A Novel Pathway for the Biosynthesis of Heme in Archaea: Genome-Based Bioinformatic Predictions and Experimental Evidence

Table 1

Heme biosynthesis genes in Archaea.

	Organism	ℎ𝑒𝑚𝐴^𝐵a	hemL	hemB	hemC	hemD	SUMT	PC2-DH	nirD	nirH	nirJ1	nirJ2	heme^b	heme 𝑑1	B12^c	siroheme^d	F430
1	Aeropyrum pernix K1	APE_2296 e	_2299.1	_2300.1	_2298.1	—	_0236.1	_1491.1	_1497.1	_1497.1	_1655	_1652	+	—	—		—	1
2	Desulfurococcus kamchatkensis 1221n	—	—	—	—	—	—	—	—	—	—	—		—			—	2
3	Ignicoccus hospitalis KIN4/I	IGNI_0512	_0683	_0324	_0684	_0090	_0089	_0483	_0839	_0839	_0397	_0630		—	—		—	3
4	Staphylothermus marinus F1	—	—	—	—	—	—	—	—	—	—	—		—	—		—	4
5	Hyperthermus butylicus DSM 5456	HBUT_0206	_0837	_1386	_0836	_0834	_0835	_0510	_0036	_0036	_0035	_0037		—	—		—	5
6	Metallosphaera sedula DSM 5348	MSED_0214	_0216	_0215	_0217	_0218	_0608	_0213	_0013	_0013	_0512	_0511		—	+	+	—	6
7	Sulfolobus acidocaldarius DSM 639	SACI_0777	_0779	_0778	_0780	_0781	_0914	_0776	_0711	_0711	—	—	+	—	+	+	—	7
8	Sulfolobus islandicus M.14.25	M1425_1955	_1953	_1954	_1952	_1951	_0226	_1956	_1894	_1894	_1048	_1047		—		+	—	8
9	Sulfolobus solfataricus P2	SSO0180	0182	0181	0183	0184	2435	—	0245	0245	1631	1632	+	—	+	+	—	9
											1840	1839
10	Sulfolobus tokodaii 7	ST0212	0215	0214	0217	0218	0563	0211	0293	0293	0127	0126	+	—	+	+	—	10
11	Thermofilum pendens Hrk 5	—	—	—	—	—	—	—	—	—	—	—		—	—	—	—	11
12	Caldivirga maquilingensis IC-167	CMAQ_1730	_1413	_1740	_1121	_1901	_1313	_1731	_0150	_0150	_1900	_1347		—	—	+	—	12
13	Pyrobaculum aerophilum IM2	PAE0601	0594	0583	0580	0589	0590	0585	0581	0581	0596	0579	+	+	+	+	—	13
14	Pyrobaculum arsenaticum DSM 13514	PARS_2261	_2254	_2247	_2245	_2250	_2251	_2248	_2246	_2246	_2255	_2244	+	+	—	+	—	14
15	Pyrobaculum calidifontis JCM 11548	PCAL_2034 _1481	_1717	_1709	_1707	_1712	_1713	_1710	_1708	_1708	_1716	_1706	+	+	+	+	—	15
16	Pyrobaculum islandicum DSM 4184	PISL_0096	_0114	_0042	_0050	_0116	_0115	_0119	_0044	_0044	_0113	_0051		—	—	+	—	16
17	Thermoproteus neutrophilus V24Sta	TNEU_1917	_1900	_0957	_0968	_1898	_1899	_1896	_0962	_0962	_1901	_0969		—		+	—	17
18	Archaeoglobus fulgidus DSM 4304	AF1975	1241	1974	1242	0116	1243	1592	1593M	1594M	2413	1125	+	—	+	+	—	18
									1594M
19	Haloarcula marismortui ATCC 43049	RRNAC1708	2628	2610	3086	3088	3087	1709	1711	1711	3489	1363	+	—	+	+	—	19
20	Halobacterium sp. NRC-1	VNG1774G	2326G	2322G	2330G	2332G	2331G	1775C	1776G	1776G	1185G	1184GM	+	—	+		—	20
21	Halomicrobium mukohataei DSM 12286	HMUK_1612	_0914	_0925	_1105	_1103	_1104	_1613	_1614	_1614	_1679	_1984	+	—		+	—	21
22	Haloquadratum walsbyi DSM 16790:HBSQ001	HQ3336A	3447A	3443A	3450A	3452A	3451A	3335A	3334A	3334A	—	—	+	—	+	+	—	22
