"RETRACTED ARTICLE: Vibrio parahaemolyticus RhsP represents a widespread group of pro-effectors for type VI secretion systems

Jiang, Nan; Tang, Le; Xie, Ruiqiang; Li, Zhi; Burkinshaw, Brianne J.; Liang, Xiaoye; Sosa, Dylan; Aravind, L.; Dong, Tao; Zhang, David; Zheng, Jun

doi:10.1038/s41467-018-06201-5

Cited by 8 publications

(4 citation statements)

References 71 publications

(133 reference statements)

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“…B). Interestingly, a recent study showed T6SS2‐dependent killing of a V. parahaemolyticus strain that lacked a newly identified effector immunity pair (RhsP and RhsPi) by its parental WT strain, even in the absence of TfoX or TfoY induction (Jiang et al ., ). These data, therefore, suggest that the basal killing activity that we observed against E. coli as a prey might be more enhanced against nonimmune siblings or, alternatively, that the experimental conditions were different to the current work and that under such conditions the T6SS2 is highly active.…”

Section: Resultsmentioning

confidence: 99%

Ecological implications of gene regulation by TfoX and TfoY among diverse Vibrio species

Metzger

Matthey

Stoudmann

et al. 2019

Environmental Microbiology

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Summary Bacteria of the genus Vibrio are common members of aquatic environments where they compete with other prokaryotes and defend themselves against grazing predators. A macromolecular protein complex called the type VI secretion system (T6SS) is used for both purposes. Previous research showed that the sole T6SS of the human pathogen V. cholerae is induced by extracellular (chitin) or intracellular (low c‐di‐GMP levels) cues and that these cues lead to distinctive signalling pathways for which the proteins TfoX and TfoY serve as master regulators. In this study, we tested whether the TfoX‐ and TfoY‐mediated regulation of T6SS, concomitantly with natural competence or motility, was conserved in non‐cholera Vibrio species, and if so, how these regulators affected the production of individual T6SSs in double‐armed vibrios. We show that, alongside representative competence genes, TfoX regulates at least one T6SS in all tested Vibrio species. TfoY, on the other hand, fostered motility in all vibrios but had a more versatile T6SS response in that it did not foster T6SS‐mediated killing in all tested vibrios. Collectively, our data provide evidence that the TfoX‐ and TfoY‐mediated signalling pathways are mostly conserved in diverse Vibrio species and important for signal‐specific T6SS induction.

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Section: Resultsmentioning

confidence: 99%

Ecological implications of gene regulation by TfoX and TfoY among diverse Vibrio species

Metzger

Matthey

Stoudmann

et al. 2019

Environmental Microbiology

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“…The structure of such Rhs core domain was solved and showed that it forms a shell-like shape enclosing the C-terminal effector domain [63]. Recently, it was also suggested that the C-terminal effector domain might be cleaved from the Rhs core before translocation [64]. However, the accommodation of this large protein around the T6SS tip complex and the molecular mechanisms of effector translocation remain to be further characterized.…”

Section: Discussionmentioning

confidence: 99%

Manipulating the type VI secretion system spike to shuttle passenger proteins

Wettstadt

Filloux

2020

PLoS ONE

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The type VI secretion system (T6SS) is a contractile injection apparatus that translocates a spike loaded with various effectors directly into eukaryotic or prokaryotic target cells. Pseudomonas aeruginosa can load either one of its three T6SSs with a variety of toxic bullets using different but specific modes. The T6SS spike, which punctures the bacterial cell envelope allowing effector transport, consists of a torch-like VgrG trimer on which sits a PAAR protein sharpening the VgrG tip. VgrG itself sits on the Hcp tube and all elements, packed into a T6SS sheath, are propelled out of the cell and into target cells. On occasion, effectors are covalent extensions of VgrG, PAAR or Hcp proteins, which are then coined "evolved" components as opposed to canonical. Here, we show how various passenger domains could be fused to the C terminus of a canonical VgrG, VgrG1a from P. aeruginosa, and be sent into the bacterial culture supernatant. There is no restriction on the passenger type, although the efficacy may vary greatly, since we used either an unrelated T6SS protein, βlactamase, a covalent extension of an "evolved" VgrG, VgrG2b, or a Hcp-dependent T6SS toxin, Tse2. Our data further highlights an exceptional modularity/flexibility for loading the T6SS nano-weapon. Refining the parameters to optimize delivery of passenger proteins of interest would have attractive medical and industrial applications. This may for example involve engineering the T6SS as a delivery system to shuttle toxins into either bacterial pathogens or tumour cells which would be an original approach in the fight against antimicrobial resistant bacteria or cancer. OPEN ACCESSCitation: Wettstadt S, Filloux A (2020) Manipulating the type VI secretion system spike to shuttle passenger proteins. PLoS ONE 15(2): e0228941. https://doi.org/10.

