The SEED: an Annotation/Analysis Tool Provided by FIG
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SEED version cvs.1555556707 (3/17/2019 22:5:7) on gum.mcs.anl.gov
The SEED

Subsystem: Heme,_hemin_uptake_and_utilization_systems_in_GramPositives

Author: SvetaG


Functional Roles
Column Abbrev Functional Role GO Pre-Computed Publication(s) Relevant Publication(s)
1 SiderX6 Acyl carrier protein associated with anthrachelin biosynthesis Add Publication(s)
2 Hyp? Antibiotic biosynthesis monooxygenase domain-containing protein Add Publication(s)
3 IsdA Cell surface protein IsdA, transfers heme from hemoglobin to apo-IsdC Add Publication(s)
4 IsdA1 Cell surface protein IsdA1 Add Publication(s)
5 Shp Cell surface protein Shp, transfers heme from hemoglobin to apo-SiaA/HtsA Add Publication(s)
6 IsdB Cell surface receptor IsdB for hemoglobin and hemoglobin-haptoglobin complexes Add Publication(s)
7 IsdH Cell surface receptor IsdH for hemoglobin-haptoglobin complexes Add Publication(s)
8 SiaC Heme ABC transporter (Streptococcus), ATP-binding protein Add Publication(s)
9 SiaA Heme ABC transporter (Streptococcus), heme and hemoglobin-binding protein SiaA/HtsA Add Publication(s)
10 SiaB Heme ABC transporter (Streptococcus), permease protein Add Publication(s)
11 HmuV Heme ABC transporter, ATPase component HmuV Add Publication(s)
12 HmuT Heme ABC transporter, cell surface heme and hemoprotein receptor HmuT Add Publication(s)
13 HmuU Heme ABC transporter, permease protein HmuU Add Publication(s)
14 HtsA Heme ABC type transporter HtsABC, heme-binding protein Add Publication(s)
15 HtsB Heme ABC type transporter HtsABC, permease protein HtsB Add Publication(s)
16 HtsC Heme ABC type transporter HtsABC, permease protein HtsC Add Publication(s)
17 HrtA Heme efflux system ATPase HrtA Add Publication(s)
18 HrtB Heme efflux system permease HrtB Add Publication(s)
19 HmuO Heme oxygenase (EC 1.14.99.3) Add Publication(s)
20 HemO Heme oxygenase HemO, associated with heme uptake Add Publication(s)
21 IsdE Heme transporter IsdDEF, lipoprotein IsdE Add Publication(s)
22 IsdD Heme transporter IsdDEF, membrane component IsdD Add Publication(s)
23 IsdF Heme transporter IsdDEF, permease component IsdF Add Publication(s)
24 ATPase Heme transporter analogous to IsdDEF, ATP-binding protein Add Publication(s)
25 isdG Heme-degrading cytoplasmic oxygenase IsdG Add Publication(s)
26 isdI Heme-degrading cytoplasmic oxygenase IsdI Add Publication(s)
27 ChuS Hemin transport protein HmuS Add Publication(s)
28 ChrA Hemoglobin, heme-dependent two component system response regulator ChrA Add Publication(s)
29 ChrS Hemoglobin, heme-dependent two component system sensory histidine kinase ChrS Add Publication(s)
30 HrrA Hemoglobin-dependent two component system response regulator HrrA Add Publication(s)
31 HrrS Hemoglobin-dependent two component system, sensory histidine kinase HrrS Add Publication(s)
32 DUF454 FIG039061: hypothetical protein related to heme utilization Add Publication(s)
33 SiderX4 Hypothetical protein GBAA1985 associated with anthrachelin biosynthesis, unique Add Publication(s)
34 SiderX5 Hypothetical protein GBAA1986 associated with anthrachelin biosynthesis, isomerase-like TIM barrel domain Add Publication(s)
35 Hyp2 Hypothetical similar to CcmC, putative heme lyase for CcmE Add Publication(s)
36 Hem? Hypothetical, distant similarity with heme-degrading oxygenase IsdG Add Publication(s)
37 Fe-ABC3 Iron compound ABC uptake transporter ATP-binding protein Add Publication(s)
38 PiaD Iron compound ABC uptake transporter ATP-binding protein PiaD Add Publication(s)
39 PiuD Iron compound ABC uptake transporter ATP-binding protein PiuD Add Publication(s)
40 Fe-ABC2 Iron compound ABC uptake transporter permease protein Add Publication(s)
41 PiaB Iron compound ABC uptake transporter permease protein PiaB Add Publication(s)
42 PiaC Iron compound ABC uptake transporter permease protein PiaC Add Publication(s)
43 PiuB Iron compound ABC uptake transporter permease protein PiuB Add Publication(s)
44 PiuC Iron compound ABC uptake transporter permease protein PiuC Add Publication(s)
45 Fe-ABC1 Iron compound ABC uptake transporter substrate-binding protein Add Publication(s)
46 PiaA Iron compound ABC uptake transporter substrate-binding protein PiaA Add Publication(s)
47 PiuA Iron compound ABC uptake transporter substrate-binding protein PiuA Add Publication(s)
48 DtxR Iron-dependent repressor IdeR/DtxR Add Publication(s)
49 srtA LPXTG specific sortase A Add Publication(s)
50 SiderX3 Long-chain-fatty-acid--CoA ligase associated with anthrachelin biosynthesis Add Publication(s)
51 ZnH_p2 Metallo-beta-lactamase superfamily domain protein in prophage Add Publication(s)
52 IsdC NPQTN cell wall anchored protein IsdC Add Publication(s)
53 srtB NPQTN specific sortase B 2 Publication(s) Add Publication(s)
54 spy1791 Putative ABC transporter (ATP-binding protein), spy1791 homolog Add Publication(s)
55 spy1790 Putative ABC transporter ATP-binding protein, spy1790 homolog Add Publication(s)
56 SiderX1 Putative siderophore biosynthesis protein GBAA1981 Add Publication(s)
57 SiderX2 Putative siderophore biosynthesis protein GBAA1982 Add Publication(s)
58 hrtS Sensor histidine kinase colocalized with HrtAB transporter Add Publication(s)
59 Hyp1 Similar to hypothetical protein DUF454 Add Publication(s)
60 A Sortase A, LPXTG specific Add Publication(s)
61 Shr Streptococcal cell surface hemoprotein receptor Shr Add Publication(s)
62 R Two-component response regulator SA14-24 Add Publication(s)
63 hrtR Two-component response regulator colocalized with HrtAB transporter Add Publication(s)
64 S Two-component sensor kinase SA14-24 Add Publication(s)
65 X-ABC3 Uncharacterized iron compound ABC uptake transporter, ATP-binding protein Add Publication(s)
66 X-ABC2 Uncharacterized iron compound ABC uptake transporter, permease protein Add Publication(s)
67 X-ABC1 Uncharacterized iron compound ABC uptake transporter, substrate-binding protein Add Publication(s)
68 SiderB Uncharacterized siderophore biosynthesis protein near heme transporter HtsABC Add Publication(s)
69 ZnH Zn-dependent hydrolase (beta-lactamase superfamily) Add Publication(s)

