A feed-forward signalling circuit controls bacterial virulence through linking cyclic di-GMP and two mechanistically distinct sRNAs, ArcZ and RsmB

Xiaochen Yuan; Quan Zeng; Devanshi Khokhani; Fang Tian; Geoffrey B. Severin; Christopher M. Waters; Jingsheng Xu; Xiang Zhou; George W. Sundin; Abasiofiok M. Ibekwe; Fengquan Liu; Ching Hong Yang

doi:10.1111/1462-2920.14603

A feed-forward signalling circuit controls bacterial virulence through linking cyclic di-GMP and two mechanistically distinct sRNAs, ArcZ and RsmB

Xiaochen Yuan, Quan Zeng, Devanshi Khokhani, Fang Tian, Geoffrey B. Severin, Christopher M. Waters, Jingsheng Xu, Xiang Zhou, George W. Sundin, Abasiofiok M. Ibekwe, Fengquan Liu, Ching Hong Yang

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Abstract

Dickeya dadantii is a plant pathogen that causes soft rot disease on vegetable and potato crops. To successfully cause infection, this pathogen needs to coordinately modulate the expression of genes encoding several virulence determinants, including plant cell wall degrading enzymes (PCWDEs), type III secretion system (T3SS) and flagellar motility. Here, we uncover a novel feed-forward signalling circuit for controlling virulence. Global RNA chaperone Hfq interacts with an Hfq-dependent sRNA ArcZ and represses the translation of pecT, encoding a LysR-type transcriptional regulator. We demonstrate that the ability of ArcZ to be processed to a 50 nt 3′- end fragment is essential for its regulation of pecT. PecT down-regulates PCWDE and the T3SS by repressing the expression of a global post-transcriptional regulator- (RsmA-) associated sRNA encoding gene rsmB. In addition, we show that the protein levels of two cyclic di-GMP (c-di-GMP) diguanylate cyclases (DGCs), GcpA and GcpL, are repressed by Hfq. Further studies show that both DGCs are essential for the Hfq-mediated post-transcriptional regulation on RsmB. Overall, our report provides new insights into the interplays between ubiquitous signalling transduction systems that were most studied independently and sheds light on multitiered regulatory mechanisms for a precise disease regulation in bacteria.

Original language	English (US)
Pages (from-to)	2755-2771
Number of pages	17
Journal	Environmental microbiology
Volume	21
Issue number	8
DOIs	https://doi.org/10.1111/1462-2920.14603
State	Published - 2019
Externally published	Yes

Bibliographical note

Funding Information:
X.Y. was supported by the Postdoctoral Workstation of Jiangsu Academy of Agricultural Sciences. This work is funded by United States Department of Agriculture-National Institute of Food and Agriculture-Exploratory Research[2016-67030-24856 to Q.Z. and C.-H.Y.]; and United States Department of Agriculture-National Institute of Food and Agriculture-Organic Transitions [2017-51106-27001 to Q.Z., B.T.S., G.W.S., J.C.W. and C.-H.Y.]; Research Growth Initiative of the University of Wisconsin-Milwaukee (to C.-H.Y.). National Institutes of Health grants [GM109259, AI130554 to C.M.W.]. Earmarked Fund for China Agriculture Research System [CARS-28-16 to F.L.]. B.T.S. and J.C.W. represent Blaire T. Steven and Jason C. White. The funders had no role in study design, data collection and interpretation or the decision to submit the work for publication.

Publisher Copyright:
© 2019 Society for Applied Microbiology and John Wiley & Sons Ltd.

