Bacillus subtilis YqkI is a novel malic/Na⁺-lactate antiporter that enhances growth on malate at low protonmotive force

Bacillus subtilis yheL encodes a Na⁺/H⁺ antiporter, whereas its paralogue, yqkI, encodes a novel antiporter that achieves a simultaneous Na⁺/H⁺ and malolactate antiport. B. subtilis yufR, a control in some experiments, encodes a Na⁺/malate symporter. YqkI complemented a malate transport mutant of Escherichia coli if Na⁺ and lactate were present. YheL conferred Na⁺ uptake capacity on everted membrane vesicles from an antiporter-deficient E. coli mutant that was consistent with a secondary Na⁺/H⁺ antiport, but YqkI-dependent Na⁺ uptake depended on intravesicular malate and extravesicular lactate. YqkI-dependent lactate uptake depended on intravesicular malate and extravesicular Na⁺. YqkI mediated an electroneutral exchange, which is proposed to be a malic^-2-2H⁺ (or fully protonated malate)/Na⁺-lactate^-1 antiport. Because the composite YqkI-mediated exchanges could be driven by gradients of the malate-lactate pair, this transporter could play a role in growth of B. subtilis on malate at low protonmotive force. A mutant with a disruption of yqkI exhibited an abrupt arrest in the mid-logarithmic phase of growth on malate when low concentrations of protonophore were present. Thus growth of B. subtilis to high density on a putatively nonfermentative dicarboxylic acid substrate depends on a malolactate exchange at suboptimal protonmotive force.