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
-
- 3,649
- Page views
-
- 429
- Downloads
-
- 26
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
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
-
- Immunology and Inflammation
- Microbiology and Infectious Disease
Pyroptosis and apoptosis are two forms of regulated cell death that can defend against intracellular infection. When a cell fails to complete pyroptosis, backup pathways will initiate apoptosis. Here, we investigated the utility of apoptosis compared to pyroptosis in defense against an intracellular bacterial infection. We previously engineered Salmonella enterica serovar Typhimurium to persistently express flagellin, and thereby activate NLRC4 during systemic infection in mice. The resulting pyroptosis clears this flagellin-engineered strain. We now show that infection of caspase-1 or gasdermin D deficient macrophages by this flagellin-engineered S. Typhimurium induces apoptosis in vitro. Additionally, we engineered S. Typhimurium to translocate the pro-apoptotic BH3 domain of BID, which also triggers apoptosis in macrophages in vitro. During mouse infection, the apoptotic pathway successfully cleared these engineered S. Typhimurium from the intestinal niche but failed to clear the bacteria from the myeloid niche in the spleen or lymph nodes. In contrast, the pyroptotic pathway was beneficial in defense of both niches. To clear an infection, cells may have specific tasks that they must complete before they die; different modes of cell death could initiate these ‘bucket lists’ in either convergent or divergent ways.
-
- Microbiology and Infectious Disease
SARS-CoV-2 spike protein plays a key role in mediating viral entry and inducing host immune responses. It can adopt either an open or closed conformation based on the position of its receptor-binding domain (RBD). It is yet unclear what causes these conformational changes or how they influence the spike’s functions. Here, we show that Lys417 in the RBD plays dual roles in the spike’s structure: it stabilizes the closed conformation of the trimeric spike by mediating inter-spike–subunit interactions; it also directly interacts with ACE2 receptor. Hence, a K417V mutation has opposing effects on the spike’s function: it opens up the spike for better ACE2 binding while weakening the RBD’s direct binding to ACE2. The net outcomes of this mutation are to allow the spike to bind ACE2 with higher probability and mediate viral entry more efficiently, but become more exposed to neutralizing antibodies. Given that residue 417 has been a viral mutational hotspot, SARS-CoV-2 may have been evolving to strike a balance between infection potency and immune evasion, contributing to its pandemic spread.