Subsets of Roles
Subset Includes These Roles
*DUF454? 32,59
*Fe_compound_ABC 45,40,37
*Heme_efflux?_HrtAB 17,18,63,58
*Heme_oxygenases 25,26,27,19,20,36
*HmuTUV 12,13,11
*HtsABC 14,15,16
*IsdA 3,4
*IsdDEF 22,21,23,24
*PiaABC 46,41,42,38
*PiuABC 47,43,44,39
*Regul 30,31,28,29,48
*SiaABC 9,10,8
*X-ABC 67,66,65
ABC_transporters 17,18,47,43,44,39,46,41,38,45,40,37
AUX 68
Corynebacteria 19,12,13,11,30,31,28,29,48
Eric 17,18,63,58,45,40,37
Isd_surface_determinant_system 7,6,3,4,52,22,21,23,24,53,25,26
Shr-Shp_SiaABC_system 61,5,9,10,8,54,55
Sortases 53,49
auxiullary 45,40,37,32,59,69,51,62,64


Show Phylogenetic Tree
Basic Spreadsheet
Genome ID Organism Variant Code SiderX6 Hyp? *IsdA Shp IsdB IsdH *SiaABC *HmuTUV *HtsABC *Heme_efflux?_HrtAB *Heme_oxygenases *IsdDEF *Regul *DUF454? SiderX4 SiderX5 Hyp2 *Fe_compound_ABC *PiaABC *PiuABC srtA SiderX3 ZnH_p2 IsdC srtB spy1791 spy1790 SiderX1 SiderX2 A Shr R S *X-ABC SiderB ZnH
644279.4 Staphylococcus aureus subsp. aureus 132 [B] 1.3     1137-3   1136 1876    
1042-14, 2315-14, 2314-15, 2313-16
2502-17, 2503-18, 2504-63, 2505-58
1143-25, 237-26
1139-22, 1140-21, 1141-23   238-32       824-45, 821-40, 822-40, 823-37     2676   2139 1138 1142             109 110   2317, 2319 113
585143.3 Staphylococcus aureus subsp. aureus 55/2053 [B] 1.3     1582-3   1581 2261    
322-14, 321-15, 320-16, 1486-14
835-17, 836-18, 837-63, 838-58
1588-25, 427-26
1584-22, 1585-21, 1586-23   428-32       1256-45, 1253-40, 1254-40, 1255-37     27     1583 1587             250 251   324, 326 254
585144.3 Staphylococcus aureus subsp. aureus 58-424 [B] 1.3     1950-3   1949 2292    
632-14, 631-15, 630-16, 1855-14
825-17, 826-18, 827-63, 828-58
1956-25, 323-26
1952-22, 1953-21, 1954-23   324-32       1614-45, 1611-40, 1612-40, 1613-37     995     1951 1955             226 227   634, 636 230
585145.3 Staphylococcus aureus subsp. aureus 65-1322 [B] 1.3     1575-3   1574 1992, 1993    
442-14, 441-15, 440-16, 1479-14
634-17, 635-18, 636-63, 637-58
1581-25, 140-26
1577-22, 1578-21, 1579-23   141-32       1244-45, 1241-40, 1242-40, 1243-37     801     1576 1580             44 45   444, 446 48
585146.3 Staphylococcus aureus subsp. aureus 68-397 [B] 1.3     1706-3   1705 2258    
12-14, 11-15, 10-16, 1484-14
264-17, 265-18, 266-63, 267-58
1712-25, 750-26
1708-22, 1709-21, 1710-23   751-32       1248-45, 1245-40, 1246-40, 1247-37     432     1707 1711             656 657   14, 16 660
585147.3 Staphylococcus aureus subsp. aureus A017934/97 [B] 1.3     612-3   611 1332, 1333    
519-14, 1733-14, 1732-15, 1731-16
1983-17, 1984-18, 1985-63, 1986-58
618-25, 2491-26
614-22, 615-21, 616-23   2492-32       328-45, 325-40, 326-40, 327-37     2155     613 617             2371 2372   1735, 1737 2375
762962.3 Staphylococcus aureus subsp. aureus ATCC 51811 [B] 1.3     936-3   937 258    
1031-14, 2333-14, 2334-15, 2335-16
2150-17, 2149-18, 2148-63, 2147-58
930-25, 1664-26
934-22, 933-21, 932-23   1663-32       1243-45, 1245-40, 1246-40, 1244-37     1982   2675 935 931             1773 1772   2329, 2331 1769
585148.3 Staphylococcus aureus subsp. aureus Btn1260 [B] 1.3     614-3   613 1309, 1310    
518-14, 1724-14, 1723-15, 1722-16
2144-17, 2145-18, 2146-63, 2147-58
620-25, 2628-26
