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- Evolution of mosaic operons by horizontal gene transfer and gene displacement in situ

Table 1

Examples of horizontally transferred operons

Operon	Recipient organism and correspondent genes	Probable source	Other probable recipients	Comment

Operon acquisition
Pyruvate:ferredoxin oxidoreductase	Thermotoga maritima TM0015-TM0018	Archaea	Aae, Hpy, Bha/Sau	Apparently, the related operon for 2-oxoisovalerate oxidoreductase (TM1758-TM1759) was also transferred from archaea
Sulfate/molybdate transport	Bacillus halodurans BH3128-BH3130	Gram-negative bacteria	-	No other such operons in Bacillus-Clostridium group members
Putative effector of murein hydrolase	Pyrococcus horikoshii PH1801-PH1802	Bacteria	Pab, Mac
Allophanate hydrolase subunits	Pyrococcus horikoshii PH0987-PH0988	Bacteria	Pab

Paralogous operon acquisition
Dipeptide transporter	Vibrio cholerae VC0620-VC0616	Thermotoga/Archaea	Tma	It has several another bacterial operons including VC1091-VC1095
Ribonucleotide reductase alpha and beta subunit	Halobacterium sp. VNG2384G VNG2383G	Bacteria	-	Additional to "archaeal:" Ribonucleotide reductase alpha subunit VNG1644G, beta subunit is apparently lost
Aromatic amino-acid biosynthesis	Halobacterium sp. VNG0384G VNG0386G	Bacteria	-	Paralogs of this pair are VNG1646G-VNG1647G

Xenologous operon displacement
Histidine biosynthesis suboperon	Pseudomonas aeruginosa PA3151-PA3152	Epsilon-Proteobacteria	-
Panthothenate synthesis	Campylobacter jejuni Cj0297c-Cj0298c	Gram-positive bacteria	-
DNA repair SbcDC	Vibrio cholerae VCA0520-VCA0521	Gram-positive bacteria	-
DNA gyrase A and B	Halobacterium sp. VNG0887G-VNG0889G	Bacteria	Hbs, Tac, Tvo, Afu,
Dipeptide transporter	Streptococcus pyogenes SPy2000-SPy2004	Gamma-Proteobacteria	-
Glutamate synthase complex	Thermotoga maritima TM0394-TM0398	Archaea	-	There is another homolog for gene TM0397 of possible archaeal origin
NADH:ubiquinone oxidoreductase	Halobacterium sp. VNG0635G-VNG0637G	Bacteria	-
Phosphate transporter	Methanothermobacter thermoautotrophicum MTH1727-MTH1734	Bacteria	-

Table 2

Examples of probable mosaic operons

Species	Predicted operon	General operon function	Horizontally acquired genes	Probable source of horizontally acquired genes	Functions of horizontally acquired genes

Cluster 1*
Rickettsia prowazekii Rickettsia conorii	RP633-661, RC0980-1008	Ribosomal operon	RP651 RC0998	Chlamydia	L29
Aquifex aeolicus	Aq001-021	Ribosomal operon	Aq018a	Archaea	L29

Cluster 2
Rickettsia prowazekii Rickettsia conorii	RP800-804, RC1234-1238	F0F1-type ATPase	RP804 RC1238 Gram-positive bacteria	Delta subunit
Ureaplasma urealyticum	UU128-138	F0F1-type ATPase	UU128, UU132_1, UU133, UU134	Gram-negative bacteria	Epsilon subunit, alpha subunit, delta subunit, delta subunit
Mycobacterium leprae	ML1139-1146	F0F1-type ATPase	ML1139	Gram-negative bacteria	A chain protein

Cluster 3
Rickettsia prowazekii Rickettsia conorii	RP134-139, RC175-180	Ribosomal proteins, transcription antiterminator, SecE	RP134 RC175	Gram-positive bacteria	Preprotein translocase subunit SecE

Cluster 5
Aquifex aeolicus	Aq1968_1_2 two domains	Histidine biosynthesis	Gram-negative bacteria	Phosphoribosyl-AMP cyclohydrolase

Cluster 8
Methanococcus jannaschii	MJ1037-1038	Tryptophan biosynthesis	MJ1037	Bacteria	Tryptophan synthase beta chain
Methanobacterium thermoautotrophicum	MTH1655-1661	Tryptophan biosynthesis	MTH1660	Gram-negative bacteria	Tryptophan synthase alpha chain
Halobacterium sp.	VNG0305-0309	Tryptophan biosynthesis	VNG0307G	Bacteria	Tryptophan synthase beta chain
Bacillus subtilis Bacillus halodurans	PabB-folK BH0090-0095	Tryptophan biosynthesis	PabB, BH0090	Gram-negative bacteria	Anthranilate/para-aminobenzoate synthases component I

Cluster 9
Halobacterium sp.	VNG0635G-0647G	NADH:ubiquinone oxidoreductase	VNG0640G	Gram-negative bacteria	NADH dehydrogenase-like protein

Cluster 18
Rickettsia prowazekii Rickettsia conorii	RP423-425, RC0588-0590	Lipid metabolism	RP425, RC0590	Spirochetes	Undecaprenyl pyrophosphate synthase

Cluster 27
Halobacterium sp.	VNG1306G-1310G	Succinate dehydrogenase/fumarate reductase	VNG1310G	Actinobacteria	Succinate dehydrogenase subunit C

Cluster 29
Mycoplasma genitalium Mycoplasma pneumoniae	MG461-466 MPN677-682	Housekeeping	MG466 MPN682	Gram-negative bacteria	Ribosomal protein L34

