. 2020 Jul 18;367(15):fnaa118. doi: 10.1093/femsle/fnaa118

Table 1.

Microbial organic acid transporter proteins (experimentally verified). Table includes the transporter family, the species, the Transport Classification Database (TC number), the number of transmembrane segments (TMS), description of the transporter activity and references.

Family	Transporter protein	Species	TC number	TMS^*	Description	References
2-HCT	CimH (YxkJ)	Bacillus subtilis	2.A.24.2.4	10	Electroneutral L-Malate/Citrate:H⁺ symporter; citrate (K_m 10 μM), L-Malate (K_m 1.5 mM)	Krom, Aardema and Lolkema (2001)
	MaeN (YufR)		2.A.24.2.3	11	Malate:Na⁺ symporter	Tanaka, Kobayashi and Ogasawara (2003)
	CitS	Klebsiella pneumoniae	2.A.24.1.1	12	Sodium:Citrate symporter	Kebbel et al. (2013)
	MleP	Lactococcus lactis	2.A.24	13	Sodium:Citrate symporter; malate (K_m 0.46 mM), lactate (K_m 4.6 mM)	Bandell et al. (1997); Poolman et al. (1991); Pudlik and Lolkema (2011)
	CitP (CitN)		2.A.24.3.1	12	Electrogenic citrate:L-Lactate exchanger; citrate (K_m 56 µM), malate (K_m 0.1 mM), lactate (K_m 26 mM)	Pudlik and Lolkema (2012)
	CitP	Leuconostoc mesenteroides	2.A.24.3.2	13	Citrate:Lactate antiporter; citrate, citramalate, malate, 2-Hydroxyisobutyrate and lactate	Bandell et al. (1998); Marty-Teysset et al. (1996)
AAEx	SucE	Corynebacterium glutamicum	2.A.81.1.3	9	Succinate exporter	Fukui et al. (2011)
AceTr	SatP	Escherichia coli	2.A.96.1.1	6 in hexameric channels	Acetate, lactate and succinate transporter; acetate (K_m 1.24 mM) and succinate (K_m 1.18 mM)	Sá-Pessoa et al. (2013)
	AceP	Methanosarcina acetivorans	2.A.96.1	6	Acetate transporter; acetate (K_m 0.49 mM)	Ribas et al. (2019)
	Ady2 (Ato1)	Saccharomyces cerevisiae	2.A.96.1.4	6	Acetate permease; acetate (K_m 0.84 mM), lactate, propionate and formate	Pacheco et al. (2012); Paiva et al. (2004); Ribas et al. (2019)
	Gpr1	Yarrowia lipolytica	2.A.96.1.2	6	Acetate transporter; acetate (K_m 0.95 mM)	Augstein et al.(2003); Paiva et al. (2004); Ribas et al. (2019)
Bestrophin	Best1 (AN2251)	Aspergillus nidulans	1.A.46.2.1	4	Ca²⁺-activated anion-selective channel; citrate, propionate, benzoate and sorbate	Galagan et al.(2005); Roberts, Milnes and Caddick (2011)
CitMHS	CitM	Bacillus subtilis	2.A.11.1.1	9	Citrate or D-Isocitrate divalent metal:H⁺ symporter; (K_m 35–63 µM), metal (in order of preference): Mg²⁺, Mn²⁺, Ni²⁺, Zn²⁺ and Co²⁺	Krom et al. (2000); Li and Pajor (2002)
	CitH (CitN)		2.A.11.1.2	11	Citrate divalent metal:H⁺ symporter: (K_m 35–63 µM) metal (in order of preference): Ca²⁺, Ba²⁺ and Sr²⁺	Krom et al. (2000)
	YRAO		2.A.11.1.5	13	Citrate:H⁺ symporter	Watanabe et al. (2012)
	CitH	Corynebacterium glutamicum	2.A.11.1.6	10	Divalent cation:citrate; citrate transport in complex with Ca²⁺ or Sr²⁺	Brocker et al. (2009)
DAACS	Dct	Aspergillus carbonarius	2.A.23.1.7	9	Fumarate, L-Aspartate: symporter	Yang et al. (2017)
		Actinobacillus succinogenes	2.A.23	12	Malate and citrate exporter	Darbani et al. (2019)
	DctA	Bacillus subtilis	2.A.23.1.6	8	Dicarboxylate:H⁺ symporter; succinate (K_m 2.6 μM), fumarate	Asai et al. (2000); Groeneveld et al. (2010)
		Corynebacterium glutamicum	2.A.23	7	Dicarboxylate:H⁺ symporter; L-Malate (K_m 736 μM), fumarate (K_m 232 μM), succinate (K_m 218 μM), oxaloacetate and glyoxylate	Youn et al. (2008)
		Escherichia coli	2.A.23.1.7	8	Aerobic dicarboxylate transporter; succinate (K_m 25 µM), orotate, fumarate and L- and D-Malate	Baker et al. (1996); Karinou et al. (2013); Kay and Kornberg (1971)
DASS	DccT (DcsT)	Corynebacterium glutamicum	2.A.47.1.12	14	Aerobic sodium dicarboxylate transporter; succinate (K_m 30 μM), fumarate (K_m 79 μM), malate (K_m 360 μM) and oxaloacetate	Ebbighausen, Weil and Krämer (1991); Teramoto et al. (2008); Youn et al. (2008)
	TtdT (YgjE)	Escherichia coli	2.A.47.3.3	12	L-Tartrate:Succinate antiporter; L-Tartrate (K_m 700 µM) uptake, succinate (K_m 400 µM) efflux	Kim and Unden (2007)
	CitT		2.A.47.3.2	13	Citrate:Succinate antiporter; citrate uptake and efflux of succinate, fumarate and tartrate.	Pos, Dimroth and Bott (1998)
	SLC13	Actinobacillus succinogenes	2.A.47	14	Citrate exporter	Darbani et al. (2019)
	SdcA		2.A.47.5.3	13	Dicarboxylate: Na⁺ transporter; fumarate (K_m 536 µM) and succinate (K_m 389 µM) uptake	Rhie et al. (2014)
	SdcS	Staphylococcus aureus	2.A.47.1.11	14	Dicarboxylate: Na⁺ symporter; succinate (K_m 7 mM), malate (K_m 8 mM), fumarate (K_m 15 mM), aspartate and α-Ketoglutarate transporter	Hall and Pajor (2005); Hall and Pajor (2007)
Dcu	DcuA	Escherichia coli	2.A.13.1.1	11	Anaerobic antiporter of aspartate, malate, fumarate and succinate; uptake and efflux of fumarate	Six et al. (1994); Zientz et al. (1996)
	DcuB		2.A.13.1.2	11	Anaerobic antiporter of aspartate, malate, fumarate and succinate; uptake and efflux of fumarate and citrate exporter	Darbani et al. (2019); Kim and Unden (2007); Six et al. (1994); Zientz et al. (1996)
