Table 2.

Regulation of the expression of SBPs at the transcriptional and protein levels by different ligand families and environmental cues.

SBP	Gene/ Gene associated witha	SBP family/Pfam	Species	SBP ligands	Experimental conditions	Fold change	Ref.
Amino acids and peptides
AatJ	PA1342/Ta	SBP_bac_3/PF00497	Pseudomonas aeruginosa	L-Glu	5 mM L-Glu vs 5 mM L-Arg	2.6b	[142]
					5 mM D-Glu vs 5 mM L-Arg	2.2b
AliB	spd_1357/Ta	SBP_bac_5/PF00496	Streptococcus pneumoniae	Oligopeptides	10 mM Arg vs 0.05 mM Arg	−2.9b	[143]
ApbA	spd_0109/Ta	SBP_bac_3/PF00497	S. pneumoniae	Arg	10 mM Arg vs 0.05 mM Arg	−10.1b	[143]
ArtI	artI/Ta	SBP_bac_3/PF00497	Escherichia coli	Arg, ornithine	0.6 mM Arg vs no Arg	−3.4b	[121]
					5.7 mM Arg vs no Arg	No changec	[144]
					5.0 mM ornithine vs no ornithine	No changec
ArtJ	artJ/Ta	SBP_bac_3/PF00497	E. coli	Arg	5.7 mM Arg vs no Arg	Reduced ArtJ levels in the presence of Argc	[144]
					0.6 mM Arg vs no Arg	−11.4b/-14.3d	[121]
					LB medium vs human urine (low Arg)	−16.6e	[145]
						−4.7b	[146]
Atu2422	atu2422/Ta	Peripla_BP_6/PF13458	Agrobacterium fabrum	GABA, L-Pro, L-Ala, L-Val	1 mM GABA vs no GABA	No changeb	[147]
Atu4243	atu4243/Ta	SBP_bac_8/PF13416	A. fabrum	GABA	1 mM GABA vs no GABA	No changeb	[147]
DppA	dppA/Ta	SBP_bac_5/PF00496	E. coli	Dipeptides	2% (w/v) casamino acids vs no casamino acids	Reduced DppA levels in the presence of casamino acidsc	[148]
						Reduced dppA transcript levels in the presence of casamino acidsf
					LB medium vs human urine	−4.1b	[146]
GltI	gltI/Ta	SBP_bac_3/PF00497	E. coli	Glu, Asp	LB medium vs human urine (low Arg)	−3.4b	[146]
HisJ	hisJ/Ta	SBP_bac_3/PF00497	E. coli	His, Arg	0.6 mM Arg vs no Arg	−2.5b	[121]
					0.6 mM Arg vs no Arg	-2.8d	[121]
					0.6 mM His vs no His	No changee	[91]
					LB medium vs human urine (low Arg)	−2.4b	[146]
LAO	argT/Ta	SBP_bac_3/PF00497	E. coli	Lys, Arg, ornithine	0.6 mM Arg vs no Arg	No changed	[121]
					4 g/l glucose vs 10 mg/l glucoseq	−2.5g	[108]
					1 g/l glucose vs 0.1 g/l glucoseq	−8.3b	[109]
LivJ	CJJ81176_1038/Ta	Peripla_BP_6/PF13458	Campylobacter jejuni	Leu, Ile, Val	CDM medium (0.7 mM L-Leu, 0.2 mM L-Ile, 0.9 mM L-Val) vs CDM-LIV medium (no L-Leu, L-Ile, L-Val)	No changed	[149]
LivJ	livJ/Ta	Peripla_BP_6/PF13458	E. coli	Leu, Ile, Val	0.1 mg/ml Leu vs no Leu	−25e	[150]
					LB medium vs human urine	−2.4b	[146]
LivK	livk/Ta	Peripla_BP_6/PF13458	E. coli	Leu	0.1 mg/ml Leu vs no Leu	−11.4e	[150]
MetQ	metQ/Ta	Lipoprotein_9/PF03180	E. coli	D- and L-Met	20 µg/ml L-Met vs no L-Met	−2.6e	[151]
					20 µg/ml D-Met vs no D-Met	−1.4e
