Abstract
Phosphorous, in the form of phosphate, is a key element in the nutrition of all living beings. In nature, it is present in the form of phosphate salts, organophosphates, and phosphonates. Bacteria transport inorganic phosphate by the high affinity phosphate transport system PstSCAB, and the low affinity PitH transporters. The PstSCAB system consists of four components. PstS is the phosphate binding protein and discriminates between arsenate and phosphate. In the Streptomyces species, the PstS protein, attached to the outer side of the cell membrane, is glycosylated and released as a soluble protein that lacks its phosphate binding ability. Transport of phosphate by the PstSCAB system is drastically regulated by the inorganic phosphate concentration and mediated by binding of phosphorylated PhoP to the promoter of the PstSCAB operon. In Mycobacterium smegmatis, an additional high affinity transport system, PhnCDE, is also under PhoP regulation. Additionally, Streptomyces have a duplicated low affinity phosphate transport system encoded by the pitH1–pitH2 genes. In this system phosphate is transported as a metal-phosphate complex in simport with protons. Expression of pitH2, but not that of pitH1 in Streptomyces coelicolor, is regulated by PhoP. Interestingly, in many Streptomyces species, three gene clusters pitH1–pstSCAB–ppk (for a polyphosphate kinase), are linked in a supercluster formed by nine genes related to phosphate metabolism. Glycerol-3-phosphate may be transported by the actinobacteria Corynebacterium glutamicum that contains a ugp gene cluster for glycerol-3-P uptake, but the ugp cluster is not present in Streptomyces genomes. Sugar phosphates and nucleotides are used as phosphate source by the Streptomyces species, but there is no evidence of the uhp gene involved in the transport of sugar phosphates. Sugar phosphates and nucleotides are dephosphorylated by extracellular phosphatases and nucleotidases. An isolated uhpT gene for a hexose phosphate antiporter is present in several pathogenic corynebacteria, such as Corynebacterium diphtheriae, but not in non-pathogenic ones. Phosphonates are molecules that contains phosphate linked covalently to a carbon atom through a very stable C–P bond. Their utilization requires the phnCDE genes for phosphonates/phosphate transport and genes for degradation, including those for the subunits of the C–P lyase. Strains of the Arthrobacter and Streptomyces genera were reported to degrade simple phosphonates, but bioinformatic analysis reveals that whole sets of genes for putative phosphonate degradation are present only in three Arthrobacter species and a few Streptomyces species. Genes encoding the C–P lyase subunits occur in several Streptomyces species associated with plant roots or with mangroves, but not in the laboratory model Streptomyces species; however, the phnCDE genes that encode phosphonates/phosphate transport systems are frequent in Streptomyces species, suggesting that these genes, in the absence of C–P lyase genes, might be used as surrogate phosphate transporters. In summary, Streptomyces and related actinobacteria seem to be less versatile in phosphate transport systems than Enterobacteria.
Highlights
Inorganic phosphate (Pi) is a key nutrient in cell metabolism, since it is constitutive of nucleic acids, phospholipids, teichoic acids, membranes, highly phosphorylated nucleotides, and phosphorylated proteins
Taking into account all available evidence, it is concluded that actinobacteria in general lack some of the phosphate transport systems that exist in E. coli and other Enterobacteria
The high affinity PstSCAB and the low affinity duplicate Pit (PitH1–PitH2) systems are universally conserved in all studied actinobacteria including Arthrobacter, Mycobacterium, Corynebacterium, and Streptomyces species
Summary
Inorganic phosphate (Pi) is a key nutrient in cell metabolism, since it is constitutive of nucleic acids, phospholipids, teichoic acids, membranes, highly phosphorylated nucleotides, and phosphorylated proteins. Streptomyces species and related actinobacteria are prolific producers of a plethora of secondary metabolites with useful biological activities [5,6] The biosynthesis of these metabolites in Streptomyces, filamentous fungi, and plants is controlled by the phosphate concentration in the cells, reflecting the availability of phosphate in the different environments [7]. A response of Streptomyces and other microorganisms to the phosphate availability in the environment is to maintain a reservoir of phosphate in the form of polyphosphate [15,16].
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