Duplicated gene clusters suggest an interplay of glycogen and trehalose metabolism during sequential stages of aerial mycelium development in Streptomyces coelicolor A3(2)

Abstract

DNA sequencing and operon disruption experiments indicate that the genes glgBI and glgBII, which code for the two developmentally specific glycogen branching enzymes of Streptomyces coelicolor A3(2) each form part of larger duplicated operons consisting of at least four genes in the order pep1-treS-pep2-glgB. The sequences of the TreS proteins are 73% identical (93% similar) to that of an enzyme that converts maltose into trehalose in Pinmelobacter, a distantly related actinomycete; and the Pep1 proteins show relatedness to the alpha-amylase superfamily. Disruptions of each operon have spatially specific effects on the nature of glycogen deposits, as assessed by electron microscopy. Upstream of the glgBI operon, and diverging from it, is a gene (glgP) that encodes a protein resembling glycogen phosphorylase from Thermatoga maritima and a homologue in Mycobacterium tuberculosis. These three proteins form a distinctive subgroup compared with glycogen phosphorylases from most other bacteria, which more closely resemble the enzymes from eukaryotes. Diverging from the glgBII operon, and separated from the pep1 gene by two very small ORFs, is a gene (glgX) encoding a probable glycogen debranching enzyme. It is suggested that most of these gene products participate in the developmentally modulated interconversion of immobile, inert glycogen reservoirs, and diffusible forms of carbon, both metabolically active (e.g. glucose-1-phosphate generated by glycogen phosphorylase) and metabolically inert but physiologically significant (trehalose).

Genomics ofActinobacteria: Tracing the Evolutionary History of an Ancient Phylum

“…Probably reflecting the complex morphological and physiological differentiation of streptomycetes, their genomes contain several examples of apparent redundancy of metabolic genes. The most studied involves two nearly identical clusters (SCO5443 to -5440 and SCO7335 to -7332) that contain genes encoding functions involved in carbon storage transactions, with each cluster being specific for different hyphal cell type (51,387), but others include gene sets for enzymes of the pentose phosphate pathway (SCO1935 to -1939 and SCO6657 to -6663) and multiple fabH-like genes for the first step in fatty acid biosynthesis (several of these are associated with secondary metabolism gene sets).…”

Structure of Streptomyces Maltosyltransferase GlgE, a Homologue of a Genetically Validated Anti-tuberculosis Target

“…For example, it is involved in carbon management in Streptomyces coelicolor (13)(14)(15). The genes of this pathway are duplicated and separately and developmentally regulated in this organism, such that each is respectively associated with transient glycogen deposition at the initiation of aerial growth (phase I) and during the first stages of sporulation (phase II).…”

The interplay of glycogen metabolism and differentiation provides an insight into the developmental biology of Streptomyces coelicolor

“…In contrast, in the whiG mutant glycogen was present in nearly all cell compartments of the colony, other than young vegetative mycelium, making it impossible to recognize the two discrete phases of glycogen deposition. Here we first set out to verify these observations using a series of constructed null whi mutants, all containing the hygromycinresistance cassette (hyg), in an isogenic genetic background (J1508 was chosen because it accumulated comparatively large amounts of glycogen: Schneider et al, 2000). Thin sections of colonies that had been grown on solid medium were stained with silver proteinate to reveal polysaccharide deposits, and examined by TEM.…”

“…A search of the DNA sequence upstream of the glgBII operon (as far as the diverging coding sequence SCO7337, and including SCO7336, an uncharacterized small gene that may also be part of the operon: Schneider et al, 2000) revealed some regions similar to the consensus '210' sequence for s WhiG -dependent promoters, but we were not successful in attempts to identify the transcript of the glgBII operon, so we have yet to establish a role for these sequences. None of the potential promoter sequences was conserved in the genome of Streptomyces avermitilis (Ikeda et al, 2003).…”

“…Glycogen is virtually absent from three other cell-types: the young vegetative hyphae; the regions of aerial hyphae ('stalks') immediately below the sporulating apical compartment; and mature spores. It has been suggested that some of the carbohydrate that makes up glycogen is transferred from one phase to the next in the form of trehalose (a-1,1-linked diglucose), which is diffusible, and metabolically inert compared with sugars that retain a reducing end (Schneider et al, 2000).…”