616-22, 617-21, 618-23   2629-32       297-45, 294-40, 295-40, 296-37     2313     615 619             2532 2533   1726, 1728 2536
585149.6 Staphylococcus aureus subsp. aureus C101 [B] 1.3     1216-3   1215 1897    
1121-14, 2351-14, 2350-15, 2349-16
2537-17, 2538-18, 2539-63, 2540-58
1222-25, 314-26
1218-22, 1219-21, 1220-23   315-32       872-45, 869-40, 870-40, 871-37     2710     1217 1221             220 221   2353, 2355 224
585150.3 Staphylococcus aureus subsp. aureus C160 [B] 1.3     1640-3   1639 1984, 1985    
15-14, 14-15, 13-16, 1544-14
753-17, 754-18, 755-63, 756-58
1646-25, 254-26
1642-22, 1643-21, 1644-23   255-32       1323-45, 1320-40, 1321-40, 1322-37     923   2607 1641 1645             134 135   17, 19 138
Genome ID Organism Variant Code SiderX6 Hyp? *IsdA Shp IsdB IsdH *SiaABC *HmuTUV *HtsABC *Heme_efflux?_HrtAB *Heme_oxygenases *IsdDEF *Regul *DUF454? SiderX4 SiderX5 Hyp2 *Fe_compound_ABC *PiaABC *PiuABC srtA SiderX3 ZnH_p2 IsdC srtB spy1791 spy1790 SiderX1 SiderX2 A Shr R S *X-ABC SiderB ZnH
585151.3 Staphylococcus aureus subsp. aureus C427 [B] 1.3     669-3   668 942    
574-14, 1892-14, 1891-15, 1890-16
2346-17, 2347-18, 2348-63, 2349-58
675-25, 2019-26
671-22, 672-21, 673-23   2020-32       360-45, 357-40, 358-40, 359-37     2516   1686 670 674             2732 2733   1894, 1896 2736
93062.19 Staphylococcus aureus subsp. aureus COL [B] 1.3     1111-3   1110 1737    
1017-14, 2111-14, 2110-15, 2109-16
2301-17, 2302-18, 2303-63, 2304-58
1117-25, 150-26
1113-22, 1114-21, 1115-23   151-32       779-45, 776-40, 777-40, 778-37     2472     1112 1116             18 19   2113, 2115 22
93062.4 Staphylococcus aureus subsp. aureus COL [B] 1.3     1409-3   1408 447    
1214-14, 2196-14, 2195-15, 2194-16
2415-17, 2417-18, 2418-63, 2419-58
1513-25, 619-26
1411-22, 1412-21, 1511-23   620-32       285-45, 283-40, 282-40, 284-37     2587     1410 1512             38 39   2200, 2198 42
585152.3 Staphylococcus aureus subsp. aureus D139 [B] 1.3     979-3   978 1722    
885-14, 2149-14, 2148-15, 2147-16
2340-17, 2341-18, 2342-63, 2343-58
985-25, 81-26
981-22, 982-21, 983-23   82-32       670-45, 667-40, 668-40, 669-37     2518     980 984             2730 2731   2151, 2153 2734
585153.3 Staphylococcus aureus subsp. aureus E1410 [B] 1.3     2206-3   2205 2003    
445-14, 444-15, 443-16, 1545-14
633-17, 634-18, 635-63, 636-58
2212-25, 93-26
2208-22, 2209-21, 2210-23   94-32       1303-45, 1300-40, 1301-40, 1302-37     804     2207 2211             1026 1027   447, 449 1030
681288.4 Staphylococcus aureus subsp. aureus ED98 [B] 1.3     1100-3   1099 1743    
1005-14, 2194-14, 2193-15, 2192-16
2387-17, 2388-18, 2389-63, 2390-58
1106-25, 132-26
1102-22, 1103-21, 1104-23   133-32       699-45, 696-40, 697-40, 698-37     2557     1101 1105             18 19   2196, 2198 22
585154.3 Staphylococcus aureus subsp. aureus EMRSA16 [B] 1.3     1356-3   1355 1753, 1754    
954-14, 2236-14, 2235-15, 2234-16
2425-17, 2426-18, 2427-63, 2428-58
1362-25, 119-26
1358-22, 1359-21, 1360-23   120-32       734-45, 731-40, 732-40, 733-37     2591   2032 1357 1361             2812 2813   2238, 2239, 2241 2816
585155.3 Staphylococcus aureus subsp. aureus H19 [B] 1.3     1302-3   1301 1963, 1964    
716-14, 715-15, 714-16, 2308-14
905-17, 906-18, 907-63, 908-58
1308-25, 400-26
