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

Rocchi, Iara; Ericson, Charles F; Malter, Kyle E.; Zargar, Sahar; Eisenstein, Fabian; Pilhofer, Martin; Beyhan, Sinem; Shikuma, Nicholas J.

doi:10.1016/j.celrep.2019.06.019

Cited by 42 publications

(41 citation statements)

References 34 publications

(51 reference statements)

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“…Pseudoalteromonas luteoviolacea . mutant strains were constructed using double‐homologous recombination (Shikuma et al ., 2014; Ericson et al ., 2019; Rocchi et al ., 2019). The mutant strains contain in‐frame deletions of the bmp2 gene (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…luteoviolacea MACs stimulate Hydroides metamorphosis while they are lethal to Hydractinia larvae. MACs carry two characterized effector proteins; one effector called Mif1 that stimulates Hydroides metamorphosis (Ericson et al ., 2019), and another effector called Pne1 that is toxic to insect and mouse cell lines ex vivo (Rocchi et al ., 2019). Interestingly, MACs were also observed to be lethal in Hydroides at high biofilm densities and crude extract concentrations (Shikuma et al ., 2014).…”

Section: Discussionmentioning

confidence: 99%

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Genetic examination of the marine bacterium Pseudoalteromonas luteoviolacea and effects of its metamorphosis‐inducing factors

Alker

Delherbe

Purdy

et al. 2020

Environmental Microbiology

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Summary Pseudoalteromonas luteoviolacea is a globally distributed marine bacterium that stimulates the metamorphosis of marine animal larvae, an important bacteria–animal interaction that can promote the recruitment of animals to benthic ecosystems. Recently, different P. luteoviolacea isolates have been shown to produce two stimulatory factors that can induce tubeworm and coral metamorphosis; Metamorphosis‐Associated Contractile structures (MACs) and tetrabromopyrrole (TBP) respectively. However, it remains unclear what proportion of P. luteoviolacea isolates possess the genes encoding MACs, and what phenotypic effect MACs and TBP have on other larval species. Here, we show that 9 of 19 sequenced P. luteoviolacea genomes genetically encode both MACs and TBP. While P. luteoviolacea biofilms producing MACs stimulate the metamorphosis of the tubeworm Hydroides elegans, TBP biosynthesis genes had no effect under the conditions tested. Although MACs are lethal to larvae of the cnidarian Hydractinia symbiologicarpus, P. luteoviolacea mutants unable to produce MACs are capable of stimulating metamorphosis. Our findings reveal a hidden complexity of interactions between a single bacterial species, the factors it produces and two species of larvae belonging to different phyla.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Genetic examination of the marine bacterium Pseudoalteromonas luteoviolacea and effects of its metamorphosis‐inducing factors

Alker

Delherbe

Purdy

et al. 2020

Environmental Microbiology

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“…MACs loci produce arrays of ~100 eCIS structures that trigger metamorphosis of the marine tubeworm Hydroides elegans hos ng the bacteria 12 . MACs par cles inject a nuclease effector that kills eukaryo c cell lines but this ac vity is not essen al for metamorphosis 13 .…”

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confidence: 99%

The extracellular contractile injection system is enriched in environmental microbes and associates with numerous toxins

Geller

Pollin

Zlotkin

et al. 2020

Preprint

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Bacteria employ toxin delivery systems to exclude bacterial competitors and to infect host cells. Characterization of these systems and the toxins they secrete is important for understanding microbial interactions and virulence in different ecosystems. The extracellular Contractile Injection System (eCIS) is a toxin delivery particle that evolved from a bacteriophage tail. Four known eCIS systems have been shown to mediate interactions between bacteria and their invertebrate hosts, but the broad ecological function of these systems remains unknown. Here, we identify eCIS loci in 1,249 prokaryotic genomes and reveal a striking enrichment of these loci in environmental microbes and absence from mammalian pathogens. We uncovered 13 toxin genes that associate with eCIS from diverse microbes and show that they can inhibit growth of bacteria, yeast or both. We also found immunity genes that protect bacteria from self-intoxication, supporting an antibacterial role for eCIS. Furthermore, we identified multiple new eCIS core genes including a conserved eCIS transcriptional regulator. Finally, we present our data through eCIStem; an extensive eCIS repository. Our findings define eCIS as a widespread environmental prokaryotic toxin delivery system that likely mediates antagonistic interactions with eukaryotes and prokaryotes. Future understanding of eCIS functions can be leveraged for the development of new biological control systems, antimicrobials, and cell-free protein delivery tools.

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“…Like other described CIS, BIS gene clusters possess genes encoding the syringe-like structural components and could encode for effectors that elicit specific cellular responses from target host cells. For example, the closely related injection system called MACs possesses two different effectors; one effector protein promotes the metamorphic development of a tubeworm (Ericson et al, 2019) and a second toxic effector kills insect and mammalian cell lines (Rocchi et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

A Distinct Contractile Injection System Found in a Majority of Adult Human Microbiomes

Rojas

Cavalcanti

McNair

et al. 2019

Preprint

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

Abstract: Highlights d Contractile injection systems are syringe-like structures from bacteria d A contractile injection system called MACs targets insect and mouse cell lines d MACs kill cell lines by delivering an effector called Pne1 with nuclease activity

Cited by 42 publications

References 34 publications

Genetic examination of the marine bacterium Pseudoalteromonas luteoviolacea and effects of its metamorphosis‐inducing factors

Genetic examination of the marine bacterium Pseudoalteromonas luteoviolacea and effects of its metamorphosis‐inducing factors

The extracellular contractile injection system is enriched in environmental microbes and associates with numerous toxins

A Distinct Contractile Injection System Found in a Majority of Adult Human Microbiomes

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