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10.1111/1462-2920.14603

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Yuan, X., Zeng, Q., Khokhani, D., Tian, F., Severin, G. B., Waters, C. M., Xu, J., Zhou, X., Sundin, G. W., Ibekwe, A. M., Liu, F., & Yang, C. H. (2019). A feed-forward signalling circuit controls bacterial virulence through linking cyclic di-GMP and two mechanistically distinct sRNAs, ArcZ and RsmB. Environmental microbiology, 21(8), 2755-2771. https://doi.org/10.1111/1462-2920.14603

Yuan, X, Zeng, Q, Khokhani, D, Tian, F, Severin, GB, Waters, CM, Xu, J, Zhou, X, Sundin, GW, Ibekwe, AM, Liu, F & Yang, CH 2019, 'A feed-forward signalling circuit controls bacterial virulence through linking cyclic di-GMP and two mechanistically distinct sRNAs, ArcZ and RsmB', Environmental microbiology, vol. 21, no. 8, pp. 2755-2771. https://doi.org/10.1111/1462-2920.14603

@article{c2e44f54cc8d47cd93a1cbfda2e6af27,

title = "A feed-forward signalling circuit controls bacterial virulence through linking cyclic di-GMP and two mechanistically distinct sRNAs, ArcZ and RsmB",

abstract = "Dickeya dadantii is a plant pathogen that causes soft rot disease on vegetable and potato crops. To successfully cause infection, this pathogen needs to coordinately modulate the expression of genes encoding several virulence determinants, including plant cell wall degrading enzymes (PCWDEs), type III secretion system (T3SS) and flagellar motility. Here, we uncover a novel feed-forward signalling circuit for controlling virulence. Global RNA chaperone Hfq interacts with an Hfq-dependent sRNA ArcZ and represses the translation of pecT, encoding a LysR-type transcriptional regulator. We demonstrate that the ability of ArcZ to be processed to a 50 nt 3′- end fragment is essential for its regulation of pecT. PecT down-regulates PCWDE and the T3SS by repressing the expression of a global post-transcriptional regulator- (RsmA-) associated sRNA encoding gene rsmB. In addition, we show that the protein levels of two cyclic di-GMP (c-di-GMP) diguanylate cyclases (DGCs), GcpA and GcpL, are repressed by Hfq. Further studies show that both DGCs are essential for the Hfq-mediated post-transcriptional regulation on RsmB. Overall, our report provides new insights into the interplays between ubiquitous signalling transduction systems that were most studied independently and sheds light on multitiered regulatory mechanisms for a precise disease regulation in bacteria.",

author = "Xiaochen Yuan and Quan Zeng and Devanshi Khokhani and Fang Tian and Severin, {Geoffrey B.} and Waters, {Christopher M.} and Jingsheng Xu and Xiang Zhou and Sundin, {George W.} and Ibekwe, {Abasiofiok M.} and Fengquan Liu and Yang, {Ching Hong}",

note = "Funding Information: X.Y. was supported by the Postdoctoral Workstation of Jiangsu Academy of Agricultural Sciences. This work is funded by United States Department of Agriculture-National Institute of Food and Agriculture-Exploratory Research[2016-67030-24856 to Q.Z. and C.-H.Y.]; and United States Department of Agriculture-National Institute of Food and Agriculture-Organic Transitions [2017-51106-27001 to Q.Z., B.T.S., G.W.S., J.C.W. and C.-H.Y.]; Research Growth Initiative of the University of Wisconsin-Milwaukee (to C.-H.Y.). National Institutes of Health grants [GM109259, AI130554 to C.M.W.]. Earmarked Fund for China Agriculture Research System [CARS-28-16 to F.L.]. B.T.S. and J.C.W. represent Blaire T. Steven and Jason C. White. The funders had no role in study design, data collection and interpretation or the decision to submit the work for publication. Publisher Copyright: {\textcopyright} 2019 Society for Applied Microbiology and John Wiley & Sons Ltd.",

year = "2019",

doi = "10.1111/1462-2920.14603",

language = "English (US)",

volume = "21",

pages = "2755--2771",

journal = "Environmental microbiology",

issn = "1462-2912",

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T1 - A feed-forward signalling circuit controls bacterial virulence through linking cyclic di-GMP and two mechanistically distinct sRNAs, ArcZ and RsmB

AU - Yuan, Xiaochen

AU - Zeng, Quan

AU - Khokhani, Devanshi

AU - Tian, Fang

AU - Severin, Geoffrey B.

