Attachment organelle ultrastructure correlates with phylogeny, not gliding motility properties, in Mycoplasma pneumoniae relatives

Abstract

The Mycoplasma pneumoniae cluster is a clade of eight described species which all exhibit cellular polarity. Their polar attachment organelle is a hub of cellular activities including cytadherence and gliding motility, and its duplication in the species M. pneumoniae is coordinated with cell division and DNA replication. The attachment organelle houses a detergent-insoluble, electron-dense core whose presence is required for structural integrity. Although mutant analysis has led to the identification of attachment organelle proteins, the mechanistic basis for the activities of the attachment organelle remains poorly understood, with gliding motility attributed alternatively to the core or to the adhesins. In this study we investigated attachment organelle-associated phenotypes, including gliding motility characteristics and ultrastructural details, in seven species of the M. pneumoniae cluster under identical conditions, allowing direct comparison. We identified gliding ability in three species in which it has not previously been reported, Mycoplasma imitans, Mycoplasma pirum and Mycoplasma testudinis. Across species, ultrastructural features of attachment organelles and their cores do not correlate with gliding speed, and morphological features of cores are inconsistent with predictions about how these structures are involved in the gliding process, disfavouring a prominent, direct role for the electron-dense core in gliding. In addition, we found M. pneumoniae to be an outlier in terms of cell structure with respect to its close relatives, suggesting that it has acquired a special set of adaptations during its evolution.