23	Halorhabdus utahensis DSM 12940	HUTA_2825	_1970	_1362	_0927	_0928	_1761	_1755	—	—	_0031	_0734	+	—		+	—	23
24	Halorubrum lacusprofundi ATCC 49239	HLAC_2132	_2622	_0015	_2252	_2254	_2253	_2131	_2130	_2130	_1215	_2081	+	—	+	+	—	24
25	Natronomonas pharaonis DSM 2160	NP4502A	1246A	0920A	1326A	1330A	1328A	4500A	4498A	4498A	1546A	1542A	+	—	+	+	—	25
26	Methanobrevibacter smithii ATCC 35061	MSM_0967	_1233	_1476	_0881	_1504	_1550	_0968	—	—	—	—		—	+		+	26
27	Methanosphaera stadtmanae DSM 3091	MSP_1408	_1180	_0416	_1332	_1191	_1192	_1407	—	—	—	—		—	+		+	27
28	Methanothermobacter thermautotrophicus delta He	MTH1012	228	744	874	166	167	1013	—	—	—	—		—	+	+	+	28
29	Methanocaldococcus fervens AG86	MEFER_0496	_1387	_0258	_0770	_1494	_0849	_0978	—	—	—	—		—			+	29
30	Methanococcus jannaschii DSM 2661	MJ0143	0603	0643	0569	0994	0965	0140	—	—	—	—		—	+	+	+	30
31	Methanocaldococcus vulcanius M7	METVU_1458	_0867	_0542	_0749	_0380	_1448	_0492	—	—	—	—		—			+	31
32	Methanococcus aeolicus Nankai-3	MAEO_0052	_1208	_0916	_1324	_0075	_0861	_0053	—	—	—	—		—	+		+	32
33	Methanococcus maripaludis S2	MMP0088	0224	1258	0872	0394	0966	0089	—	—	—	—		—	+		+	33
34	Methanococcus vannielii SB	MEVAN_1100	_1237	_0571	_0048	_1381	_0289	_1101	—	—	—	—		—	+		+	34
35	Methanocorpusculum labreanum Z	MLAB_0523	_0525	_0524	_0526	_0073	_0526	_0522	—	—	—	—		—	+		+	35
						_0359
36	Methanoculleus marisnigri JR1	MEMAR_0980	_0982	_0981	_0983	_0539	_0984	_0979	_0878	_0877	_0879	_0876		—	+		+	36
37	Methanospirillum hungatei JF-1	MHUN_2562	_2560	_2561	_2559	_2267	_2558	_2563	—	—	—	—		—	+		+	37
38	Methanoregula boonei 6A8	MBOO_1238	_1235	_1236	_1234	_0514	_1233	_1239	_0957	_0956	_0958	_0955		—	+		+	38
39	Methanosphaerula palustris E1-9c	MPAL_1728	_1726	_1727	_1725	_2749	_1724	_1729	_2627	_2628	_2626	_2629		—			+	39
40	Methanosaeta thermophila PT	MTHE_0049	_1126	_0050	_1125	_1124	_1124	—	_1134	_0047	_1135	_1123	+	—	+		+	40
41	Methanococcoides burtonii DSM 6242	MBUR_1229	_1227	_1228	_1226	_1106	_1105	_1230	_1232	_1231	_1233	_1236	+	—	+	+	+	41
42	Methanosarcina acetivorans C2A	MA0577	0581	0578	0582	3034	3033	0576	0574	0575	0573	3035	+	—	+		+	42
43	Methanosarcina barkeri fusaro	MBAR_A1462	_A1464	_A1463	_A1465	_A1792	_A1791	_A1461	_A1459	_A1460	_A1458	_A1793	+	—	+		+	43
44	Methanosarcina mazei Goe1	MM_1741	_1743	_1742	_1744	_0308	_0307	_1740	_1738	_1739	_1737	_0309	+	—	+		+	44
45	Methanopyrus kandleri AV19	MK0200	MKT08	0198	0746	1550	1548	1495	—	—	0896	0980		—	+	+	+	45
46	Pyrococcus abyssi GE5	—	—	—	—	—	—	—	—	—	—	—		—	—		—	46
47	Pyrococcus furiosus DSM 3638	—	—	—	—	—	—	—	—	—	—	—		—	—		—	47
48	Pyrococcus horikoshii OT3	—	—	—	—	—	—	—	—	—	—	—		—	—		—	48
49	Thermococcus gammatolerans EJ3	—	—	—	—	—	—	—	—	—	—	—		—			—	49
50	Thermococcus kodakarensis KOD1	—	—	—	—	—	—	—	—	—	—	—		—	—		—	50
