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University of Groningen Precursor/Product Antiport In University of Groningen Precursor/product antiport in bacteria Poolman, Berend Published in: Molecular Microbiology DOI: 10.1111/j.1365-2958.1990.tb00539.x IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 1990 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Poolman, B. (1990). Precursor/product antiport in bacteria. Molecular Microbiology, 4(10), 1629-1636. DOI: 10.1111/j.1365-2958.1990.tb00539.x Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 10-02-2018 Molecular Microbiology (1990) 4(10), 1629-1636 MicroReview Precursor/product anti port in bacteria B. Poolman Δp. The main goal of this article is to review the evidence Department of Microbiology, University of Groningen, for anti port systems of metabolites in bacteria and to give Kerklaan 30, 9751 NN Haren, The Netherlands. new examples of metabolic pathways in which an antiport mechanism may be operative. These examples could be instructive for further identification of anti port systems in Summary pathways of microbial degradation and fermentation. Many microorganisms metabolize their substrates Cation anti port systems involved in the accumulation (precursors) only partially and excrete the products of and/or extrusion of inorganic cations, like the Na+/H+ the metabolism into the medium. Although uptake of anti porters, the Ca2+/H+ anti porter and others, will not be precursor and exit of product can proceed as two discussed. independent steps, there is increasing evidence that these processes are often linked and that transport is Solute antiport or exchange facilitated by a single anti port mechanism. Features of antiport mechanisms and advantages for the organ- Transport systems that mediate proton-coupled solute ism of catalysing precursor/product anti port will be transport bind the solute and proton at the outer surface of illustrated by discussing a number of well-character- the cytoplasmic membrane, and, following transmem- ized systems. Based on precursor-product conversion brane translocation, the molecules are released into the stoichiometries, structural relatedness between pre- cytoplasm (Kaback, 1983; Konings et al., 1989; Poolman cursors and products, and energetic and kinetic con- et al., 1987b). If the rate of release of the solute from the siderations, new examples of antiport systems will be carrier exceeds the rate of deprotonation and if excess proposed. solute is present in the cytoplasm, rebinding and efflux of solute can occur prior to the release of the proton. Under these conditions, the carrier protein catalyses solute/ Introduction solute exchange (or antiport) instead of solute/H+ sym- Solute transport systems in bacteria can be classified into port. The exchange reaction can be monitored by differ- three categories according to the mode of energy coupling ential labelling of the solutes in the external and internal (Konings et al., 1989): (i) primary transport systems utilize compartments. The exchange of identical solutes is chemical or light energy to translocate a molecule across termed 'homologous exchange' or 'solute self-exchange'. the cytoplasmic membrane; (ii) secondary transport sys- Solute exchange can be homologous but also hetero- tems utilize electrochemical energy for solute trans- logous (with different solutes internally and externally), location; (iii) group translocation systems couple the and can proceed independently of the magnitude and translocation to a chemical modification of the solute. For polarity of the Δp. the secondary solute transport systems the electrochemi- Although mechanistically similar to the antiport re- cal gradient for protons and/or sodium ions most often actions described below, the homologous exchange does provides the driving force for transport. In recent years, not contribute to net movement of a solute. In contrast, however, a number of transport systems have been heterologous exchange results in the accumulation of a described in which the inward movement of precursor is solute (precursor) in the cytoplasm concomitant with the directly coupled to the outward movement of product excretion of another solute (product) into the external (precursor/product antiport). Depending on the charge of medium. This type of transport, also referred to as the substrates and the stoichiometry of the anti port, the 'facilitated exchange diffusion', has been known to occur process can be independent of the proton-motive force across the inner mitochondrial membrane, the inner (Δp), the antiport can generate metabolic energy in the membrane of chloroplasts, and the vacuolar membrane of form of a Δp or the anti port can be partially driven by the yeasts (Fliege et al., 1978; Flugge and Heldt, 1986; Klingenberg, 1980; McGiven and Klingenberg, 1971; Sato Received 9 April, 1990; revised 28 May, 1990. Tel. (50) 632150; Fax (50) et al., 1984). For instance, ADP enters the mitochondrial 635205. matrix only if ATP exits into the cytosol, and vice versa. 