An RNA sponge controls quorum sensing dynamics and biofilm formation in Vibrio cholerae

Michaela Huber; Anne Lippegaus; Sahar Melamed; Malte Siemers; Benjamin R. Wucher; Mona Hoyos; Carey Nadell; Gisela Storz; Kai Papenfort

doi:10.1038/s41467-022-35261-x

An RNA sponge controls quorum sensing dynamics and biofilm formation in Vibrio cholerae

Michaela Huber, Anne Lippegaus, Sahar Melamed, Malte Siemers, Benjamin R. Wucher, Mona Hoyos, Carey Nadell, Gisela Storz, Kai Papenfort^*

^*Corresponding author for this work

Department of Microbiology and Molecular Genetics

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

3 Scopus citations

Abstract

Small regulatory RNAs (sRNAs) acting in concert with the RNA chaperone Hfq are prevalent in many bacteria and typically act by base-pairing with multiple target transcripts. In the human pathogen Vibrio cholerae, sRNAs play roles in various processes including antibiotic tolerance, competence, and quorum sensing (QS). Here, we use RIL-seq (RNA-interaction-by-ligation-and-sequencing) to identify Hfq-interacting sRNAs and their targets in V. cholerae. We find hundreds of sRNA-mRNA interactions, as well as RNA duplexes formed between two sRNA regulators. Further analysis of these duplexes identifies an RNA sponge, termed QrrX, that base-pairs with and inactivates the Qrr1-4 sRNAs, which are known to modulate the QS pathway. Transcription of qrrX is activated by QrrT, a previously uncharacterized LysR-type transcriptional regulator. Our results indicate that QrrX and QrrT are required for rapid conversion from individual to community behaviours in V. cholerae.

Original language	American English
Article number	7585
Journal	Nature Communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-35261-x
State	Published - Dec 2022

Bibliographical note

Funding Information:
We thank Andreas Starick and Yvonne Greiser for excellent technical support. We thank all members of the Papenfort lab for insightful discussions and suggestions. Work in the Papenfort group was supported by the DFG (PA2820/1–2 and EXC2051 - Project‐ID 390713860), the Vallee Foundation, and the European Research Council (StG-758212).

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© 2022, The Author(s).

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title = "An RNA sponge controls quorum sensing dynamics and biofilm formation in Vibrio cholerae",

abstract = "Small regulatory RNAs (sRNAs) acting in concert with the RNA chaperone Hfq are prevalent in many bacteria and typically act by base-pairing with multiple target transcripts. In the human pathogen Vibrio cholerae, sRNAs play roles in various processes including antibiotic tolerance, competence, and quorum sensing (QS). Here, we use RIL-seq (RNA-interaction-by-ligation-and-sequencing) to identify Hfq-interacting sRNAs and their targets in V. cholerae. We find hundreds of sRNA-mRNA interactions, as well as RNA duplexes formed between two sRNA regulators. Further analysis of these duplexes identifies an RNA sponge, termed QrrX, that base-pairs with and inactivates the Qrr1-4 sRNAs, which are known to modulate the QS pathway. Transcription of qrrX is activated by QrrT, a previously uncharacterized LysR-type transcriptional regulator. Our results indicate that QrrX and QrrT are required for rapid conversion from individual to community behaviours in V. cholerae.",

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AU - Wucher, Benjamin R.

AU - Hoyos, Mona

AU - Nadell, Carey

AU - Storz, Gisela

AU - Papenfort, Kai

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N2 - Small regulatory RNAs (sRNAs) acting in concert with the RNA chaperone Hfq are prevalent in many bacteria and typically act by base-pairing with multiple target transcripts. In the human pathogen Vibrio cholerae, sRNAs play roles in various processes including antibiotic tolerance, competence, and quorum sensing (QS). Here, we use RIL-seq (RNA-interaction-by-ligation-and-sequencing) to identify Hfq-interacting sRNAs and their targets in V. cholerae. We find hundreds of sRNA-mRNA interactions, as well as RNA duplexes formed between two sRNA regulators. Further analysis of these duplexes identifies an RNA sponge, termed QrrX, that base-pairs with and inactivates the Qrr1-4 sRNAs, which are known to modulate the QS pathway. Transcription of qrrX is activated by QrrT, a previously uncharacterized LysR-type transcriptional regulator. Our results indicate that QrrX and QrrT are required for rapid conversion from individual to community behaviours in V. cholerae.

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An RNA sponge controls quorum sensing dynamics and biofilm formation in Vibrio cholerae

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