51	Thermococcus onnurineus NA1	—	—	—	—	—	—	—	—	—	—	—		—			—	51
52	Thermococcus sibiricus MM 739	—	—	—	—	—	—	—	—	—	—	—		—			—	52
53	Picrophilus torridus DSM 9790	PTO0918	0248	1311	0249	0250	1435	—	—	—	—	—	+	—	+		—	53
54	Thermoplasma acidophilum DSM 1728	TA0536	0571	0955	0572	0573	—	0652	—	—	—	—	+	—	+		—	54
55	Thermoplasma volcanium GSS1	TVN0590	0635	1100	0634	0633	—	0924	—	—	—	—		—	+		—	55
56	uncultured methanogenic archaeon RC-I	RCIX911	913	912	914	916	915	909	—	—	—	—		—			+	56
57	Korarchaeum cryptofilum OPF8	—	—	—	—	—	—	—	—	—	—	—		—			—	57
58	Nanoarchaeum equitans Kin4-M	—	—	—	—	—	—	—	—	—	—	—		—	—		—	58
59	Nitrosopumilus maritimus SCM1	NMAR_0510	_0490	_0509	_0491	_0493	_0492	_0511	_0512	_0512	—	—		—		+	—	59
60	Escherichia coli K-12 MG1655	B1210	0154	0369	3805	3804	3368	3368	—	—	—	—	+	—	—	+	—	60
61	Pseudomonas aeruginosa PAO1	PA4666	3977	5243	5260	5259	0510 f	2611	0515 f	0512 f	—	0511 f	+	+	+	+	—	61
62	Desulfovibrio vulgaris Hildenborough	DVU1461	3168	0856	1890	0734	0734	1463	0854	3167	0855	0857	+	—	+	+	—	62

^aℎ𝑒𝑚𝐴^𝐵 gene encoding glutamyl-tRNA reductase in the listed organisms. In the case of two or more copies for one gene, these copies are only listed if none of them is located in the gene cluster, otherwise only the copy within the cluster is listed. This is valid for all listed genes. Genes colocated within the same gene cluster in a certain species are highlighted in the same font (bold, italics, bold italics).
bOrganisms possessing heme-containing proteins according to the literature [14–22] are marked with +. For organisms with empty fields the presence of heme-containing proteins was not clearly obvious from literature and bioinformatics data.
cOrganisms possessing cobalamin biosynthesis genes according to [35] are marked with +. Organisms that do not synthesize cobalamin are marked with — [35]. For organisms with empty fields the ability to synthesize cobalamin was not obvious from the literature.
dOrganisms possessing siroheme-containing sulfite or nitrite reductases based on sequence homology are marked with +. For organisms with empty fields the presence of siroheme-containing sulfite and nitrite reductases was not clearly obvious from literature and bioinformatics data.
eNumbers represent the database gene number. The full database gene numbers including the strain abbreviation is given for the ℎ𝑒𝑚𝐴^𝐵 genes. For all other genes the database gene numbers are given without the strain abbreviation. For genes that are located as direct or near neighbors in an individual strain the numbers are written in the same font.
fP. aeruginosa nirE, nirD, nirH, and nirJ genes involved in heme 𝑑₁ biosynthesis.