1304-22, 1305-21, 1306-23   401-32       1619-45, 1616-40, 1617-40, 1618-37     77     1303 1307             288 289   718, 720 292
359787.11 Staphylococcus aureus subsp. aureus JH1 [B] 1.3     1244-3   1243 1864    
1150-14, 2297-14, 2296-15, 2295-16
2486-17, 2487-18, 2488-63, 2489-58
1250-25, 188-26
1246-22, 1247-21, 1248-23   189-32       813-45, 810-40, 811-40, 812-37     2654   363, 2125 1245 1249             49 50   2299, 2301 53
Genome ID Organism Variant Code SiderX6 Hyp? *IsdA Shp IsdB IsdH *SiaABC *HmuTUV *HtsABC *Heme_efflux?_HrtAB *Heme_oxygenases *IsdDEF *Regul *DUF454? SiderX4 SiderX5 Hyp2 *Fe_compound_ABC *PiaABC *PiuABC srtA SiderX3 ZnH_p2 IsdC srtB spy1791 spy1790 SiderX1 SiderX2 A Shr R S *X-ABC SiderB ZnH
359787.3 Staphylococcus aureus subsp. aureus JH1 [B] 1.3           90     8-14, 6-15, 7-15, 5-16 1868-17, 1831-18, 1832-63, 1833-58
1585-25, 1984-26
1546-22, 1545-21, 1544-23   2036-32       2371-45, 2354-40, 2353-40, 2381-37     1014   2090 1547 1548             989 990   12, 10 949
359786.13 Staphylococcus aureus subsp. aureus JH9 [B] 1.3     1262-3   1261 1888    
1169-14, 2328-14, 2327-15, 2326-16
2523-17, 2524-18, 2525-63, 2526-58
1268-25, 191-26
1264-22, 1265-21, 1266-23   192-32       822-45, 819-40, 820-40, 821-37     2692   366, 2156 1263 1267             51 52   2330, 2332 55
359786.3 Staphylococcus aureus subsp. aureus JH9 [B] 1.3     2645-3     1658    
1468-14, 1462-15, 1463-16, 2339-14
1374-17, 1373-18, 1372-63, 1371-58
350-25, 1128-26
2647-22, 2648-21, 2649-23   1127-32       2545-45, 2544-40, 2543-40, 2546-37     1932   1545 2646 2650             2011 2012   1459, 1467 2015
585156.3 Staphylococcus aureus subsp. aureus M1015 [B] 1.3     598-3   597 1277    
503-14, 1729-14, 1728-15, 1727-16
2036-17, 2037-18, 2038-63, 2039-58
604-25, 2519-26
600-22, 601-21, 602-23   2520-32       268-45, 265-40, 266-40, 267-37     2206     599 603             2426 2427   1731, 1733 2430
585157.3 Staphylococcus aureus subsp. aureus M809 [B] 1.3     721-3   720 1455    
625-14, 1847-14, 1846-15, 1845-16
2033-17, 2034-18, 2035-63, 2036-58
727-25, 2575-26
723-22, 724-21, 725-23   2576-32       430-45, 427-40, 428-40, 429-37     2202     722 726             2480 2481   1849, 1851 2484
585158.3 Staphylococcus aureus subsp. aureus M876 [B] 1.3     1574-3   1573 2242    
223-14, 222-15, 221-16, 1473-14
412-17, 413-18, 414-63, 415-58
1580-25, 896-26
1576-22, 1577-21, 1578-23   897-32       1240-45, 1237-40, 1238-40, 1239-37     580     1575 1579             800 801   225, 227 804
585159.3 Staphylococcus aureus subsp. aureus M899 [B] 1.3     1182-3   1181 1797    
1088-14, 2280-14, 2279-15, 2278-16
2468-17, 2469-18, 2470-63, 2471-58
1188-25, 308-26
1184-22, 1185-21, 1186-23   309-32       855-45, 852-40, 853-40, 854-37     2634     1183 1187             217 218   2282, 2284 221
548470.3 Staphylococcus aureus subsp. aureus MN8 [B] 1.3     238-3   239 2525, 2526    
1171-14, 1172-15, 1173-16, 2605-14
982-17, 981-18, 980-63, 979-58
232-25, 1265-26
236-22, 235-21, 234-23   2819-32       1748-45, 1750-40, 1751-40, 1749-37     819   2031 237 233             1366 1365   1166, 1168 1362
282458.4 Staphylococcus aureus subsp. aureus MRSA252 [B] 1.3     1105-3   1104 1812, 1813    
1009-14, 2278-14, 2277-15, 2276-16
2467-17, 2468-18, 2469-63, 2470-58
1111-25, 168-26