DcuC	DcuC	Escherichia coli	2.A.61.1.1	12	Anaerobic electroneutral C4-dicarboxylate exchanger; dicarboxylate-proton symporter; citrate exporter	Chen et al. (2014); Darbani et al. (2019); Zientz et al. (1999,1996)
DHA1	CexA	Aspergillus niger	2.A.1.2	12	Citrate exporter	Steiger et al. (2019)
FNT	FocA	Escherichia coli	1.A.16.1.1	6 in pentameric channels (PDB 3KCU)	Exporter of acetate; (K_m 23.9 mM), lactate (K_m 96 mM) and pyruvate (K_m 11.6 mM); uptake/efflux of formate (K_m 11.7 mM)	Lü et al. (2012); Wang et al. (2009)
	PfFNT	Plasmodium falciparum	1.A.16.2.7	6	Lactate:H⁺ symporter; D-Lactate, pyruvate, acetate and formate	Marchetti et al. (2015); Wu et al.(2015)
LctP	LldP	Escherichia coli	2.A.14.1.1	12	Lactate permease; L-Lactate, D-Lactate and glycolate	Núñez et al. (2001)
	GlcA (YghK)		2.A.14.1.2	13	Glycolate permease; L-Lactate, D-Lactate and glycolate	Núñez et al. (2002); Núñez et al. (2001)
	LutP	Bacillus subtilis	2.A.14.1.3	14	Lactate permease	Chai, Kolter and Losick (2009)
		Bacillus coagulans	2.A.14.1	14	Lactate permease	Wang et al. (2019)
MFS	MfsA	Aspergillus terreus	2.A.1	12	Dicarboxylate transporter; Itaconate exporter	Hossain et al. (2016); Huang et al. (2014)
	Itp1	Ustilago maydis	2.A.1	12	Itaconate exporter	Geiser et al. (2016)
MHS	Dehp2	Burkholderia caribensis	2.A.1.6.11	12	Acetate/haloacid transporter; acetate, chloroacetate, bromoacetate, 2-chloropropionate; low-affinity to glycolate, lactate and pyruvate	Su et al. (2016); Su and Tsang (2013)
	Deh4p		2.A.1.6.13	11	Acetate/Monochloroacetate (haloacid) permease; acetate (K_m 5.5 μM) and monochloroacetate (K_m 9 μM)	Su et al. (2016); Su and Tsang (2013)
NhaC	MleN (YqkI)	Bacillus subtilis	2.A.35.1.2	10	Malate:Lactate antiporter coupled with proton uptake and sodium efflux; Malic²⁻-2H⁺: Na⁺-Lactate¹⁻	Wei et al. (2000)
SHS	Jen1	Saccharomyces cerevisiae	2.A.1.12.2	12	Lactate/Pyruvate:H⁺ symporter; acetate (K_m 4.8 mM), lactate (K_m 0.2 mM), propionate, pyruvate (K_m 0.7 mM), selenite	Casal et al. (1999); McDermott, Rosen and Liu (2010); Soares-Silva et al. (2007, 2003)
	CaJen1	Candida albicans	2.A.1.12	10	Monocarboxylate permease; lactate (K_m 0.33 mM), pyruvate and propionate	Soares-Silva et al. (2004)
	CaJen2		2.A.1.12	10	Dicarboxylate permease; succinate (K_m 0.49 mM), malate (K_m 0.12 mM); affinity for the sugar acids gluconate, xylarate and mucate	Ribas et al. (2017); Vieira et al. (2010)
	DH17	Debaryomyces hansenii	2.A.1.12	12	Malate permease (K_m 0.27 mM)	Soares-Silva et al. (2015)
SHS	DH18	Debaryomyces hansenii	2.A.1.12	12	Succinate permease (K_m 0.31 mM)	Soares-Silva et al. (2015)
	DH24		2.A.1.12	12	Succinate permease (K_m 0.16 mM)	Soares-Silva et al. (2015)
	DH27		2.A.1.12	12	Acetate permease (K_m 0.94 mM)	Soares-Silva et al. (2015)
	KlJen1	Kluyveromyces lactis	2.A.1.12	12	Monocarboxylate permease; lactate (K_m 2.08 mM), pyruvate	Lodi et al. (2004); Queirós et al. (2007)
	KlJen2		2.A.1.12	11	Dicarboxylate permease; malate (K_m 0.15 mM), succinate (K_m 0.11 mM), fumarate; affinity for the sugar acids gluconate and saccharate	Lodi et al. (2004); Queirós et al. (2007); Ribas et al. (2019)
SSS	MctC	Corynebacterium glutamicum	2.A.21.7.3	13	Acetate/Propionate:H⁺ symporter; pyruvate (K_m 250 µM), acetate (Km 31 µM), propionate (K_m 9 µM)	Jolkver et al. (2009)
	ActP (YjcG)	Escherichia coli	2.A.21.7.2	13	Acetate (K_m 5.4 μM) and glyoxylate coupling ion: proton transporter, with affinity for tellurite	Elías et al. (2015); Gimenez et al. (2003)
	ActP1	Rhodobacter capsulatus	2.A.21.7.4	14	Acetate permease; acetate (K_m 1.89 mM), pyruvate, lactate, tellurite (K_m 163 μM)	Borghese et al. (2016); Borghese Cicerano and Zannoni (2011); Borghese and Zannoni (2010)
ST	KgtP (WitA)	Escherichia coli	2.A.1.6.2	12	α -Ketoglutarate (Oxoglutarate) :symporter; arabinose exporter	Koita and Rao (2012)
SulP	DauA (YchM)	Escherichia coli	2.A.53.3.11	11	Aerobic succinate transporter; succinate (K_m 0.56 mM), aspartate and fumarate	Karinou et al. (2013)
TDT	Mae1	Schizosaccharomyces pombe	2.A.16.2.1	10	Malate:H⁺ symporter; oxaloacetate, malonate, succinate, fumarate and thio-malate; exporter of fumarate, succinate and malate	Camarasa et al. (2001); Darbani et al. (2019); Grobler et al.(1995); Osawa and Matsumoto (2006)
	Ssu1	Ustilago trichophora	2.A.16	9	Malate transporter	Zambanini et al. (2017)
	Ssu2		2.A.16	9	Malate transporter	Zambanini et al. (2017)
TRAP-T	DctPQM	Rhodobacter capsulatus	2.A.56.1.1	12 (DctM) + 4 (DctQ) + receptor	Tripartite dicarboxylate: H⁺ symporter; malate (K_d 8.4 μM) competitively inhibited by fumarate (K_i 2 μM) and succinate (K_i 8 μM)	Forward et al. (1997)
TTT	TctABC	Corynebacterium glutamicum	2.A.80.1.4	12(TctA) + 4(TctB) + 1(TctC)	Citrate transport in complex with Ca²⁺ or Mg²⁺	Brocker et al. (2009)

