A chimeric nuclease substitutes a phage CRISPR-Cas system to provide sequence-specific immunity against subviral parasites
Mobile genetic elements, elements that can move horizontally between genomes, have profound effects on their host's fitness. The phage-inducible chromosomal island-like element (PLE) is a mobile element that integrates into the chromosome of Vibrio cholerae and parasitizes the bacteriophage ICP...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-07-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/68339 |
| _version_ | 1818027218735988736 |
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| author | Zachary K Barth Maria HT Nguyen Kimberley D Seed |
| author_facet | Zachary K Barth Maria HT Nguyen Kimberley D Seed |
| author_sort | Zachary K Barth |
| collection | DOAJ |
| description | Mobile genetic elements, elements that can move horizontally between genomes, have profound effects on their host's fitness. The phage-inducible chromosomal island-like element (PLE) is a mobile element that integrates into the chromosome of Vibrio cholerae and parasitizes the bacteriophage ICP1 to move between cells. This parasitism by PLE is such that it abolishes the production of ICP1 progeny and provides a defensive boon to the host cell population. In response to the severe parasitism imposed by PLE, ICP1 has acquired an adaptive CRISPR-Cas system that targets the PLE genome during infection. However, ICP1 isolates that naturally lack CRISPR-Cas are still able to overcome certain PLE variants, and the mechanism of this immunity against PLE has thus far remained unknown. Here, we show that ICP1 isolates that lack CRISPR-Cas encode an endonuclease in the same locus, and that the endonuclease provides ICP1 with immunity to a subset of PLEs. Further analysis shows that this endonuclease is of chimeric origin, incorporating a DNA-binding domain that is highly similar to some PLE replication origin-binding proteins. This similarity allows the endonuclease to bind and cleave PLE origins of replication. The endonuclease appears to exert considerable selective pressure on PLEs and may drive PLE replication module swapping and origin restructuring as mechanisms of escape. This work demonstrates that new genome defense systems can arise through domain shuffling and provides a greater understanding of the evolutionary forces driving genome modularity and temporal succession in mobile elements. |
| first_indexed | 2024-12-10T04:44:25Z |
| format | Article |
| id | doaj.art-ac909c46f0ff45d68da1fa93f65ade29 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-12-10T04:44:25Z |
| publishDate | 2021-07-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-ac909c46f0ff45d68da1fa93f65ade292022-12-22T02:01:48ZengeLife Sciences Publications LtdeLife2050-084X2021-07-011010.7554/eLife.68339A chimeric nuclease substitutes a phage CRISPR-Cas system to provide sequence-specific immunity against subviral parasitesZachary K Barth0https://orcid.org/0000-0002-1321-306XMaria HT Nguyen1https://orcid.org/0000-0003-2441-4948Kimberley D Seed2https://orcid.org/0000-0002-0139-1600Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Plant and Microbial Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Plant and Microbial Biology, University of California, Berkeley, Berkeley, United States; Chan Zuckerberg Biohub, San Francisco, United StatesMobile genetic elements, elements that can move horizontally between genomes, have profound effects on their host's fitness. The phage-inducible chromosomal island-like element (PLE) is a mobile element that integrates into the chromosome of Vibrio cholerae and parasitizes the bacteriophage ICP1 to move between cells. This parasitism by PLE is such that it abolishes the production of ICP1 progeny and provides a defensive boon to the host cell population. In response to the severe parasitism imposed by PLE, ICP1 has acquired an adaptive CRISPR-Cas system that targets the PLE genome during infection. However, ICP1 isolates that naturally lack CRISPR-Cas are still able to overcome certain PLE variants, and the mechanism of this immunity against PLE has thus far remained unknown. Here, we show that ICP1 isolates that lack CRISPR-Cas encode an endonuclease in the same locus, and that the endonuclease provides ICP1 with immunity to a subset of PLEs. Further analysis shows that this endonuclease is of chimeric origin, incorporating a DNA-binding domain that is highly similar to some PLE replication origin-binding proteins. This similarity allows the endonuclease to bind and cleave PLE origins of replication. The endonuclease appears to exert considerable selective pressure on PLEs and may drive PLE replication module swapping and origin restructuring as mechanisms of escape. This work demonstrates that new genome defense systems can arise through domain shuffling and provides a greater understanding of the evolutionary forces driving genome modularity and temporal succession in mobile elements.https://elifesciences.org/articles/68339bacteriophageVibrio choleraemobile elementsatellite |
| spellingShingle | Zachary K Barth Maria HT Nguyen Kimberley D Seed A chimeric nuclease substitutes a phage CRISPR-Cas system to provide sequence-specific immunity against subviral parasites eLife bacteriophage Vibrio cholerae mobile element satellite |
| title | A chimeric nuclease substitutes a phage CRISPR-Cas system to provide sequence-specific immunity against subviral parasites |
| title_full | A chimeric nuclease substitutes a phage CRISPR-Cas system to provide sequence-specific immunity against subviral parasites |
| title_fullStr | A chimeric nuclease substitutes a phage CRISPR-Cas system to provide sequence-specific immunity against subviral parasites |
| title_full_unstemmed | A chimeric nuclease substitutes a phage CRISPR-Cas system to provide sequence-specific immunity against subviral parasites |
| title_short | A chimeric nuclease substitutes a phage CRISPR-Cas system to provide sequence-specific immunity against subviral parasites |
| title_sort | chimeric nuclease substitutes a phage crispr cas system to provide sequence specific immunity against subviral parasites |
| topic | bacteriophage Vibrio cholerae mobile element satellite |
| url | https://elifesciences.org/articles/68339 |
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