MppA	mppA/-	SBP_bac_5/PF00496	E. coli	Murein peptide L-alanyl-gamma-D-glutamyl-meso-diaminopimelate	4 g/l glucose vs <10 mg/l glucose, fed-batch conditionsq	−3.0g	[108]
OppA	oppA/Ta	SBP_bac_5/PF00496	E. coli	Two and five amino acids long peptides	4 g/l glucose vs <10 mg/l glucose, fed-batch conditionsq	−2.2g	[108]
PEB1a	Cj0921c/Ta	SBP_bac_3/PF00497	C. jejuni	Asp, Glu	7.5% (v/v) O2vs 1.9% (v/v) O2q	5.6h/13.3i	[152]
Inorganic nutrients and metal ions (complexed and uncomplexed)
AioX	aioX/SPa	Phosphonate-bd/PF12974	Agrobacterium tumefaciens	As(III)	100 µM As(III) vs no As(III)	3.3j	[98]
CeuE	ceuE/Ta	Peripla_BP_2/PF01497	C. jejuni	Fe(III)-siderophore complexes	Iron replete (40 μM FeSO4) vs iron-chelated	−3.0b	[153]
					Iron replete (40 μM Fe2(SO4)3) vs iron-chelated	−16.6b	[154]
CeuE	HP_1561/Ta	Peripla_BP_2/PF01497	Helicobacter pylori	Ni-(L-His)2	0.5 mM Ni(II) vs no Ni(II)	−6.5j	[96]
					Non-chelated iron (high iron) vs iron-chelated (low iron)q	−3.5b	[155]
FatB	VV2_0842/-	Peripla_BP_2/PF01497	Vibrio vulnificus	Ferric vulnibactin	Non-chelated iron (high iron) vs iron-chelated (low iron)	−12.9h	[156]
FbpA	NGO0217/Ta	SBP_bac_1/PF01547	Neisseria gonorrhoeae	Fe(III), Ga(III)	Iron replete (100 μM Fe(NO3)3) vs iron-chelated	−6.1j	[95]
FecB	fecB/Ta	Peripla_BP_2/PF01497	E. coli	Fe(III)-citrate	High iron citrate (1 mM citrate, 100 µM Fe2SO4) vs low iron citrate (1 mM citrate, chelated iron)	−3.5e	[157]
					LB vs bovine milk (most iron is chelated or bound to proteins)	−10.6d	[158]
FepB	fepB/Ta	Peripla_BP_2/PF01497	E. coli	Ferric-enterobactin complexes	High iron (20 μM FeSO4) vs iron-chelated (low iron)	−8.3e	[159]
VcFhuD	VC0395_A2582/Ta	Peripla_BP_2/PF01497	Vibrio cholerae	Hydroxamate and catecholate type xenosiderophores	LB (high iron) vs LB + iron chelator (iron-depleted)	−12e	[160]
HbpA	hbpA/-	SBP_bac_5/PF00496	Haemophilus influenzae	Reduced and oxidized glutathione, heme, hemin	10 μg/ml heme vs heme-deficient medium	6.2d	[161]
hHbp	HD1816/Ta	ZnuA/PF01297	Haemophilus ducreyi	Heme	100 µg/ml heme vs 15 µg/ml heme	−3.9h	[162]
CpHmuT	hmuT/Ta	Peripla_BP_2/PF01497	Corynebacterium pseudotuberculosis	Heme	Non-chelated (high iron) vs iron-chelated (low iron)	−1.9j	[163]
CgHmuT	hmuT/Ta	Peripla_BP_2/PF01497	Corynebacterium glutamicum	Heme	36 μM FeSO4vs 1 μM FeSO4	−8.8b	[164]
YpHmuT	hmuT/Ta	Peripla_BP_2/PF01497	Yersinia pestis	Heme	40 μM FeCl3vs iron-chelated (low iron)	−6.8b	[165]
HtxB	htxB/Ta	No data	Pseudomonas stutzeri	Hypophosphite, phosphite	2 mM Pi vs 0.1 mM Pi	−10.6e	[166]
					2 mM Pi vs 0.1 mM phosphite	−13.2e
					2 mM Pi vs 0.1 mM hypophosphite	−17.5e
