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. 2020 Nov 6;8(11):1739.
doi: 10.3390/microorganisms8111739.

A Genomic Survey of Signalling in the Myxococcaceae

David E Whitworth  1 , Allison Zwarycz  1
Affiliations

A Genomic Survey of Signalling in the Myxococcaceae

David E Whitworth et al. Microorganisms. .

Abstract

As prokaryotes diverge by evolution, essential 'core' genes required for conserved phenotypes are preferentially retained, while inessential 'accessory' genes are lost or diversify. We used the recently expanded number of myxobacterial genome sequences to investigate the conservation of their signalling proteins, focusing on two sister genera (Myxococcus and Corallococcus), and on a species within each genus (Myxococcus xanthus and Corallococcus exiguus). Four new C. exiguus genome sequences are also described here. Despite accessory genes accounting for substantial proportions of each myxobacterial genome, signalling proteins were found to be enriched in the core genome, with two-component system genes almost exclusively so. We also investigated the conservation of signalling proteins in three myxobacterial behaviours. The linear carotenogenesis pathway was entirely conserved, with no gene gain/loss observed. However, the modular fruiting body formation network was found to be evolutionarily plastic, with dispensable components in all modules (including components required for fruiting in the model myxobacterium M. xanthus DK1622). Quorum signalling (QS) is thought to be absent from most myxobacteria, however, they generally appear to be able to produce CAI-I (cholerae autoinducer-1), to sense other QS molecules, and to disrupt the QS of other organisms, potentially important abilities during predation of other prokaryotes.

Keywords: Myxococcales; carotenoids; comparative genomics; development; fruiting body formation; myxobacteria; one-component systems; quorum signalling; two-component systems.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Response regulator (RR) families encoded in myxobacterial genomes. The strains under consideration are in the same order (front to back) as those detailed in Table 1 (top to bottom). Different strains and species exhibit similar profiles of RR families, although conserved differences can be seen in some groups of genomes.
Figure 2
Figure 2
The percentage of RRs and TFs + OCSs found in the pan-genome core for the four groups of genomes.
Figure 3
Figure 3
Conservation of signalling pathway proteins in Myxococcaceae. Regulatory proteins are shown as ovals. Positive regulation is shown with pointed arrows, and negative regulation with blunt-headed arrows. (A) Carotenoid production. In the dark (top), CarQ is held inactive by CarR, while CarA and CarH repress expression of the constitutively active crt promoter. In the light (bottom), CarH is directly inactivated while CarF inactivates CarR, releasing CarQ to direct transcription of carQRS, producing CarS which binds to CarA, relieving repression of the crt genes, which encode enzymes for the biosynthesis of carotenoids (lycopene shown as an example). (B) Fruiting body formation. Gene products work together in modules (dark grey boxes). Starvation triggers the production of the secondary messengers c-di-GMP and (p)ppGpp and activates the EBP (enhancer binding protein) cascade and the Mrp module. The A-signalling, C-signalling, FruA and Nla24/DmxB modules are stimulated by secondary messengers and regulatory modules. Various ‘development timer’ proteins regulate the timing of fruiting, and the DevTRS/CRISPR module modulates the timing of sporulation. ‘Other’ proteins regulate fruiting, but their relationship to other modules is not clear. (C) Quorum signalling. Four common Gram-negative bacterial quorum signals (AI-I, AI-II, CAI-I and HAI-I), and their corresponding synthase and receptor/regulator proteins, are shown. Also shown is the quorum-quenching AHL acylase, PvdQ. Whether regulatory proteins are core, conserved, or dispensable, is indicated based on their pattern of evolutionary conservation. Core proteins are found at a constant number per genome across the Myxococcaceae and are highlighted in bold text. Conserved proteins are found in all groups of Myxococcaceal genomes, but in variable numbers, and are indicated with a pale grey background and dashed outline. Dispensable proteins are absent from some groups of Myxococcaeal genomes and are shown with a transparent background, and grey text.
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