Uniport of anionic citrate and proton consumption in citrate metabolism generates a proton motive force in Leuconostoc oenos

Ramos, António Manuel Pinho; Poolman, Berend; Santos, Helena; Lolkema, Juke S.; Konings, Wn

doi:10.1128/jb.176.16.4899-4905.1994

Cited by 54 publications

(55 citation statements)

References 27 publications

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“…The internal degradation of the substrate involves a decarboxylation step that consumes a scalar proton, which results in the formation of a pH gradient (11). The anions are taken up in exchange with a metabolic end product of the pathway (precursor/product exchange) or by a uniport mechanism, in which case the end product leaves the cell by passive diffusion.Examples of pathways using the exchange type of uptake are oxalate fermentation in Oxalobacter formigenes (1), malolactic fermentation in Lactococcus lactis (17), and histidine decarboxylation in Lactobacillus buchneri (15), and an example of a pathway using the uniporter mechanism is malate and citrate fermentation in the acidophilic bacterium Leuconostoc oenos (18,20).Cometabolism of glucose and citrate by the lactic acid bacterium Leuconostoc mesenteroides results in a growth advantage relative to growth on glucose alone. The increased growth rate is usually attributed to a metabolic shift in the heterofermentative pathway for glucose breakdown, yielding additional ATP (2, 4, 9, 21).…”

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“…Examples of pathways using the exchange type of uptake are oxalate fermentation in Oxalobacter formigenes (1), malolactic fermentation in Lactococcus lactis (17), and histidine decarboxylation in Lactobacillus buchneri (15), and an example of a pathway using the uniporter mechanism is malate and citrate fermentation in the acidophilic bacterium Leuconostoc oenos (18,20).…”

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Proton motive force generation by citrolactic fermentation in Leuconostoc mesenteroides

et al. 1996

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In Leuconostoc mesenteroides subsp. mesenteroides 19D, citrate is transported by a secondary citrate carrier (CitP). Previous studies of the kinetics and mechanism of CitP performed in membrane vesicles of L. mesenteroides showed that CitP catalyzes divalent citrate Hcit In bacteria, metabolic energy present in the form of ATP and ion gradients of H ϩ and Na ϩ are used to drive various endergonic reactions associated with cellular growth. The two forms of metabolic energy can be interconverted by the action of membrane-bound F 0 F 1 -ATPases that couple the translocation of an H ϩ (or Na ϩ ) to the hydrolysis/synthesis of ATP. In fermentative organisms, ATP is usually formed by substratelevel phosphorylation (glycolysis; arginine deaminase pathway), which is subsequently used to generate an electrochemical gradient of protons across the cytoplasmic membrane (proton motive force [pmf]) (16). Recently, a different mechanism of pmf generation was discovered that is of particular importance in the energetics of certain anaerobes and allows the F 0 F 1 -ATPase to function in the synthesis mode, i.e., the pmf drives the synthesis of ATP. The mechanism involves the action of secondary transporters and is therefore termed secondary metabolic energy generation (7). The pmf is formed indirectly during the metabolic breakdown of weak acids. The anionic forms of the acids are transported into the cell by an electrogenic secondary carrier that translocates net negative charge into the cell, generating a membrane potential. The internal degradation of the substrate involves a decarboxylation step that consumes a scalar proton, which results in the formation of a pH gradient (11). The anions are taken up in exchange with a metabolic end product of the pathway (precursor/product exchange) or by a uniport mechanism, in which case the end product leaves the cell by passive diffusion.Examples of pathways using the exchange type of uptake are oxalate fermentation in Oxalobacter formigenes (1), malolactic fermentation in Lactococcus lactis (17), and histidine decarboxylation in Lactobacillus buchneri (15), and an example of a pathway using the uniporter mechanism is malate and citrate fermentation in the acidophilic bacterium Leuconostoc oenos (18,20).Cometabolism of glucose and citrate by the lactic acid bacterium Leuconostoc mesenteroides results in a growth advantage relative to growth on glucose alone. The increased growth rate is usually attributed to a metabolic shift in the heterofermentative pathway for glucose breakdown, yielding additional ATP (2, 4, 9, 21). In the absence of citrate, acetyl-P formed from glucose is reduced to ethanol, which balances the redox equivalents produced in the other steps of the phosphoketolase pathway (see also Fig. 1). In the presence of citrate, the redox equivalents are shuttled to pyruvate produced from citrate, yielding D-lactate, and acetyl-P is converted into acetate via the acetate kinase pathway, which results in the production of ATP. In a previous study in this laboratory, the cataly...