1107-22, 1108-21, 1109-23   169-32       788-45, 785-40, 786-40, 787-37     2635   2094 1106 1110             18 19   2280, 2282 22
Genome ID Organism Variant Code SiderX6 Hyp? *IsdA Shp IsdB IsdH *SiaABC *HmuTUV *HtsABC *Heme_efflux?_HrtAB *Heme_oxygenases *IsdDEF *Regul *DUF454? SiderX4 SiderX5 Hyp2 *Fe_compound_ABC *PiaABC *PiuABC srtA SiderX3 ZnH_p2 IsdC srtB spy1791 spy1790 SiderX1 SiderX2 A Shr R S *X-ABC SiderB ZnH
282458.1 Staphylococcus aureus subsp. aureus MRSA252 [B] 1.3     1034-3   1033      
2138-14, 2137-15, 2136-16, 945-14
2315-17, 2316-18, 2317-63, 2318-58
1040-25, 155-26
1036-22, 1037-21, 1038-23   156-32       736-45, 734-40, 733-40, 735-37     2470   1967 1035 1039             18 19   2142, 2140 22
282459.5 Staphylococcus aureus subsp. aureus MSSA476 [B] 1.3     1103-3   1102 1721    
1008-14, 2160-14, 2159-15, 2158-16
2340-17, 2341-18, 2342-63, 2343-58
1109-25, 150-26
1105-22, 1106-21, 1107-23   151-32       731-45, 728-40, 729-40, 730-37     2510   1983 1104 1108             18 19   2162, 2164 22
282459.1 Staphylococcus aureus subsp. aureus MSSA476 [B] 1.3     1055-3   1054 1643    
965-14, 2053-14, 2052-15, 2051-16
2229-17, 2230-18, 2231-63, 2232-58
1061-25, 129-26
1057-22, 1058-21, 1059-23   130-32       696-45, 694-40, 693-40, 695-37     2393   1885 1056 1060             18 19   2057, 2055 22
196620.5 Staphylococcus aureus subsp. aureus MW2 [B] 1.3     1061-3   1060 1742    
966-14, 2175-14, 2174-15, 2173-16
2357-17, 2358-18, 2359-63, 2360-58
1067-25, 152-26
1063-22, 1064-21, 1065-23   153-32       735-45, 732-40, 733-40, 734-37     2526   1998 1062 1066             18 19   2177, 2179 22
196620.1 Staphylococcus aureus subsp. aureus MW2 [B] 1.3     1012-3   1011 1673    
921-14, 2103-14, 2102-15, 2101-16
2280-17, 2281-18, 2282-63, 2283-58
1018-25, 140-26
1014-22, 1015-21, 1016-23   141-32       698-45, 695-40, 696-40, 697-37     2448   1922 1013 1017             18 19   2105, 2107 22
418127.6 Staphylococcus aureus subsp. aureus Mu3 [B] 1.3     1139-3   1138 1763    
1047-14, 2219-14, 2218-15, 2217-16
2407-17, 2408-18, 2409-63, 2410-58
1145-25, 162-26
1141-22, 1142-21, 1143-23   163-32       749-45, 746-40, 747-40, 748-37     2576   2026 1140 1144             18 19   2221, 2223 22
418127.4 Staphylococcus aureus subsp. aureus Mu3 [B] 1.3     1033-3   1032 1598    
950-14, 2003-14, 2002-15, 2001-16
2166-63, 2167-58
1039-25, 148-26
1035-22, 1036-21, 1037-23           689-45, 686-40, 687-40, 688-37     2320   1828 1034 1038             17 18   2007, 2005 21
158878.14 Staphylococcus aureus subsp. aureus Mu50 [B] 1.3     1157-3   1156 1786    
1064-14, 2250-14, 2249-15, 2248-16
2442-17, 2443-18, 2444-63, 2445-58
1163-25, 163-26
1159-22, 1160-21, 1161-23   164-32       753-45, 750-40, 751-40, 752-37     2619   2055 1158 1162             18 19   2252, 2254 22
585891.3 Staphylococcus aureus subsp. aureus Mu50-omega [B] 1.3     1154-3   1153 1783    
1061-14, 2246-14, 2245-15, 2244-16
2438-17, 2439-18, 2440-63, 2441-58
1160-25, 163-26
1156-22, 1157-21, 1158-23   164-32       752-45, 749-40, 750-40, 751-37     2609   2053 1155 1159             18 19   2248, 2250 22
Genome ID Organism Variant Code SiderX6 Hyp? *IsdA Shp IsdB IsdH *SiaABC *HmuTUV *HtsABC *Heme_efflux?_HrtAB *Heme_oxygenases *IsdDEF *Regul *DUF454? SiderX4 SiderX5 Hyp2 *Fe_compound_ABC *PiaABC *PiuABC srtA SiderX3 ZnH_p2 IsdC srtB spy1791 spy1790 SiderX1 SiderX2 A Shr R S *X-ABC SiderB ZnH
