A Tad-like apparatus is required for contact-dependent prey killing in predatory social bacteria
- CNRS-Aix Marseille University, France
- Aix-Marseille Université - CNRS UMR 7288,, France
- Centre national de la recherche scientifique - Aix-Marseille Université, France
Abstract
Myxococcus xanthus, a soil bacterium, predates collectively using motility to invade prey colonies. Prey lysis is mostly thought to rely on secreted factors, cocktails of antibiotics and enzymes, and direct contac with Myxococcus cells. In this study, we show that on surfaces the coupling of A-motility and contact-dependent killing is the central predatory mechanism driving effective prey colony invasion and consumption. At the molecular level, contact-dependent killing involves a newly discovered type IV filament-like machinery (Kil) that both promotes motility arrest and prey cell plasmolysis. In this process, Kil proteins assemble at the predator-prey contact site, suggesting that they allow tight contact with prey cells for their intoxication. Kil-like systems form a new class of Tad-like machineries in predatory bacteria, suggesting a conserved function in predator-prey interactions. This study further reveals a novel cell-cell interaction function for bacterial pili-like assemblages.
Data availability
Source Data files have been provided for :- Figure 2-source data 1: E. coli loss of fluorescence during contact-dependent lysis (Figure 2c).- Figure 2-figure supplement 5-source data 1: Contact dependent-lysis and VipA-GFP dynamics.- Figure 2-figure supplement 7-source data 1: CPRG assay.- Figure 3-source data 1: CPRG assay (Figure 3b).- Figure 3-source data 2: counting percentage of contacts with a prey leading to motility pauses and prey cell lysis (Figure 3c, 3d).- Figure 3-figure supplement 3-source data 1: CPRG assay.- Figure 4-source data 1: counting percentage of contacts with a prey leading to NG-KilD foci formation and counting percentage of NG-KilD foci associated with motility pause and prey cell lysis (Figure 4e, 4f, 4g).- Figure 4-figure supplement 1-source data 1: CPRG assay.- Figure 4-figure supplement 2-source data 1: CPRG assay.- Figure 4-figure supplement 3-source data 1: Lysis time.- Figure 4-figure supplement 4-source data 1: Western Blot.- Figure 5-source data 1: Flow cytometry (Figure 5c, 5d).- Figure 5-source data 2: M. xanthus growth during prey colony invasion (Figure 5e).- Figure 5-source data 3: Increase in M. xanthus cell length during predation (Figure 5f).- Figure 5-figure supplement 2-source data 1: Growth curves.- Figure 6-source data 1: Prey CFU counts during predation (Figure 6b,c,d,e,f).- Figure 7-source data 1: Supermatrix alignment.- Figure 3-figure supplement 2: RNA-seq Data from Livingstone PG et al. (2018) Microb Genom. PMID:29345219, Supplementary File 1 available online: https://www.microbiologyresearch.org/content/journal/mgen/10.1099/mgen.0.000152#supplementary_data).
Article and author information
Author details
Bianca H Habermann
Funding
Centre National de la Recherche Scientifique (2019 CNRS 80-Prime)
- Tâm Mignot
Ministère de l'Éducation et de l'Enseignement supérieur (MENRT thesis grant)
- Sofiene Seef
Ministère de l'Éducation et de l'Enseignement supérieur (MENRT thesis grant)
- Paul de Boissier
Ministère de l'Éducation et de l'Enseignement supérieur (MENRT thesis grant)
- Donovan Robert
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Michael T Laub, Massachusetts Institute of Technology, United States
Version history
- Preprint posted: February 27, 2021 (view preprint)
- Received: July 22, 2021
- Accepted: September 9, 2021
- Accepted Manuscript published: September 10, 2021 (version 1)
- Version of Record published: September 23, 2021 (version 2)
Copyright
© 2021, Seef et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 3,883
- views
-
- 461
- downloads
-
- 48
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
A Tad-like apparatus is required for contact-dependent prey killing in predatory social bacteria
eLife 10:e72409.
https://doi.org/10.7554/eLife.72409
Further reading
-
- Microbiology and Infectious Disease
In the Firmicutes phylum, GpsB is a membrane associated protein that coordinates peptidoglycan synthesis with cell growth and division. Although GpsB has been studied in several bacteria, the structure, function, and interactome of Staphylococcus aureus GpsB is largely uncharacterized. To address this knowledge gap, we solved the crystal structure of the N-terminal domain of S. aureus GpsB, which adopts an atypical, asymmetric dimer, and demonstrates major conformational flexibility that can be mapped to a hinge region formed by a three-residue insertion exclusive to Staphylococci. When this three-residue insertion is excised, its thermal stability increases, and the mutant no longer produces a previously reported lethal phenotype when overexpressed in Bacillus subtilis. In S. aureus, we show that these hinge mutants are less functional and speculate that the conformational flexibility imparted by the hinge region may serve as a dynamic switch to fine-tune the function of the GpsB complex and/or to promote interaction with its various partners. Furthermore, we provide the first biochemical, biophysical, and crystallographic evidence that the N-terminal domain of GpsB binds not only PBP4, but also FtsZ, through a conserved recognition motif located on their C-termini, thus coupling peptidoglycan synthesis to cell division. Taken together, the unique structure of S. aureus GpsB and its direct interaction with FtsZ/PBP4 provide deeper insight into the central role of GpsB in S. aureus cell division.
-
- Microbiology and Infectious Disease
The agr quorum-sensing system links Staphylococcus aureus metabolism to virulence, in part by increasing bacterial survival during exposure to lethal concentrations of H2O2, a crucial host defense against S. aureus. We now report that protection by agr surprisingly extends beyond post-exponential growth to the exit from stationary phase when the agr system is no longer turned on. Thus, agr can be considered a constitutive protective factor. Deletion of agr resulted in decreased ATP levels and growth, despite increased rates of respiration or fermentation at appropriate oxygen tensions, suggesting that Δagr cells undergo a shift towards a hyperactive metabolic state in response to diminished metabolic efficiency. As expected from increased respiratory gene expression, reactive oxygen species (ROS) accumulated more in the agr mutant than in wild-type cells, thereby explaining elevated susceptibility of Δagr strains to lethal H2O2 doses. Increased survival of wild-type agr cells during H2O2 exposure required sodA, which detoxifies superoxide. Additionally, pretreatment of S. aureus with respiration-reducing menadione protected Δagr cells from killing by H2O2. Thus, genetic deletion and pharmacologic experiments indicate that agr helps control endogenous ROS, thereby providing resilience against exogenous ROS. The long-lived ‘memory’ of agr-mediated protection, which is uncoupled from agr activation kinetics, increased hematogenous dissemination to certain tissues during sepsis in ROS-producing, wild-type mice but not ROS-deficient (Cybb−/−) mice. These results demonstrate the importance of protection that anticipates impending ROS-mediated immune attack. The ubiquity of quorum sensing suggests that it protects many bacterial species from oxidative damage.