AU - Waters, Christopher M.

AU - Xu, Jingsheng

AU - Zhou, Xiang

AU - Sundin, George W.

AU - Ibekwe, Abasiofiok M.

AU - Liu, Fengquan

AU - Yang, Ching Hong

N1 - Funding Information: X.Y. was supported by the Postdoctoral Workstation of Jiangsu Academy of Agricultural Sciences. This work is funded by United States Department of Agriculture-National Institute of Food and Agriculture-Exploratory Research[2016-67030-24856 to Q.Z. and C.-H.Y.]; and United States Department of Agriculture-National Institute of Food and Agriculture-Organic Transitions [2017-51106-27001 to Q.Z., B.T.S., G.W.S., J.C.W. and C.-H.Y.]; Research Growth Initiative of the University of Wisconsin-Milwaukee (to C.-H.Y.). National Institutes of Health grants [GM109259, AI130554 to C.M.W.]. Earmarked Fund for China Agriculture Research System [CARS-28-16 to F.L.]. B.T.S. and J.C.W. represent Blaire T. Steven and Jason C. White. The funders had no role in study design, data collection and interpretation or the decision to submit the work for publication. Publisher Copyright: © 2019 Society for Applied Microbiology and John Wiley & Sons Ltd.

PY - 2019

Y1 - 2019

N2 - Dickeya dadantii is a plant pathogen that causes soft rot disease on vegetable and potato crops. To successfully cause infection, this pathogen needs to coordinately modulate the expression of genes encoding several virulence determinants, including plant cell wall degrading enzymes (PCWDEs), type III secretion system (T3SS) and flagellar motility. Here, we uncover a novel feed-forward signalling circuit for controlling virulence. Global RNA chaperone Hfq interacts with an Hfq-dependent sRNA ArcZ and represses the translation of pecT, encoding a LysR-type transcriptional regulator. We demonstrate that the ability of ArcZ to be processed to a 50 nt 3′- end fragment is essential for its regulation of pecT. PecT down-regulates PCWDE and the T3SS by repressing the expression of a global post-transcriptional regulator- (RsmA-) associated sRNA encoding gene rsmB. In addition, we show that the protein levels of two cyclic di-GMP (c-di-GMP) diguanylate cyclases (DGCs), GcpA and GcpL, are repressed by Hfq. Further studies show that both DGCs are essential for the Hfq-mediated post-transcriptional regulation on RsmB. Overall, our report provides new insights into the interplays between ubiquitous signalling transduction systems that were most studied independently and sheds light on multitiered regulatory mechanisms for a precise disease regulation in bacteria.

AB - Dickeya dadantii is a plant pathogen that causes soft rot disease on vegetable and potato crops. To successfully cause infection, this pathogen needs to coordinately modulate the expression of genes encoding several virulence determinants, including plant cell wall degrading enzymes (PCWDEs), type III secretion system (T3SS) and flagellar motility. Here, we uncover a novel feed-forward signalling circuit for controlling virulence. Global RNA chaperone Hfq interacts with an Hfq-dependent sRNA ArcZ and represses the translation of pecT, encoding a LysR-type transcriptional regulator. We demonstrate that the ability of ArcZ to be processed to a 50 nt 3′- end fragment is essential for its regulation of pecT. PecT down-regulates PCWDE and the T3SS by repressing the expression of a global post-transcriptional regulator- (RsmA-) associated sRNA encoding gene rsmB. In addition, we show that the protein levels of two cyclic di-GMP (c-di-GMP) diguanylate cyclases (DGCs), GcpA and GcpL, are repressed by Hfq. Further studies show that both DGCs are essential for the Hfq-mediated post-transcriptional regulation on RsmB. Overall, our report provides new insights into the interplays between ubiquitous signalling transduction systems that were most studied independently and sheds light on multitiered regulatory mechanisms for a precise disease regulation in bacteria.

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A feed-forward signalling circuit controls bacterial virulence through linking cyclic di-GMP and two mechanistically distinct sRNAs, ArcZ and RsmB

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