The problem of hyphal growth in streptomycetes and fungi

Apical growth is the growth habit of both filamentous streptomycetes and mycelial fungi. It is also the tactic of higher plants, but only hyphal growth is considered here. The problem of apical hyphal growth is that the structure is only supported from its base giving little support to the continuously elongating tip. Clearly, a different strategy is needed for the two classes of micro-organisms because the prokaryote has no cytoskeleton to perform mechanical work, but instead has a passive exoskeleton resisting the cell's turgor pressure; i.e. it has a covalently cross-linked fabric covering the entire cell--the sacculus--that resists the cell's turgor pressure. Conversely, the lower eukaryote does have a cytoskeleton, but has no totally enclosing cross-linked fabric; rather, the hyphal wall of the eukaryotic fungi resembles fiberglass in that the wall is composed of fibers embedded in a plastic phase that gradually sets to become more rigid. Very different models are considered here for apical growth of these two classes of micro-organisms. It is proposed that the prokaryotic streptomycetes carry out a rapid turnover of the tip wall, reminiscent of the well-established inside-to-outside growth of the side wall of bacilli. This process maintains the integrity of the wall during growth because an intact covalently linked portion of the tip is always present. This model depends on the ability of the murein composing the sacculus to expand elastically. Two models are considered for the mycelial fungi, where the tip wall is enlarged by the result of fusion of vesicles. The recent model of Bartnicki-Garcia et al. (1989 Protoplasma 153, 46-57) is critically discussed. Their model is that the rate of addition to a particular element of wall area depends on its distance from an autonomously moving Spitzenkorper (idealized as the vesicle supply center, VSC, in the theoretical constructs). The three-dimensional version of their model is also analyzed. The favored model is the "soft spot hypothesis"; it is based on ideas formulated more than a century ago and recently revived independently by F. M. Harold, J. G. M. Wessels, and A. L. Koch for different reasons. It assumes that the vesicles are fused (intussuscepted) only if they reach points in the wall that are sufficiently new to be still plastic. Thus newer wall will be preferentially incorporated into fresh wall. This could provide a way for turgor pressure to facilitate the incorporation of wall materials and synthetic enzymes and couple elongation to the success of the organism in converting resources into cytoplasm. It could also provide a way for vacuole formation to force elongation. For the efficient and safe elongation of fungal hyphae there may be a role for a combination of a "vesicle supply center" and a "soft spot" model to work together.