Mycoplasma pneumoniae, an underutilized model for bacterial cell biology

Abstract

In recent decades, bacterial cell biology has seen great advances, and numerous model systems have been developed to study a wide variety of cellular processes, including cell division, motility, assembly of macromolecular structures, and biogenesis of cell polarity. Considerable attention has been given to these model organisms, which include Escherichia coli, Bacillus subtilis, Caulobacter crescentus, and Myxococcus xanthus. Studies of these processes in the pathogenic bacterium Mycoplasma pneumoniae and its close relatives have also been carried out on a smaller scale, but this work is often overlooked, in part due to this organism's reputation as minimalistic and simple. In this minireview, I discuss recent work on the role of the M. pneumoniae attachment organelle (AO), a structure required for adherence to host cells, in these processes. The AO is constructed from proteins that generally lack homology to those found in other organisms, and this construction occurs in coordination with cell cycle events. The proteins of the M. pneumoniae AO share compositional features with proteins with related roles in model organisms. Once constructed, the AO becomes activated for its role in a form of gliding motility whose underlying mechanism appears to be distinct from that of other gliding bacteria, including Mycoplasma mobile. Together with the FtsZ cytoskeletal protein, motility participates in the cell division process. My intention is to bring this deceptively complex organism into alignment with the better-known model systems.

FIG 1

Scanning electron micrographs of M. pneumoniae (A) and M. genitalium (B). Arrows, AOs. Scale bar, 200 nm.

FIG 2

Model of template-driven duplication of the AO core in M. pneumoniae and its relatives. Several lines of data suggest that duplication of the core begins at the distal terminal button and proceeds toward the cell interior in a TopJ- and P24-dependent manner. Substructures are labeled. Red, original, motility-competent core; blue, new, motility-incompetent core.

FIG 3

Model of M. pneumoniae cell division. (A) In a predivisional cell, the AO contains an electron-dense core (solid black), to the base of which (black arc) the nucleoid (red) is attached. The base is likely the bowl structure observed in some images (28). (B) Using the TopJ/P24-dependent mechanism, the core duplicates, resulting in a second AO with newly replicated DNA attached. (C) Movement of the cell body, driven by motility of only the old AO, pulls the new AO to the rear of the cell. At this point, the new AO is not motility active. (D) As the dividing cell grows, two nascent daughter cells become apparent as the old AO continues to stretch and pull the cell body. Constriction of FtsZ (blue) at midcell contributes to the separation of the daughter cells. (E) The continued combination of pulling and constriction leads to the formation of a filament that connects the nascent daughter cells. (F) When the connecting filament ruptures, cytokinesis has occurred. The cell with the old AO continues its forward motion, and the other daughter cell remains inactive for some amount of time. (G) The new AO becomes activated for motility, and both daughter cells are now motile. This model is an extension of that of Hasselbring et al. (91). (Adapted from Mollicutes: Molecular Biology and Pathogenesis [97].)