A Tad-like apparatus is required for contact-dependent prey killing in predatory social bacteria
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
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.
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
-
- 4,069
- views
-
- 493
- downloads
-
- 55
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
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)
Further reading
-
- Microbiology and Infectious Disease
Antibiotic tolerance in Mycobacterium tuberculosis reduces bacterial killing, worsens treatment outcomes, and contributes to resistance. We studied rifampicin tolerance in isolates with or without isoniazid resistance (IR). Using a minimum duration of killing assay, we measured rifampicin survival in isoniazid-susceptible (IS, n=119) and resistant (IR, n=84) isolates, correlating tolerance with bacterial growth, rifampicin minimum inhibitory concentrations (MICs), and isoniazid-resistant mutations. Longitudinal IR isolates were analyzed for changes in rifampicin tolerance and genetic variant emergence. The median time for rifampicin to reduce the bacterial population by 90% (MDK90) increased from 1.23 days (IS) and 1.31 days (IR) to 2.55 days (IS) and 1.98 days (IR) over 15–60 days of incubation, indicating fast and slow-growing tolerant sub-populations. A 6 log10-fold survival fraction classified tolerance as low, medium, or high, showing that IR is linked to increased tolerance and faster growth (OR = 2.68 for low vs. medium, OR = 4.42 for low vs. high, p-trend = 0.0003). High tolerance in IR isolates was associated with rifampicin treatment in patients and genetic microvariants. These findings suggest that IR tuberculosis should be assessed for high rifampicin tolerance to optimize treatment and prevent the development of multi-drug-resistant tuberculosis.
-
- Evolutionary Biology
- Microbiology and Infectious Disease
HERV-K(HML-2), the youngest clade of human endogenous retroviruses (HERVs), includes many intact or nearly intact proviruses, but no replication competent HML-2 proviruses have been identified in humans. HML-2-related proviruses are present in other primates, including rhesus macaques, but the extent and timing of HML-2 activity in macaques remains unclear. We have identified 145 HML-2-like proviruses in rhesus macaques, including a clade of young, rhesus-specific insertions. Age estimates, intact open reading frames, and insertional polymorphism of these insertions are consistent with recent or ongoing infectious activity in macaques. 106 of the proviruses form a clade characterized by an ~750 bp sequence between env and the 3′ long terminal repeat (LTR), derived from an ancient recombination with a HERV-K(HML-8)-related virus. This clade is found in Old World monkeys (OWM), but not great apes, suggesting it originated after the ape/OWM split. We identified similar proviruses in white-cheeked gibbons; the gibbon insertions cluster within the OWM recombinant clade, suggesting interspecies transmission from OWM to gibbons. The LTRs of the youngest proviruses have deletions in U3, which disrupt the Rec Response Element (RcRE), required for nuclear export of unspliced viral RNA. We show that the HML-8-derived region functions as a Rec-independent constitutive transport element (CTE), indicating the ancestral Rec–RcRE export system was replaced by a CTE mechanism.