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“…In the environment, Pseudoalteromonas species are found in association with many marine invertebrates (Holmstrom and Kjelleberg, 1999), and might utilize MACs and Pne1 to antagonize specific eukaryotes, like bacterivorous ciliates, while also stimulating the metamorphosis of other eukaryotes like Hydroides . While several CIS nuclease effectors have been identified targeting bacterial cells, including Tde1 from the soil bacterium Agrobacterium tumefaciens (Ma et al, 2014), RhsA from D. dandantii (Koskiniemi et al, 2013), and RhsP from Vibrio parahaemolyticus (Jiang et al, 2018), Pne1 is the first CIS nuclease effector to our knowledge that targets eukaryotic organisms. Interestingly, the eukaryotic NLS at the N-terminus of Pne1 had a partial effect on its ability to kill insect cells, further implying its evolved role in targeting eukaryotic hosts.…”

Section: Discussionmentioning

confidence: 99%

Bacterial Phage Tail-like Structure Kills Eukaryotic Cells by Injecting a Nuclease Effector

Rocchi

Ericson

Malter

et al. 2019

Preprint

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24Many bacteria interact with target organisms using syringe-like structures called 25 Contractile Injection Systems (CIS). CIS structurally resemble headless bacteriophages 26 and share evolutionarily related proteins such as the tail tube, sheath, and baseplate 27 complex. Recent evidence shows that CIS are specialized to puncture membranes and 28 often deliver effectors to target cells. In many cases, CIS mediate trans-kingdom 29 interactions between bacteria and eukaryotes, however the effectors delivered to target 30 cells and their mode of action are often unknown. In this work, we establish an in vitro 31 model to study a CIS called Metamorphosis Associated Contractile structures (MACs) 32 that target eukaryotic cells. We show that MACs kill two eukaryotic cell lines, Fall 33Armyworm Sf9 cells and J774A.1 murine macrophage cells through the action of a 34 newly identified MAC effector, termed Pne1. To our knowledge, Pne1 is the first CIS 35 effector exhibiting nuclease activity against eukaryotic cells. Our results define a new 36 mechanism of CIS-mediated bacteria-eukaryote interaction and are a first step toward 37 understanding structures with the potential to be developed as novel delivery systems 38 for eukaryotic hosts. 39 40 63 targeting eukaryotic cells are yet described that possess nuclease activity. 64 65One group of evolutionarily related CIS have been shown to mediate interactions with 66 diverse eukaryotic organisms including amoeba, grass grubs, wax moths and wasps 67 (Böck et al., 2017; Hurst et al., 2007; Penz et al., 2012 Penz et al., , 2010 Sarris et al., 2014; Yang 68 et al., 2006). We recently described a related eCIS mediating the beneficial relationship 69 between the Gram-negative bacterium Pseudoalteramonas luteoviolacea and a marine 70 tubeworm, Hydroides elegans, hereafter Hydroides (Shikuma et al., 2014(Shikuma et al., , 2016. We 71 called this eCIS from P. luteoviolacea MACs for Metamorphosis Associated Contractile 72 structures, because they stimulate the metamorphosis of Hydroides (Shikuma et al., 73 2014). MACs are the first CIS discovered to form arrays of phage tail-like structures 74 composed of about 100 tails and often measure about 1 µm in diameter. While MACs 75 provide another example of CIS-eukaryote interactions, the range of hosts targeted by 76 eCIS like MACs as well as the identity and mode of action of effectors that mediate 77 these interactions remain poorly understood. 78 79To study the interaction between MACs and eukaryotic cells, we establish an in vitro 80 CIS-cell line interaction model with insect and mammalian cell types. Using these 81 systems, we identify a new MAC effector with nuclease activity that is responsible for 82 cytotoxicity in both cell types. Our results indicate that MACs can interact with a range 83 of host cells and a specific effector mediates killing of eukaryotic cells. 84 85 RESULTS 86 MACs kill insect cell lines in vitro. To study MACs from P. luteoviolacea and test their 87 effect on eukaryotic cells, we focused ...

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"RETRACTED ARTICLE: Vibrio parahaemolyticus RhsP represents a widespread group of pro-effectors for type VI secretion systems

Cited by 8 publications

References 71 publications

Ecological implications of gene regulation by TfoX and TfoY among diverse Vibrio species

Ecological implications of gene regulation by TfoX and TfoY among diverse Vibrio species

Manipulating the type VI secretion system spike to shuttle passenger proteins

Bacterial Phage Tail-like Structure Kills Eukaryotic Cells by Injecting a Nuclease Effector

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