IdiA	Tery_3377/-	No data	Trichodesmium erythraeum	Fe(III)	Non-chelated (high iron) vs iron-chelated (low iron)	−50d	[167]
MntC	mntC/Ta	ZnuA/PF01297	N. gonorrhoeae	Mn(II), Zn(II)	Mn(II) excess vs Mn(II)-chelated	Increased MntC levels in the presence of ion chelatorc	[90]
ModA	modA/Ta	No data	E. coli	Molybdate, chromate, perrhenate	100 µM Mo(II) vs no Mo(II)	−36.7e	[168]
NikA	nikA/Ta	SBP_bac_5/PF00496	E. coli	Ni(II)	250 µM Ni(II) vs no Ni(II)	−5.33e	[169]
					1 µM Ni(II) vs no Ni(II)	−4.5e	[170]
					10 mM nitrate vs no nitrateq	−3.6e
NikZ	cj1584c/Ta	SBP_bac_5/(PF00496	C. jejuni	Ni(II)	500 µM Ni(II) vs no Ni(II)	NikZ was not detected in the presence of nickelk	[171]
PhnD	phnD/Ta	No data	E. coli	Phosphonate, 2-aminoethylphosphonate	2 mM Pi vs 0.2 mM Pi	−3466e	[87]
PstS	pstS/Ta	PBP_like_2/PF12849	P. aeruginosa	Pi	1 mM Pi vs 0.2 mM Pi	−223b	[51]
PstS1	Rv0934/Ta	PBP_like_2/PF12849	Mycobacterium tuberculosis	Pi	3.6 mM Pi vs Pi starvation	-2.2d	[172]
PstS3	Rv0928/Ta	PBP_like_2/PF12849	M. tuberculosis	Pi	3.6 mM Pi vs Pi starvation	−6.5d	[172]
PtxB	ptxB/Ta	No data	P. stutzeri	Pi, hypophosphite, phosphite, methylphosphonate	2 mM Pi vs 0.1 mM Pi	−15e	[166]
					2 mM Pi vs 0.1 mM phosphite	−20e
					2 mM Pi vs 0.1 mM hypophosphite	−17e
Sbp	XAC1017/Ta	No data	Xanthomonas citri	Sulfate	2 mM sulfate vs 1 mM sulfate	−1.9k	[173]
VatD	VV2_1012/Ta	Peripla_BP_2/PF01497	V. vulnificus	Ferric aerobactin, ferric vulnibactin	Non-chelated iron (high iron) vs iron-chelated (low iron)	−9.0h	[156]
ViuP	viuP/Ta	Peripla_BP_2/PF01497	V. cholerae	Ferric vibriobactin	40 µM FeSO4vs no iron	−6.1b	[174]
ZnuA	znuA/Ta	ZnuA/PF01297	E. coli	Zn(II), Co(II), Cu(II), Cu(I), Cd(II)	5 µM ZnSO4vs ZnSO4-depleted	−20e	[175]
					0.2 mM ZnSO4vs no ZnSO4	No changeb	[176]
Organic acids
AdpC	adpC (RPA4515)/SPa	TctC/PF03401	Rhodopseudomonas palustris	Adipate, 2-oxoadipate, trans-trans-muconate, pimelate, suberate, azelate	1 µM adipate vs no adipate	5.8d	[103]
					10 mM adipate vs no adipate	−2.6d
					10 mM pimelate vs no pimelate	−2.8d
					10 mM suberate vs no suberate	−10.0d
					10 mM azelate vs no azelate	−10.0d
BctC	bp3867/Ta & SPa	TctC/PF03401	Bordetella pertussis	Citrate	10 mM citrate vs no citrate	16.9e	[89]
CouP	RPA1789/Ta	Peripla_BP_6/PF13458	R. palustris	p-coumarate, ferulate, caffeate, cinnamate	3 mM p-coumarate vs 3 mM benzoate	5.7b/4.3g	[177]
MatC	RPA3494/Ta	TctC/PF03401	R. palustris	L- and D-malate, succinate, fumarate, L- and D-Met	10 mM succinate vs 3 mM p-coumarate	No changeb	[177]
					10 mM succinate vs 3 mM benzoate	No changeb
SiaP	siaP/Ta	DctP/PF03480	H. influenzae	Sialic acid, N-acetylneuraminic acid, N-glycolylneuraminic acid	0.1 mM sialic acid vs no sialic acid	3.3d,l	[178]