158878.1 Staphylococcus aureus subsp. aureus Mu50 [B] 1.3     1130-3   1129 1731    
2177-14, 2176-15, 2175-16, 1038-14
2359-17, 2360-18, 2361-63, 2362-58
2778-25, 165-26
1132-22, 1133-21, 1134-23   166-32       736-45, 734-40, 733-40, 735-37     2528   1984 1131 1135             18 19   2181, 2179 22
158879.11 Staphylococcus aureus subsp. aureus N315 [B] 1.3     1045-3   1044 1674    
952-14, 2140-14, 2139-15, 2138-16
2333-17, 2334-18, 2335-63, 2336-58
1051-25, 165-26
1047-22, 1048-21, 1049-23   166-32       730-45, 727-40, 728-40, 729-37     2512   1941 1046 1050             18 19   2142, 2144 22
158879.1 Staphylococcus aureus subsp. aureus N315 [B] 1.3     1009-3   1008 1603    
2052-14, 2051-15, 2050-16, 919-14
2234-17, 2235-18, 2236-63, 2237-58
2680-25, 163-26
1011-22, 1012-21, 1013-23   164-32       707-45, 705-40, 704-40, 706-37     2401   1854 1010 1014             18 19   2054, 2056 22
93061.5 Staphylococcus aureus subsp. aureus NCTC 8325 [B] 1.3     991-3   990 1679    
897-14, 2193-14, 2192-15, 2191-16
2388-17, 2389-18, 2390-63, 2391-58
998-25, 122-26
993-22, 994-21, 995-23, 996-23   123-32       676-45, 673-40, 674-40, 675-37     2564     992 997             18 19   2195, 2197 22
93061.3 Staphylococcus aureus subsp. aureus NCTC 8325 [B] 1.3     1036-3   1035 1677    
938-14, 2292-14, 2291-15, 2290-16
2495-17, 2496-18, 2497-63, 2498-58
1043-25, 143-26
1038-22, 1039-21, 1041-23, 1040-23   144-32       724-45, 720-40, 719-40, 721-37     2685     1037 1042             51 52   2297, 2295 55
548474.3 Staphylococcus aureus subsp. aureus TCH130 [B] 1.3     1186-3   1187 2164    
66-14, 67-15, 68-15, 69-16, 1279-14
517-17, 516-18, 515-63, 514-58
1180-25, 4-26
1184-22, 1183-21, 1182-23   3-32       1486-45, 1488-40, 1489-40, 1487-37     348   2482 1185 1181             140 139   62, 64 136
548473.3 Staphylococcus aureus subsp. aureus TCH60 [B] 1.3     2222-3   2223 1551    
416-14, 417-15, 418-16, 2317-14
230-17, 229-18, 228-63, 227-58
2216-25, 658-26
2220-22, 2219-21, 2218-23   657-32       1187-45, 1189-40, 1190-40, 1188-37     991     2221 2217             773 772   412, 414 769
548475.3 Staphylococcus aureus subsp. aureus TCH70 [B] 1.3     1360-3   1359 715    
1268-14, 1987-14, 1988-15, 1989-16
1810-17, 1809-18, 1808-63, 1807-58
1366-25, 2252-26
1362-22, 1363-21, 1364-23   2251-32       1039-45, 1036-40, 1037-40, 1038-37     1641   2422 1361 1365             1435 1434   1983, 1985 1431
367830.3 Staphylococcus aureus subsp. aureus USA300 [B] 1.3     2273-3   2081 1017    
1507-14, 1037-14, 1036-15, 1035-16
198-17, 199-18, 200-63, 201-58
2279-25, 1458-26
2275-22, 2276-21, 2277-23   1459-32       1687-45, 1684-40, 1685-40, 1686-37     1249   2361 2274 2278             233 234   1041, 1039 525
Genome ID Organism Variant Code SiderX6 Hyp? *IsdA Shp IsdB IsdH *SiaABC *HmuTUV *HtsABC *Heme_efflux?_HrtAB *Heme_oxygenases *IsdDEF *Regul *DUF454? SiderX4 SiderX5 Hyp2 *Fe_compound_ABC *PiaABC *PiuABC srtA SiderX3 ZnH_p2 IsdC srtB spy1791 spy1790 SiderX1 SiderX2 A Shr R S *X-ABC SiderB ZnH
451515.3 Staphylococcus aureus subsp. aureus USA300_FPR3757 [B] 1.3     1127-3   1126 1828    
1033-14, 2270-14, 2269-15, 2268-16