Number of TMS predicted with the TMHMM software (http://www.cbs.dtu.dk/services/TMHMM/) or verified.

TCDB Families: 2-HCT–2-Hydroxycarboxylate Transporter; AAEx—Aspartate:Alanine Exchanger; AceTr—Acetate Uptake Transporter; Bestrophin—Anion Channel-forming Bestrophin; CitMHS—Citrate-Mg²⁺:H⁺ (CitM) Citrate-Ca²⁺:H⁺ (CitH) Symporter; DAACS—Dicarboxylate/Amino Acid:Cation (Na⁺ or H⁺) Symporter; DASS—Divalent Anion:Na⁺ Symporter; Dcu—C4-Dicarboxylate Uptake; DcuC—C4-dicarboxylate Uptake C; DHA1–Drug:H⁺ Antiporter-1; FNT—Formate-Nitrite Transporter; LctP—Lactate Permease; MFS—Major Facilitator Superfamily; MHS—Metabolite:H⁺ Symporter; NhaC—Na⁺:H⁺ Antiporter; SHS—Sialate:H⁺ Symporter; SSS—Solute:Sodium Symporter; ST—Sugar transporter; SulP—Sulfate Permease; TDT—Telurite-resistance/Dicarboxylate Transporter; TRAP-T—Tripartite ATP-independent Periplasmic Transporter; TTT—Tripartite Tricarboxylate Transporter. na—not annotated at TC Database.