TarP	RPA1782/Ta	DctP/PF03480	R. palustris	p-coumarate, ferulate, caffeate, cinnamate	3 mM p-coumarate vs 10 mM succinate	2.3b/3.2g	[177]
TauA	tauA/Ta	OpuAC/PF04069	E. coli	Taurine, N-(2-acetamido)-2-aminoethanesulfonic acid, 2-(N-morpholino)ethanesulfonate	250 µM taurine vs 250 µM sulfate	143e	[88]
Polyamines and quaternary ammonium compounds
BetS	betS	BCCT/PF02028	Sinorhizobium (Ensifer) meliloti	Glycine betaine, proline betaine	1 mM glycine betaine vs no glycine betaine	No changee	[179]
					0.3 M NaCl vs no NaClq	No changee
ChoX	choX/Ta	OpuAC/PF04069	S. meliloti	Choline, acetylcholine	7 mM choline vs no choline	Increased ChoX levels in the presence of cholinec	[180]
NspS	VC0704/SPa	SBP_bac_8/Pf13416	V. cholerae	Spermidine, norspermidine, spermine	Increased vs low c-di-GMP levelsq	2.9b	[181]
OpuAC	opuAC/Ta	OpuAC/PF04069	Bacillus subtilis	Glycine betaine, proline betaine, arsenobetaine, dimethylglycine	1 mM glycine betaine vs no glycine betaine	−2.2b	[124]
					1.2 M NaCl vs no NaClq	2.1b
					0.5 M NaCl vs no NaClq	Increased transcription under osmotic stressm	[182]
PotD	potD/Ta	SBP_bac_8/Pf13416	E. coli	Spermidine, putrescine	0.1 mg/ml putrescine vs no putrescine	−2m	[183]
ProX	proX/Ta	OpuAC/PF04069	E. coli	Glycine betaine, proline betaine	0.7 M sorbitol vs no sorbitolq	10.0h	[184]
					0.4 M NaCl vs no NaClq	9.3h
					1 mM glycine betaine vs no glycine betaine	−5.7e	[123]
SpuD	spuD/Ta	SBP_bac_8/PF13416	P. aeruginosa	Putrescine	20 mM putrescine vs no putrescine	8.4e	[185]
SpuE	spuE/Ta	SBP_bac_8/PF13416	P. aeruginosa	Spermidine	20 mM spermidine vs no spermidine	14e	[185]
Mono-, oligo- and polysaccharides
AguE	TM_0432/Ta	SBP_bac_1/PF01547	Thermotoga maritima	α-1,4-digalacturonate	10 mM pectin vs 10 mM D-ribose	24b	[186]
AlgQ2	algQ2/Ta	SBP_bac_1/PF01547	Sphingomonas sp. A1	Alginate oligosaccharides	0.5% (w/v) alginate vs 0.5% (w/v) glucose	AlgQ2 was only detected in cells growing in alginatec	[187]
AraF	araF/Ta	Peripla_BP_1/PF00532	E. coli	L-Arabinose, D-arabinose, D-fucose	0.2% (w/v) arabinose vs no arabinose	27.8b	[94]
BglE	TM_0031/Ta	SBP_bac_5/PF00496	T. maritima	Cellobiose and laminaribiose	10 mM cellobiose vs 10 mM D-ribose	5b	[186]
CBP	VC_0620/Ta & SPa	SBP_bac_5/Pf00496	V. cholerae	Chitin oligosacharides ((GlcNAc)x)	0.6 mM GlcNAc vs no GlcNAc	No changeb,d	[102]
					0.6 mM (GlcNAc)2vs no (GlcNAc)2	67.9b/129d
					0.6 mM (GlcNAc)3vs no (GlcNAc)3	48.8b
					0.6 mM (GlcNAc)4vs no (GlcNAc)4	108.2b
					0.6 mM (GlcNAc)5vs no (GlcNAc)5	51.0b
					0.6 mM (GlcNAc)6vs no (GlcNAc)6	54.1b