2462-17, 2463-18, 2464-63, 2465-58
1133-25, 227-26
1129-22, 1130-21, 1131-23   228-32       798-45, 795-40, 796-40, 797-37     2638   2094 1128 1132             65 66   2272, 2274 69
451516.9 Staphylococcus aureus subsp. aureus USA300_TCH1516 [B] 1.3     1131-3   1130 1817    
1037-14, 2259-14, 2258-15, 2257-16
2451-17, 2452-18, 2453-63, 2454-58
1137-25, 216-26
1133-22, 1134-21, 1135-23   217-32       802-45, 799-40, 800-40, 801-37     2631   2084 1132 1136             51 52   2261, 2263 55
450394.6 Staphylococcus aureus subsp. aureus USA300_TCH959 [B] 1.3     320-3   319 982    
230-14, 1388-14, 1387-15, 1386-16
1860-17, 1861-18, 1862-63, 1863-58
326-25, 1925-26
322-22, 323-21, 324-23   1926-32       1299-45, 1296-40, 1297-40, 1298-37     1527   2510 321 325             1737 1738   1390, 1392 1741
585160.3 Staphylococcus aureus subsp. aureus WBG10049 [B] 1.3     596-3   595 1264    
500-14, 1664-14, 1663-15, 1662-16
2176-17, 2177-18, 2178-63, 2179-58
602-25, 1694-26
598-22, 599-21, 600-23   1695-32       262-45, 259-40, 260-40, 261-37     2347     597 601             2566 2567   1666, 1668 2570
585161.3 Staphylococcus aureus subsp. aureus WW2703/97 [B] 1.3     814-3   813 1447, 1448, 1449    
705-14, 2009-14, 2008-15, 2007-16
2230-17, 2231-18, 2232-63, 2233-58
820-25, 189-26
816-22, 817-21, 818-23   190-32       938-45, 935-40, 936-40, 937-37     2395     815 819             2578 2579   2011, 2013 2582
505321.3 Staphylococcus aureus subsp. aureus str. CF-Marseille [B] 1.3     2664-3   2665 552    
1722-14, 1723-14, 2498-14, 2497-15, 2496-16
145-17, 146-18, 147-63, 148-58
2658-25, 1836-26
2662-22, 2661-21, 2660-23   1835-32       1341-45, 1343-40, 1344-40, 1342-37     1606   447 2663 2659             2408 2409   2501, 2503 2412
546342.3 Staphylococcus aureus subsp. aureus str. JKD6008 [B] 1.3     1707-3   1708, 1709 950    
155-14, 156-15, 157-16, 1007-14
379-17, 380-18, 381-63, 382-58
1701-25, 1858-26
1705-22, 1704-21, 1703-23   1859-32       620-45, 622-40, 623-40, 621-37     1668   1240 1706 1702             2724 2723   151, 153 2720
546343.3 Staphylococcus aureus subsp. aureus str. JKD6009 [B] 1.3     486-3   487 2427    
1874-14, 2666-14, 2665-15, 2664-16
2671-17, 2672-18, 2673-63, 2674-58
479-25, 724-26
483-22, 484-22, 482-21, 481-23   725-32       445-45, 447-40, 448-40, 446-37     1993   1712 485 480             1437 1438   2668, 2670 1441
426430.8 Staphylococcus aureus subsp. aureus str. Newman [B] 1.3     1138-3   1137 1757    
981-14, 2264-14, 2263-15, 2262-16
2459-17, 2460-18, 2461-63, 2462-58
1144-25, 120-26
1140-22, 1141-21, 1142-23   121-32       761-45, 758-40, 759-40, 760-37     2634   2089 1139 1143             18 19   2266, 2268 22
Genome ID Organism Variant Code SiderX6 Hyp? *IsdA Shp IsdB IsdH *SiaABC *HmuTUV *HtsABC *Heme_efflux?_HrtAB *Heme_oxygenases *IsdDEF *Regul *DUF454? SiderX4 SiderX5 Hyp2 *Fe_compound_ABC *PiaABC *PiuABC srtA SiderX3 ZnH_p2 IsdC srtB spy1791 spy1790 SiderX1 SiderX2 A Shr R S *X-ABC SiderB ZnH
426430.6 Staphylococcus aureus subsp. aureus str. Newman [B] 1.3     1013-3   1012 1575    
2019-14, 2018-15, 2017-16, 879-14
2190-17, 2191-18, 2192-63, 2193-58
1019-25, 112-26
1015-22, 1016-21, 1017-23           692-45, 690-40, 689-40, 691-37     2348   1861 1014 1018             17 18   2021, 2023 21