1630 B. Poolman Since ATP has one additional negative charge relative to anti port mechanism. It is concluded that several antiport ADP, ATP/ADP exchange is driven not only by the systems used by bacteria appear to have evolved in concentration gradients of ATP and ADP but also by the specialized transport mechanisms which only catalyse Δψ (Klingenberg, 1980). The inner mitochondrial mem- exchange and not solute/cation symport. brane also contains antiport systems for dicarboxylic acids, e.g. glutamate-aspartate and malate-α-ketogluta- Arginine/ornithine antiport rate (LaNoue and Schoolwerth, 1979; Murphy et al., 1979). The arginine deiminase (ADI) pathway is widely distributed The combined action of these systems constitutes a cyclic among bacteria and serves as sole or additional source of transport pathway called the 'malate-aspartate shuttle'. energy, carbon and/or nitrogen in these organisms (Crow Besides the eukaryote organelles, an adenine nucleotide and Thomas, 1982; Cunin et al., 1986; Fenske and Kenny, exchange system has been demonstrated in the eukaryo- 1976; Pool man et al., 1987a). The ADI pathway includes: (i) tic parasite Rickettsia prowazekii (Krause et al., 1985; arginine deiminase, which catalyses the conversion of Winkler, 1976). The exchange of ATP for ADP supplies the arginine into citrulline and ammonia in an essentially parasites with a source of metabolic energy at the expense irreversible reaction (Cunin et al., 1986); (ii) ornithine of the host cell. carbamoyltransferase, which catalyses the phosphoro- Pathway intermediates are usually not abundant in the lysis of citrulline, yielding ornithine and carbamoylphos- environment of free-living bacteria, which makes anti port phate (this step is thermodynamically limiting since the mechanisms of restricted value. However, many micro- equilibrium of the reaction strongly favours the formation organisms metabolize their substrates only partially and of citrulline (K ~1 05) (Stalon, 1972; Stalon et al., 1972)); (iii) excrete the products of the metabolism into the medium. carbamate kinase, which catalyses the reversible conver- When the end-products are structurally related to the sion of carbamoylphosphate and ADP into ATP, carbon substrates (precursors), transport of both can be facil- dioxide and ammonia. In addition to these enzymatic itated by the same carrier protein. A further prerequisite for steps, the precursor and products of the ADI pathway precursor/product antiport is the stoichiometric conver- have to be translocated across the cytoplasmic mem- sion of precursor into end-product. Below (Table 1), brane (Fig. 1A). examples will be given which meet the criteria for an A number of observations have led to the suggestion Table 1. Precursor/product antiport in bacteria. Antiporter Pathway Organism Arginine/Ornithine Arginine deiminase Lactococcus lactis Streptococcus sanguis Streptococcus milleri Enterococcus faecalis Pseudomonas aeruginosa Agmatine/Putrescine Agmatine deiminase Enterococcus faecalis Sugar-phosphate/Phosphate Glycolytic Lactococcus lactis Escherichia coli Staphylococcus aureus sn-glycerol 3-phosphate/ Phosphate Glycolytic Escherichia coli PEP/Phosphate Glycolytic Salmonella typhimurium Phosphate/Phosphate - Streptococcus pyogenes Lactose/Galactose Glycolytic Streptococcus thermophilus Lactobacillus bulgaricus Oxalate/Formate Oxalate decarboxylation Oxalobacter formigenes Malate/Lactate Malolactic fermentation Leuconostoc sp. Lactobacillus sp. Lactococcus sp. Pediococcus sp. Betai ne/Di methylg Iyci ne Betaine oxidation Desulfobacterium sp. Eubacterium limosum Antiport mechanisms in bacteria 1631 Fig. 1. Bacterial antiport mechanisms. A. Arginine/ornithine antiport. Accumulation of ornithine (lysine) via the lysine
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