					0.6 mM GlcN2vs no GlcN2	No changeb,d
ChvE	chvE/Ta	Peripla_BP_4/PF13407	A. tumefaciens	Galactose, glucuronic acid, galacturonic acid, arabinose and glucose	L-arabinose (3g or 5c mM) vs no L-arabinose	8e/increased ChvE levelsc	[188], [189]
					D-fucose (3g or 5c mM) vs no D-fucose	6e/increased ChvE levelsc
					D-galactose (3g or 5c mM) vs no D-galactose	5e/increased ChvE levelsc
					D-glucose (3g or 5c mM) vs no D-glucose	No changese/increased ChvE levelsc
					5 mM glucoronic acid vs no glucuronic acid	No changese
GltB	PA3190/Ta & SPa	SBP_bac_1/PF01547	P. aeruginosa	Glucose	10 mM glucose vs no glucose	64.5e	[71]
MalE	malE/Ta	SBP_bac_1/PF01547	E. coli	Maltose, maltotriose, maltetrose, maltotetraose	1 g/l glucose vs 0.1 g/l glucoseq	−67.4b	[109]
					58 mM maltose vs no maltose	~12.0/24.0e,n	[190]
					0.2% (w/v) arabinose vs no arabinose	−12.1b	[94]
MalE	lmo2125/Ta	SBP_bac_8/PF13416	Listeria monocytogenes	Maltose	25 mM maltose vs no maltose	25d	[191]
					12.5 mM maltotriose vs no maltotriose	57d
MalE1	TM_1204/Ta	SBP_bac_8/PF13416	T. maritima	Maltose, maltotriose, β-(1-4)-mannotetraose	5 g/l trehalose vs 5 g/l glucoseq	Increased expression in trehalosef	[192]
					5 g/l lactose vs 5 g/l glucoseq	Increased expression in lactosef
MalE2	TM_1839/Ta	SBP_bac_8/PF13416	T. maritima	Maltose, maltotriose, trehalose	5 g/l trehalose vs 5 g/l glucose	Increased expression in trehalosef,h	[192]
					5 g/l maltose vs 5 g/l glucose	Increased expression in maltoseh
					5 g/l maltose vs 5 g/l glucose	3.3b/26.1d	[193]
MglB (or GBP)	mglB/Ta	Peripla_BP_4/PF13407	E. coli	D-Galactose, D-glucose	0.01-10 mM galactose vs no galactose	Strong induction of mglB transcriptiono	[92]
					4 g/l glucose vs <10 mg/l glucose	−3.5g	[108]
					1 g/l glucose vs 0.1 g/l glucose	−28.0b	[109]
MglB (or GBP)	mglB/Ta	Peripla_BP_4/PF13407	Salmonella typhimurium	D-Galactose, D-glucose	2 g/l glucose vs no glucose	−5.8e	[194]
MnBP3	TM_1223/Ta	SBP_bac_5/PF00496	T. maritima	Mannose, mannobiose, cellobiose, laminaribiose, xylobiose, mannopentaose, cellopentaose, xylopentaose, laminaripentaose, mannohexaose	0.25% (w/v) mannose vs 0.25% (w/v) arabinose	Up-regulatedb	[195]
MnBP6	TM_1226/Ta	SBP_bac_5/PF00496	T. maritima	Mannose, Mannobiose, cellobiose, laminaribiose, xylobiose, mannopentaose, cellopentaose, xylopentaose, laminaripentaose, mannohexaose	0.25% (w/v) mannose vs 0.25% (w/v) arabinose	Up-regulatedb	[195]
RBP	TM_0958/Ta	Peripla_BP_4/PF13407	T. maritima	D-ribose	10 mM D-ribose vs 10 mM L-arabinose	22b	[186]
					10 mM D-ribose vs 10 mM L-trehalose	42b
RbsB	rbsB/Ta	Peripla_BP_4/PF13407	E. coli	D-ribose	10 mM D-ribose vs no D-ribose	43.8p	[93]
