Unraveling the role of distinct cytoskeletal motility structures in Mycoplasma pneumoniae relatives

Abstract

Mycoplasma represents a unique genus of prokaryotic bacteria distinguished by the absence of a cell wall, a characteristic that sets it apart from other bacteria. Within the Mollicutes class, phylogenetic analysis reveals three distinct categories: Spiroplasma, Mycoplasma and Acholeplasma. Mycoplasmas within Pneumoniae are recognized for their capacity to induce a range of diseases in both humans and animals, frequently impacting respiratory and reproductive health. The representative strains in Pneumoniae group, particularly the M. pneumoniae clusters, have garnered significant attention due to their remarkable ability to adhere to, invade, and traverse host cells. This ability is facilitated by specialized structures known as attachment organelles, which possess a unique cytoskeletal structure that supports a distinctive gliding motility mechanism. This mode of motility is distinct from that observed in eukaryotes and the majority of bacteria. The gliding machinery of Mycoplasma is a complex assembly consisting of both surface and internal components, including a terminal button, paired plates, and a structure resembling a bowl or wheel. The internal architecture of the attachment organelles provides the essential scaffold for the operation of this sophisticated motility system. Mycoplasma's gliding motility is crucial for its infection process and its capacity to evade the host immune defenses. Understanding the role of this motility to immune evasion can offer profound insights into the pathogenesis of these bacteria, could pave the way for the development of more effective therapeutic strategies against diseases caused by Mycoplasma and related species.

Keywords: Mycoplasma; Mycoplasma pneumoniae relatives; Cytoadherence; Cytoskeleton; Motility; Pathogenesis.

Fig. 1

Gliding Mycoplasma species and the gliding mechanism schematic of the M. pneumoniae relatives. A Phylogenetic tree based on 16S rRNA sequences of mycoplasmas within the M. pneumoniae cluster. Scale bar, 0.01 substitutions per site. The evolutionary history was inferred using the Neighbor-Joining method [32]. The analytical procedure encompassed 8 coding nucleotide sequences using 1st, 2nd, 3rd, and non-coding positions. The pairwise deletion option was applied to all ambiguous positions for each sequence pair resulting in a final data set comprising 1528 positions. Evolutionary analyses were conducted in MEGA12 [33]. Immotile species are marked by black stars. B Schematic of Mycoplasma gliding. The relatives of M. pneumoniae employ attachment organelles for gliding to survive and persistently infect the host. The nap adhesin undergoes a repetitive catch-pull-release cycle with sialylated oligosaccharides on the host surface, whereas attachment organelles pull the remaining part of the cell toward the back end of the bowl complex, thereby completing a glide step

Fig. 2

The comparison of cell morphology and cytoskeleton structure of among M. pneumoniae Cluster Species. Schematic representations are oriented with the attachment organelle positioned apically. A The cellular schematic of the M. pneumoniae cluster species depicts a tripartite structure: an attachment organelle (in shades of purple), a cell body (in green), and a trailing filament (also in green). The attachment organelle itself comprises a knob (dark purple) and a shaft (light purple). The cytoskeletal structure consists of a terminal button (white), a rod (light gray), and a base (dark gray). B M. gallisepticum; C M. imitans; D M. amphoriforme; E M. testudinis; F M. pirum; G M. genitalium; H M. pneumoniae. This figure is adapted from Hatchel et al. (2008) [18]

Fig. 3

Comparative analysis of cytoskeletal architectures in M. pneumoniae A, M. genitalium B, and M. gallisepticum C. The cytoskeletons of M. pneumoniae and M. genitalium are comprised of three principal components: the terminal button, paired plates, and a bowl complex/wheel structure. In contrast, the M. gallisepticum cytoskeleton consists of five distinct elements: a cap, small oval, large oval, bowl, and connecting filaments observed bridging the large oval and bowl structures. The dimensions and constituent proteins of each cytoskeleton are indicated in the figure