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Proton motive force generation by citrolactic fermentation in Leuconostoc mesenteroides

et al. 1996

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“…oenos showed the same mechanism as observed for malate uptake (Ramos et al 1994). The citrate carrier catalyzes uniport of monovalent citrate H 2 cit -, implying that citrate metabolism by Lc.…”

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confidence: 73%

The generation of metabolic energy by solute transport

1995

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“…Thus, there is evidence that the processing of malate (8 -10), histidine (11), and aspartate (this work) offer cases in which a simple metabolic sequence is arranged so as to generate a proton-motive force by combining physically separated vectorial and scalar events. A more complex, ensemble model is found in Leuconostoc oenos (23), where entry of the anion, citrate 1Ϫ , is eventually coupled to a steady state proton-motive cycle by a subsequent proton-consuming metabolism. These few precedents suggest we are at the initial stages of understanding such emergent cycles and that it may be useful to consider wider application of this principle in cell biology (3,4,7).…”

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Exchange of Aspartate and Alanine

Abe

Hayashi

Maloney

1996

Journal of Biological Chemistry

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We examined the idea that aspartate metabolism by Lactobacillus subsp. M3 is organized as a proton-motive metabolic cycle by using reconstitution to monitor the activity of the carrier, termed AspT, expected to carry out the electrogenic exchange of precursor (aspartate) and product (alanine). Membranes of Lactobacillus subsp. M3 were extracted with 1.25% octyl glucoside in the presence of 0.4% Escherichia coli phospholipid and 20% glycerol. The extracts were then used to prepare proteoliposomes loaded with either aspartate or alanine. Aspartate-loaded proteoliposomes accumulated external [ 3 H]aspartate by exchange with internal substrate; this homologous self-exchange (K t ‫؍‬ 0.4 mM) was insensitive to potassium or proton ionophores and was unaffected by the presence or absence of Na Nutrient transport by bacteria is usually thought of as consuming metabolic energy, since this step is typically driven by an ion-motive gradient (e.g. ⌬ Hϩ or ⌬ Naϩ ) or by hydrolysis of a phosphoester bond (e.g. ATP or PEP) (1, 2). Recently, however, a new class of nutrient transport reactions has been identified, one in which substrate transport is actually used to generate rather than consume energy. The first and best understood of these reactions is found in Oxalobacter formigenes (3, 4), a Gram-negative, obligate anaerobe that exploits the decarboxylation of oxalate to support transmembrane ion-motive gradients (5). This cell mediates the exchange of divalent oxalate with the product of its intracellular decarboxylation, monovalent formate (6), using a membrane transporter named OxlT (4). The one-for-one exchange of oxalate 2Ϫ and formate 1Ϫ polarizes the membrane (electrically negative, inside), while the decarboxylation reaction serves to generate an internal alkalinity, since a single cytosolic proton is consumed during production of formate. As a result, the metabolic sequence, oxalate entry, oxalate decarboxylation, formate exit, acts as a proton pump (3) or "proton-motive metabolic cycle" (Refs. 3 and 4; reviewed in Ref. 7). In the same way and in other bacteria, the transport (vectorial) and decarboxylation (scalar) reactions associated with conversion of malate to lactate (8 -10) or histidine to histamine (11) have been shown to act as proton-motive metabolic cycles. Such precedents suggest a new way of interpreting the relationship between anion transport and decarboxylation reactions in microorganisms. For example, some strains of the Lactobacilli catalyze the decarboxylation of either L-aspartate 1 or L-glutamate, 2 with a near-stoichiometric release of the products, L-alanine or ␥-aminobutyrate (and CO 2 ), respectively 1, 2 . These decarboxylations support ATP synthesis in a manner consistent with the idea that processing of these anions involves a proton-motive metabolic cycle 1, 2 (and see below). As their central element, proton-motive metabolic cycles have a vectorial component(s) that mediates the electrogenic exchange of precursor and product. Accordingly, the specific goal of work reported here was to d...

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Uniport of anionic citrate and proton consumption in citrate metabolism generates a proton motive force in Leuconostoc oenos

Cited by 54 publications

References 27 publications

Proton motive force generation by citrolactic fermentation in Leuconostoc mesenteroides

Proton motive force generation by citrolactic fermentation in Leuconostoc mesenteroides

The generation of metabolic energy by solute transport

Exchange of Aspartate and Alanine

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