					4 g/l glucose vs <10 mg/l glucose	−4.4g	[108]
ThuE	thuE/Ta	SBP_bac_1/PF01547	S. meliloti	Trehalose, maltose	0.4% (w/v) trehalose vs 0.4% (w/v) sucrose	6.5e	[196]
					0.4% (w/v) maltose vs 0.4% (w/v) sucrose	No changee
XloE	TM_0071/Ta	SBP_bac_5/PF00496	T. maritima	Xylobiose, xylotriose	10 mM D-xylose vs 10 mM D-ribose	26b	[186]
YtfQ	ytfQ/Ta	Peripla_BP_4/PF13407	E. coli	Galactofuranose, arabinose, galactose, talose, allose, ribose	1 g/l glucose excess vs 0.1 g/l glucoseq	−11.4b	[109]
					4 g/l glucose vs <10 mg/l glucoseq	−7.8g	[108]
Cofactors and terminal electron acceptors
BtuF	synpcc7002_a0635/Ta	Peripla_BP_2/PF01497	Synechococcus sp. PCC 7002	Cyano-cobalamin (vitamin B12)	4 µg/L cobalamin vs no cobalamin	-18.1j	[197]
TorT	torT/SPa	Peripla_BP_1/PF00532	E. coli	Trimethylamine N-oxide (TMAO)	Anaerobic vs aerobic growthq	2.5e	[97]
Opines and quorum sensing molecules
AccA	accA/Ta	SBP_bac_5/PF00496	A. fabrum	Agrocinopine D, agrocinopine-3'-O-benzoate, agrocin 84, agrocinopine A, D-glucose-2-phosphate, L-arabinose-2-isopropylphosphate, L-arabinose-2-phosphate	20 µM agrocinopines vs no agrocinopines (under phosphate limiting conditions; 0.1 mM Pi)	4.5e	[198]
					20 µM agrocinopines vs no agrocinopines (under phosphate rich conditions; 25 mM Pi)	No changee
LuxP	luxP/SPa	Peripla_BP_4/PF13407	Vibrio harveyi	AI-2	1 µM AI-2 vs no AI-2	No changee	[199]
LsrB	lsrB/Ta	Peripla_BP_4/PF13407	E. coli	AI-2	100 µM AI-2 vs no AI-2	10.5b	[200]
LsrB	SM_b21016/Ta	Peripla_BP_4/PF13407	S. meliloti	AI-2	80 µM AI-2 vs no AI-2	13.0d	[201]
NocT	atu6027/Ta	SBP_bac_3/PF00497	A. tumefaciens	Nopaline, pyronopaline, octopine	Nopaline/pyronopaline mix (1 mM) vs no nopaline/pyronopaline	54.5b/68.1d	[202]

^aGenes associated with: T: transporter genes; SP: Signaling protein genes.

^bMicroarray data.

^cWestern blot.

^dQuantitative real-time PCR.

^eReporter gene expression.

^fNorthern hybridizations.

^gMass spectrometry proteome analysis.

^hProtein expression profiling (2D protein gels followed by mass spectrometry/peptide mass fingerprinting).

ⁱExponentially modified protein abundance index [emPAI].

^jRNA-sequencing.

^kSDS-PAGE gel analysis.

^lInduction was only observed in a nanAsiaB double mutant that can neither catabolize nor activate sialic acid.

^mPrimer extension analyses.

ⁿLowest and highest fold-change values measured at the different pH values ranging from 4.75 to 5.75.

^oIn vitro transcription assays.

^pGenomic SELEX screenings.

^qRegulation mediated by non-cognate ligands or by environmental cues associated with SBP function.