A surface active protein involved in aerial hyphae formation in the filamentous fungus Schizophillum commune restores the capacity of a bald mutant of the filamentous bacterium Streptomyces coelicolor to erect aerial structures

Abstract

SummaryThe filamentous bacterium Streptomyces coelicolor undergoes a complex process of morphological differentiation involving the formation of a dense lawn of aerial hyphae that grow away from the colony surface into the air to form an aerial mycelium. Bald mutants of S. coelicolor, which are blocked in aerial mycelium formation, regain the capacity to erect aerial structures when exposed to a small hydrophobic protein called SapB, whose synthesis is temporally and spatially correlated with morphological differentiation. We now report that SapB is a surfactant that is capable of reducing the surface tension of water from 72 mJ m ¹2 to 30 mJ m ¹2 at a concentration of 50 g ml ¹1 . We also report that SapB, like the surface-active peptide streptofactin produced by the species S. tendae, was capable of restoring the capacity of bald mutants of S. tendae to erect aerial structures. Strikingly, a member (SC3) of the hydrophobin family of fungal proteins involved in the erection of aerial hyphae in the filamentous fungus Schizophyllum commune was also capable of restoring the capacity of S. coelicolor and S. tendae bald mutants to erect aerial structures. SC3 is unrelated in structure to SapB and streptofactin but, like the streptomycetes proteins, the fungal protein is a surface active agent. Scanning electron microscopy revealed that aerial structures produced in response to both the bacterial or the fungal proteins were undifferentiated vegetative hyphae that had grown away from the colony surface but had not commenced the process of spore formation. We conclude that the production of SapB and streptofactin at the start of morphological differentiation contributes to the erection of aerial hyphae by decreasing the surface tension at the colony surface but that subsequent morphogenesis requires additional developmentally regulated events under the control of bald genes.

Fruiting body formation by Bacillus subtilis

“…Surfactants are known to be important for the erection of aerial hyphae in fungi and the streptomycetes, caused at least in part by their ability to lower the surface tension of water (25)(26)(27). The phenotype of mutants unable to make surfactin is consistent with a similar role for this surfactant in B. subtilis fruiting body formation.…”

“…Mutants that do not synthesize surfactin still form ordered chains of cells, yet they fail to form mature aerial structures (sfp and srfAA). This finding represents another case of a common solution among distantly related organisms, because fungi and the streptomycetes also secrete biosurfactants that play a critical role in the development of aerial mycelia (25)(26)(27). Once aerial structures are formed, sporulation first occurs at the tips of these structures.…”

Quorum signal molecules as biosurfactants affecting swarming in Rhizobium etli

“…mirabilis population migration and in influencing cell-cell interactions was previously reported (27). Remarkable is the role of small hydrophobic proteins, SapB or the hydrophobin SC3, in the formation of Streptomyces or fungal aerial mycelia (28). QSregulated biosurfactant production via AHLs with side chains from four to six carbons has been demonstrated in Serratia liquefaciens (10), Pseudomonas aeruginosa (29,30), and possibly B. cepacia (17).…”

A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation inStreptomyces coelicolorby forming amyloid-like fibrils

“…SapB is a small peptide of 18 amino acids with a high surface activity. By lowering the water surface tension of the aqueous environment from 72 to 32 mJ/m 2 , SapB enables hyphae to overcome the physical barrier posed by the medium-air interface (Tillotson et al 1998). SapB is produced on complex agar media but not on minimal media supplemented with mannitol or arabinose (Willey et al 1991).…”

“…Application of purified SapB to growing colonies of S. coelicolor bld mutants restores the capacity to form aerial hyphae that, however, do not sporulate (Tillotson et al 1998). The vegetative nature of these aerial hyphae indicates that SapB enables hyphae to grow into the air but has no role as a signaling molecule in differentiation.…”