Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium

Abstract

During the life cycle of the filamentous bacteria Streptomyces, morphological differentiation is closely integrated with fundamental growth and cell-cycle processes, as well as with truly complex multicellular behaviour that involves hormone-like extracellular signalling and coordination with an extraordinarily diverse secondary metabolism. Not only are the bacterial cytoskeleton and the machineries for cell-wall assembly, cell division and chromosome segregation reorganized during sporulation, but the developmental programme of these fascinating organisms also has many unusual elements, including the formation of a sporulating aerial mycelium and the production of a surfactant peptide and a hydrophobic sheath that allow cells to escape from the surface tension of the growth medium.

Genome plasticity and systems evolution in Streptomyces

“…A-factor is a specific γ-butyrolactone that has been well studied in S. griseus [46]. Our analysis showed that many components in the A-factor signaling cascade are conserved in the five Streptomyces genomes, including at least seven gene families functioning in a chronological order (strep 1890, strep 2366, strep 3567, strep4078, strep2310, strep1012, and strep8592) [26]: strep1890 contains an A-factor receptor ArpA, which can block the expression of AdpA (strep3567) during the growth of vegetative mycelium. Upon the activation of A-factor biosynthesis by strep2366, A-factor is accumulated, which will release the expression of AdpA (strep3567), an ECF sigma factor that can trigger the downstream effector proteins that are essential for morphological differentiation (strep4078, strep2310, and strep1012) and secondary metabolism (strep8592) [47,48].…”

“…Streptomycetes are model organisms for developmental biology as they exhibit a complex life cycle similar to filamentous fungi, beginning with spore germination, followed by the growth of vegetative mycelium, and the formation of aerial hyphae [26]. Cell morphogenesis of streptomycetes is governed by a series of gene families such as fts, whi, ssg and mre [26].…”

“…Cell morphogenesis of streptomycetes is governed by a series of gene families such as fts, whi, ssg and mre [26]. Our analysis identified 29 gene families in the core genome that are related to cell division (GO:0051301), including the members of the fts and ssg families.…”

“…This Z-ring determines the division plane and recruits other cell division proteins [56], including FtsQ (strep3218), FtsW (strep3220), and FtsH (strep3876). The subsequent segregation of multiple copies of the linear chromosome into individual copies is regulated by ParA (strep2320), ParB (strep4045) and FtsK/SpoIIIE proteins (strep1874 and strep4996) [26,57]. Moreover, MreB (strep3403) [58] and Mcl (strep3486) [59] are classified into cell morphogenesis process (GO:0000902), both of which are involved in sporulation of the aerial hyphae.…”

“…It has also served as a model system for the study of "tissue" differentiation as a large body of work has been focused on delineating the regulatory mechanisms of morphological differentiation and tightly linked secondary metabolism [26]; (4) S. bingchenggensis produces milbemycin, an antiparasitic agent against worms, ticks and fleas used in veterinary clinics [19]; (5) S. scabiei [21], unlike the majority of streptomycetes which are non-pathogenic, is the causative agent for potato scab, a disease that is responsible for significant economic losses worldwide [21,27]. …”