Functional Organization of a Multimodular Bacterial Chemosensory Apparatus

Abstract

Chemosensory systems (CSS) are complex regulatory pathways capable of perceiving external signals and translating them into different cellular behaviors such as motility and development. In the δ-proteobacterium Myxococcus xanthus, chemosensing allows groups of cells to orient themselves and aggregate into specialized multicellular biofilms termed fruiting bodies. M. xanthus contains eight predicted CSS and 21 chemoreceptors. In this work, we systematically deleted genes encoding components of each CSS and chemoreceptors and determined their effects on M. xanthus social behaviors. Then, to understand how the 21 chemoreceptors are distributed among the eight CSS, we examined their phylogenetic distribution, genomic organization and subcellular localization. We found that, in vivo, receptors belonging to the same phylogenetic group colocalize and interact with CSS components of the respective phylogenetic group. Finally, we identified a large chemosensory module formed by three interconnected CSS and multiple chemoreceptors and showed that complex behaviors such as cell group motility and biofilm formation require regulatory apparatus composed of multiple interconnected Che-like systems.

Internal Sense of Direction: Sensing and Signaling from Cytoplasmic Chemoreceptors

“…Mutations in the Frz pathway alter the frequency of reversals. Fluorescence microscopy revealed that FrzCD localizes in helical filaments that cover the cell length and that FrzCD is dynamic within these structures, continuously changing its position, number, and intensity (74,75). FrzCD in one cell transiently aligns with that in another as cells make side- to-side contacts.…”

“…FrzCD appears to respond to the presence of attractants and repellents through levels of methylation, and the modification appears to have consequences on fruiting body formation (8). The second M. xanthus cytoplasmic chemoreceptor, Mcp7, displays subpolar localization at either one or both poles and was the most mobile of the M. xanthus chemoreceptors (75). This chemoreceptor is encoded in the che7 locus with cognate copies of CheA, CheW, CheY, CheB, CheR, and the accessory protein Cpc7.…”

The nucleoid as a scaffold for the assembly of bacterial signaling complexes

“…As a control, we looked at the cellular localization of another chemoreceptor fusion, DifA-GFP, in the absence of parB . DifA has been recently shown to form membrane bound and uniformly distributed clusters [28]. In the absence of parB , even cells without nucleoid still carried DifA-GFP clusters and these clusters localized similar to the wild type [28] (Figure 1E).…”

“…Fluorescence microscopy has shown that a FrzCD-GFP fusion appears as multiple distributed clusters co-localizing with the nucleoid in M. xanthus cells (Figure 1A, 1B and Figure S1) [27–29]. It has been also shown that an inducible FrzE-YFP fusion colocalizes with FrzCD at the nucleoid [29].…”

Chemosensory Regulation of a HEAT-Repeat Protein Couples Aggregation and Sporulation in Myxococcus xanthus

“…The central processing component for all chemosensory systems is CheA. In previous work, we analyzed the M. xanthus genome for cheA homologs and identified four additional clusters, including Che5 to -8 (31,32). Because each cluster contains unique genes predicted to encode novel protein functionality regarding inputs and/or outputs, we further characterized the Che7 system (genes MXAN_6965 to MXAN_ 6957) for its role in development in M. xanthus.…”