Temperature, by Controlling Growth Rate, Regulates CRISPR-Cas Activity in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
ABSTRACT Clustered regularly interspaced short palindromic repeat (CRISPR)-associated (CRISPR-Cas) systems are adaptive defense systems that protect bacteria and archaea from invading genetic elements. In Pseudomonas aeruginosa, quorum sensing (QS) induces the CRISPR-Cas defense system at high cell...
| Main Authors: | , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2018-12-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.02184-18 |
| _version_ | 1819199685561155584 |
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| author | Nina Molin Høyland-Kroghsbo Katrina Arcelia Muñoz Bonnie L. Bassler |
| author_facet | Nina Molin Høyland-Kroghsbo Katrina Arcelia Muñoz Bonnie L. Bassler |
| author_sort | Nina Molin Høyland-Kroghsbo |
| collection | DOAJ |
| description | ABSTRACT Clustered regularly interspaced short palindromic repeat (CRISPR)-associated (CRISPR-Cas) systems are adaptive defense systems that protect bacteria and archaea from invading genetic elements. In Pseudomonas aeruginosa, quorum sensing (QS) induces the CRISPR-Cas defense system at high cell density when the risk of bacteriophage infection is high. Here, we show that another cue, temperature, modulates P. aeruginosa CRISPR-Cas. Increased CRISPR adaptation occurs at environmental (i.e., low) temperatures compared to that at body (i.e., high) temperature. This increase is a consequence of the accumulation of CRISPR-Cas complexes, coupled with reduced P. aeruginosa growth rate at the lower temperature, the latter of which provides additional time prior to cell division for CRISPR-Cas to patrol the cell and successfully eliminate and/or acquire immunity to foreign DNA. Analyses of a QS mutant and synthetic QS compounds show that the QS and temperature cues act synergistically. The diversity and level of phage encountered by P. aeruginosa in the environment exceed that in the human body, presumably warranting increased reliance on CRISPR-Cas at environmental temperatures. IMPORTANCE P. aeruginosa is a soil dwelling bacterium and a plant pathogen, and it also causes life-threatening infections in humans. Thus, P. aeruginosa thrives in diverse environments and over a broad range of temperatures. Some P. aeruginosa strains rely on the CRISPR-Cas adaptive immune system as a phage defense mechanism. Our discovery that low temperatures increase CRISPR adaptation suggests that the rarely occurring but crucial naive adaptation events may take place predominantly under conditions of slow growth, e.g., during the bacterium’s soil dwelling existence and during slow growth in biofilms. |
| first_indexed | 2024-12-23T03:20:16Z |
| format | Article |
| id | doaj.art-b926fdf6b8094ab89adcd9387db50d15 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-23T03:20:16Z |
| publishDate | 2018-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-b926fdf6b8094ab89adcd9387db50d152022-12-21T18:02:02ZengAmerican Society for MicrobiologymBio2150-75112018-12-019610.1128/mBio.02184-18Temperature, by Controlling Growth Rate, Regulates CRISPR-Cas Activity in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>Nina Molin Høyland-Kroghsbo0Katrina Arcelia Muñoz1Bonnie L. Bassler2Department of Molecular Biology, Princeton University, Princeton, New Jersey, USADepartment of Molecular Biology, Princeton University, Princeton, New Jersey, USADepartment of Molecular Biology, Princeton University, Princeton, New Jersey, USAABSTRACT Clustered regularly interspaced short palindromic repeat (CRISPR)-associated (CRISPR-Cas) systems are adaptive defense systems that protect bacteria and archaea from invading genetic elements. In Pseudomonas aeruginosa, quorum sensing (QS) induces the CRISPR-Cas defense system at high cell density when the risk of bacteriophage infection is high. Here, we show that another cue, temperature, modulates P. aeruginosa CRISPR-Cas. Increased CRISPR adaptation occurs at environmental (i.e., low) temperatures compared to that at body (i.e., high) temperature. This increase is a consequence of the accumulation of CRISPR-Cas complexes, coupled with reduced P. aeruginosa growth rate at the lower temperature, the latter of which provides additional time prior to cell division for CRISPR-Cas to patrol the cell and successfully eliminate and/or acquire immunity to foreign DNA. Analyses of a QS mutant and synthetic QS compounds show that the QS and temperature cues act synergistically. The diversity and level of phage encountered by P. aeruginosa in the environment exceed that in the human body, presumably warranting increased reliance on CRISPR-Cas at environmental temperatures. IMPORTANCE P. aeruginosa is a soil dwelling bacterium and a plant pathogen, and it also causes life-threatening infections in humans. Thus, P. aeruginosa thrives in diverse environments and over a broad range of temperatures. Some P. aeruginosa strains rely on the CRISPR-Cas adaptive immune system as a phage defense mechanism. Our discovery that low temperatures increase CRISPR adaptation suggests that the rarely occurring but crucial naive adaptation events may take place predominantly under conditions of slow growth, e.g., during the bacterium’s soil dwelling existence and during slow growth in biofilms.https://journals.asm.org/doi/10.1128/mBio.02184-18CRISPRphagePseudomonasquorum sensinggrowth rate |
| spellingShingle | Nina Molin Høyland-Kroghsbo Katrina Arcelia Muñoz Bonnie L. Bassler Temperature, by Controlling Growth Rate, Regulates CRISPR-Cas Activity in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> mBio CRISPR phage Pseudomonas quorum sensing growth rate |
| title | Temperature, by Controlling Growth Rate, Regulates CRISPR-Cas Activity in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> |
| title_full | Temperature, by Controlling Growth Rate, Regulates CRISPR-Cas Activity in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> |
| title_fullStr | Temperature, by Controlling Growth Rate, Regulates CRISPR-Cas Activity in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> |
| title_full_unstemmed | Temperature, by Controlling Growth Rate, Regulates CRISPR-Cas Activity in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> |
| title_short | Temperature, by Controlling Growth Rate, Regulates CRISPR-Cas Activity in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> |
| title_sort | temperature by controlling growth rate regulates crispr cas activity in named content content type genus species pseudomonas aeruginosa named content |
| topic | CRISPR phage Pseudomonas quorum sensing growth rate |
| url | https://journals.asm.org/doi/10.1128/mBio.02184-18 |
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