons for this lack of pathogenicity are currently unknown. Overall, the identified differences observed in the ABC system inventory of the Brucella strains studied should contribute to a greater understanding of differences in the lifestyles of the Brucella species.

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