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

Alexander Martin Geller; Inbal Pollin; David Zlotkin; Aleks Danov; Nimrod Nachmias; William B. Andreopoulos; Keren Shemesh; Asaf Levy

doi:10.1038/s41467-021-23777-7

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

Alexander Martin Geller, Inbal Pollin, David Zlotkin, Aleks Danov, Nimrod Nachmias, William B. Andreopoulos, Keren Shemesh, Asaf Levy^*

^*Corresponding author for this work

Department of Plant Pathology and Microbiology

Research output: Contribution to journal › Article › peer-review

18 Scopus citations

Abstract

The extracellular Contractile Injection System (eCIS) is a toxin-delivery particle that evolved from a bacteriophage tail. Four eCISs have previously been shown to mediate interactions between bacteria and their invertebrate hosts. Here, we identify eCIS loci in 1,249 bacterial and archaeal genomes and reveal an enrichment of these loci in environmental microbes and their apparent absence from mammalian pathogens. We show that 13 eCIS-associated toxin genes from diverse microbes can inhibit the growth of bacteria and/or yeast. We identify immunity genes that protect bacteria from self-intoxication, further supporting an antibacterial role for some eCISs. We also identify previously undescribed eCIS core genes, including a conserved eCIS transcriptional regulator. Finally, we present our data through an extensive eCIS repository, termed eCIStem. Our findings support eCIS as a toxin-delivery system that is widespread among environmental prokaryotes and likely mediates antagonistic interactions with eukaryotes and other prokaryotes.

Original language	American English
Article number	3743
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-23777-7
State	Published - 1 Dec 2021

Bibliographical note

Funding Information:
A.L. is generously supported by the Israeli Science Foundation (Grants #1535/20, #3300/ 20), Alon Fellowship of the Israeli council of higher education, The Hebrew Univeristy - Univeristy of Illinois Urbana-Champain seed grant, and the Israeli Ministry of Agriculture (Grant 12-12-0002). A.M.G. is generously supported by the Kaete Klausner Scholarship and a scholarship from the Israeli Ministry of Aliyah and Integration. We thank Prof. Maya Schuldiner, Prof. Yechiel Shay, and Prof. Saul Burdman for providing different plasmids and cells. We thank Dr. Omri Finkel, Dr. Hila Sberro, Prof. Saul Burdman, Prof. Rotem Sorek, Dr. Erez Mills, Dr. Gal Ofir, and Dr. Lianet Noda-Garcia for careful evaluation of the paper.

Publisher Copyright:
© 2021, The Author(s).

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title = "The extracellular contractile injection system is enriched in environmental microbes and associates with numerous toxins",

abstract = "The extracellular Contractile Injection System (eCIS) is a toxin-delivery particle that evolved from a bacteriophage tail. Four eCISs have previously been shown to mediate interactions between bacteria and their invertebrate hosts. Here, we identify eCIS loci in 1,249 bacterial and archaeal genomes and reveal an enrichment of these loci in environmental microbes and their apparent absence from mammalian pathogens. We show that 13 eCIS-associated toxin genes from diverse microbes can inhibit the growth of bacteria and/or yeast. We identify immunity genes that protect bacteria from self-intoxication, further supporting an antibacterial role for some eCISs. We also identify previously undescribed eCIS core genes, including a conserved eCIS transcriptional regulator. Finally, we present our data through an extensive eCIS repository, termed eCIStem. Our findings support eCIS as a toxin-delivery system that is widespread among environmental prokaryotes and likely mediates antagonistic interactions with eukaryotes and other prokaryotes.",

author = "Geller, {Alexander Martin} and Inbal Pollin and David Zlotkin and Aleks Danov and Nimrod Nachmias and Andreopoulos, {William B.} and Keren Shemesh and Asaf Levy",

note = "Funding Information: A.L. is generously supported by the Israeli Science Foundation (Grants #1535/20, #3300/ 20), Alon Fellowship of the Israeli council of higher education, The Hebrew Univeristy - Univeristy of Illinois Urbana-Champain seed grant, and the Israeli Ministry of Agriculture (Grant 12-12-0002). A.M.G. is generously supported by the Kaete Klausner Scholarship and a scholarship from the Israeli Ministry of Aliyah and Integration. We thank Prof. Maya Schuldiner, Prof. Yechiel Shay, and Prof. Saul Burdman for providing different plasmids and cells. We thank Dr. Omri Finkel, Dr. Hila Sberro, Prof. Saul Burdman, Prof. Rotem Sorek, Dr. Erez Mills, Dr. Gal Ofir, and Dr. Lianet Noda-Garcia for careful evaluation of the paper. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

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AU - Andreopoulos, William B.

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AU - Levy, Asaf

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N2 - The extracellular Contractile Injection System (eCIS) is a toxin-delivery particle that evolved from a bacteriophage tail. Four eCISs have previously been shown to mediate interactions between bacteria and their invertebrate hosts. Here, we identify eCIS loci in 1,249 bacterial and archaeal genomes and reveal an enrichment of these loci in environmental microbes and their apparent absence from mammalian pathogens. We show that 13 eCIS-associated toxin genes from diverse microbes can inhibit the growth of bacteria and/or yeast. We identify immunity genes that protect bacteria from self-intoxication, further supporting an antibacterial role for some eCISs. We also identify previously undescribed eCIS core genes, including a conserved eCIS transcriptional regulator. Finally, we present our data through an extensive eCIS repository, termed eCIStem. Our findings support eCIS as a toxin-delivery system that is widespread among environmental prokaryotes and likely mediates antagonistic interactions with eukaryotes and other prokaryotes.

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

Abstract

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