Spreadsheet Options


















notes

This Subsystem (SS) encodes ONLY those heme acquisition systems  that: (i) are 
relevant for Gram-Positive organisms, and (ii) have been experimentally 
implicated in heme acquisition in at least one organism.  SS will be extended as 
new such systems are characterized.

Variant codes:

-1 = organism does not contain any Heme acquisition systems INCLUDED in THIS SS. 
 But it can contain other Heme (or Fe) uptake systems, e.g. TonB-dependent type, 
common in Gram-Negative – see SS: “Hemin transport system” 

 1 = Isd heme import machinery (prototyped in Staphylococcus) can be asserted in 
an organism:

	1.1 = putative heme efflux system HrtAB is present in addition to Isd operon

	1.2 = putative "Iron compound ABC uptake transporter" is present in addition to 
Isd operon

	1.3 = multiple additional transporters implicated in heme uptake are present

 2 = Shr-Shp-SiaABC heme import machinery (prototyped in Streptococcus) can be 
asserted in an organism

 3= no Isd or Shr-Shp-Sia genes can be detected in a genome, but the organism is 
likely capable of heme uptake, since orthologs of multiple transporters 
implicated in heme uptake can be asserted

 4 = no Isd or Shr-Shp-Sia genes can be detected in a genome, but putative heme 
efflux (?) system HrtAB appears to be present

 5 = no Isd or Shr-Shp-Sia genes can be detected in a genome, but there is a 
good possibility that organism is capable of heme uptake: Iron compound 
transporters PiaABC and PiuABC can be asserted (their orthologs have been 
implicated in heme utilization)

 6 = no Isd or Shr-Shp-Sia genes can be detected in a genome, but there is a 
slight possibility that organism is capable of heme uptake: “Iron compound 
transporter PiuABC” or/and "Iron compound ABC uptake transporter" can be 
asserted (but their orthologs in this particular organism might or might not 
recognize heme)

 7 = only heme transport system HmuTUV can be asserted, which almost always 
co-occurs with HmuO-type heme oxygenase.  Putative cases of recent HmuTUV gene 
losses are labeled as 7* or 7**.

 9 = heme oxygenase (HO) can be asserted - in the absence of clear homologs of 
any heme transporters encoded in this SS.  This can be indicative of the 
presence of: (i) heme transporters, not included in this SS (e.g. 
TonB-dependent), or (ii) novel yet unidentified heme transport systems, or (iii) 
situation in cyanobacteria where HO is required for biosynthesis of phycobilins.

____________________________________________________

Comments, open problems

1. Notably, Corynebacterium efficiens is the only Corynebact. missing HmuTUV 
cluster AND HmuO (“Heme oxygenase (EC 1.14.99.3)”), while immediate genome 
neighborhoods are very similar to those in other Corynecbacteria – genes seem to 
have been lost recently…  But from 2 different loci simultaneously??  Why?  
Could it be that – accidental - loss of HmuO determined strong selection against 
HmuTUV – to avoid toxicity of acquired heme?  Indeed, HmuO and HmuTUV almost 
always co-occur.  

Exceptions: 

(i) Propionibacterium acnes – it is missing ALL known Heme oxygenases (I 
looked), but certainly has HmuTUV.  What does it do with acquired heme? And how 
is it protected from heme toxicity?

(ii) Streptomyces avermitilis is missing HmuTUV from a locus, otherwise nearly 
identical with that in S. coelicolor (HmuO is retained - in the same locus)

2. In Firmicutes Heme efflux HtrAB system (predicted by E.Skaar) tend to have 
complementary occurrence profile to that of “Iron compound transporter PiuABC” 
OR "Iron compound ABC uptake transporter" systems with the exception of all 
Staphylococci, which contain all three).  Does it mean they have similar 
functions?? And HtrAB is not an efflux, but rather an uptake system??

References

Reniere M.L., Torres V. J., Eric P. Skaar  2007.  Intracellular metalloporphyrin 
metabolism in Staphylococcus aureus. Biometals  DOI 10.1007/s10534-006-9032-0

Skaar EP, Humayun M, Bae T, DeBord KL, Schneewind O.  Iron-source preference of 
Staphylococcus aureus infections. Science. 2004 Sep 10;305(5690):1626-8.

Skaar EP, Gaspar AH, Schneewind O (2004a) IsdG and IsdI, heme-degrading enzymes 
in the cytoplasm of  Staphylococcus aureus. J Biol Chem 279:436–443 

Skaar EP, Schneewind O.  2004b  Iron-regulated surface determinants (Isd) of 
Staphylococcus aureus: stealing iron from heme. Microbes and Infection 6 (2004) 
390–397

Bates CS, Montanez GE, Woods CR, Vincent RM, Eichenbaum Z.   Identification and 
characterization of a Streptococcus pyogenes operon involved in binding of 
hemoproteins and acquisition of iron. Infect Immun. 2003 Mar;71(3):1042-55

Drazek, E. S., C. A. Hammack, and M. P. Schmitt. 2000. Corynebacterium 
diphtheriae genes required for acquisition of iron from haemin and haemoglobin 
are homologous to ABC haemin transporters. Mol. Microbiol. 36:68–84.

PitADC:  Brown JS, Sarah M. Gilliland, Javier Ruiz-Albert, and David W. Holden. 
2002.  Characterization of Pit, a Streptococcus pneumoniae Iron Uptake ABC 
Transporter. Infection and Immunity, 70(8): 4389–4398

PiaABC,  PiuABC:  Brown JS, Gilliland SM, Holden DW.  A Streptococcus pneumoniae 
pathogenicity island encoding an ABC transporter involved in iron uptake and 
virulence. Mol Microbiol. 2001 May;40(3):572-85