Cluster 34
Thermotoga maritima	TM0548-0556	Leucine/isoleucine biosynthesis	TM0552 TM0555 TM0554	2-Isopropylmalate synthase 3-Isopropylmalate dehydratase, small subunit 3-Isopropylmalate dehydratase, large subunit
Pyrococcus abyssi	PAB888-895	PAB0890 PAB0893	Bacteria	2-Isopropylmalate synthase (LeuA-1) 3-Isopropylmalate dehydrogenase (LeuB)
Clostridium acetobutylicum	CAC3169-3174	Leucine/isoleucine biosynthesis	CAC3172 CAC3173 CAC3174 Archaea	3-Isopropylmalate dehydratase, small subunit 3-Isopropylmalate dehydratase, large subunit 2-Isopropylmalate synthase

Cluster 41
Thermotoga maritima	TM1243-1251	Nucleotide metabolism	TM1243	Archaea	Phosphoribosylaminoimidazole-succinocarboxamide synthase

Cluster 42
Lactococcus lactis	L0104-0108	Arginine biosynthesis	L0107	Gram-negative bacteria	Acetylglutamate kinase
Thermotoga maritima	TM1780-1785	Arginine biosynthesis TM1784	Archaea	Acetylglutamate kinase

Cluster 48
Borrelia burgdorferi	BB0054-0061	Carbohydrate metabolism (glycolysis, gluconeogenesis)	BB0057	Gram-positive bacteria	Glyceraldehyde-3-phosphate dehydrogenase

Cluster 54
Thermotoga maritima	TM1780-1785	Arginine biosynthesis	TM1780	Gram-negative bacteria	Argininosuccinate synthase

Cluster 63
Mycoplasma pneumoniae Mycoplasma genitalium	MPN573-574 MG391-392	Molecular chaperones	MPN574 MG393	Gram-negative bacteria	Heat shock protein (groES)

Cluster 82
Mycoplasma pneumoniae, Mycoplasma genitalium	MPN535-536 MG358-359	DNA replication, recombination and repair	MPN536 MG359	Gram-negative bacteria	Holliday junction resolvasome helicase subunit
Ureaplasma urealyticum	UU448-449	DNA replication, recombination and repair	UU448	Gram-negative bacteria	Holliday junction resolvasome helicase subunit

Cluster 86
Halobacterium sp.	VNG6305CC-6306C	Tetrahydrobiopterin biosynthesis	VNG6305C	Gram-negative bacteria	Organic radical activating enzyme

Cluster 87
Halobacterium sp.	VNG0582C-0586C	Energy production and conversion	VNG0582, VNG0583G	Bacteria	Cytochrome b subunit of the bc complex Cytochrome b subunit of the bc complex

Cluster 103
Archaeoglobus fulgidus	AF0321-0325	Lipopolysaccharide biosynthesis	AF0323b	Bacteria	dTDP-4-dehydrorhamnose 3,5-epimerase and related enzymes
Deinococcus radiodurans	DRA0037-DRA0044	Lipopolysaccharide biosynthesis	DRA0044	Archaea	dTDP-4-dehydrorhamnose epimerase
Methanothermobacter thermoautotrophicus	MTH1789-1792	Lipopolysaccharide biosynthesis	MTH1789, MTH1790, MTH1791	Gram-positive bacteria Bacteria Bacteria	dTDP-D-glucose 4,6-dehydratase dTDP-4-dehydrorhamnose 3,5-epimerase dTDP-glucose pyrophosphorylase

*The numbering of gene clusters is from the previously published analysis of gene neighborhoods in prokaryotic genomes [25].

Table 3

Kishino-Hasegawa test for the analyzed cases of apparent xenologous gene displacement in situ

Tree*	Diff lnL^†	S.E.^‡	RELL-BP^§

L19 original	0.0	ML	0.8004
1R2	-12.6	7.7	0.0480
3R4	-6.6	6.6	0.1516
RuvB original	0.00	ML	0.9631
1R2	-27.1	15.4	0.0369
UppS original	0.00	ML	0.9883
1R2	-29.3	12.8	0.0117
NuoH original	0.00	ML	0.8336
1R2	-7.4	7.9	0.1664
RfbA original	0.00	ML	1.0000
1R2	-151.1	25.0	0.0000
RfbD original	0.00	ML	0.9005
1R2	-17.0	13.3	0.0995
LeuA original	0.00	ML	1.0000
1R2	-150.2	25.8	0.0000
3R4	-418.6	31.5	0.0000
5R6	-245.0	27.8	0.0000
LeuB original	0.00	ML	0.9847
1R2	-52.9	18.1	0.0007
3R4	-31.7	14.9	0.0146
LeuC original	0.00	ML	1.0000
1R2	-302.7	31.6	0.0000
3R4	-439.1	32.1	0.0000
LeuD original	0.00	ML	1.0000
1R2	-66.6	17.2	0.0000
3R4	-76.7	16.8	0.0000

*The numbers refer to local rearrangements of the tree as indicated on the corresponding figures. ^†Difference of the Log-likelihoods relative to the best tree. ^‡Standard error of Diff lnL. ^§Bootstrap probability of the given tree calculated using the RELL method (Resampling of Estimated Log-likelihoods).

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Tables - Evolution of mosaic operons by horizontal gene transfer and gene displacement in situ

Tables
- Evolution of mosaic operons by horizontal gene transfer and gene displacement in situ