DncV Synthesizes Cyclic GMP-AMP and Regulates Biofilm Formation and Motility in <italic toggle="yes">Escherichia coli</italic> ECOR31

ABSTRACT Cyclic dinucleotides (cDNs) act as intracellular second messengers, modulating bacterial physiology to regulate the fundamental life style transition between motility and sessility commonly known as biofilm formation. Cyclic GMP-AMP (cGAMP), synthesized by the dinucleotide cyclase DncV, is...

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Autores principales:	Fengyang Li, Annika Cimdins, Manfred Rohde, Lothar Jänsch, Volkhard Kaever, Manfred Nimtz, Ute Römling
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	CsgD DncV biofilm formation cGAMP cyclic di-GMP motility Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e081f232e0af4931a7aca242428c4f4d
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spelling	oai:doaj.org-article:e081f232e0af4931a7aca242428c4f4d2021-11-15T15:55:25ZDncV Synthesizes Cyclic GMP-AMP and Regulates Biofilm Formation and Motility in <italic toggle="yes">Escherichia coli</italic> ECOR3110.1128/mBio.02492-182150-7511https://doaj.org/article/e081f232e0af4931a7aca242428c4f4d2019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02492-18https://doaj.org/toc/2150-7511ABSTRACT Cyclic dinucleotides (cDNs) act as intracellular second messengers, modulating bacterial physiology to regulate the fundamental life style transition between motility and sessility commonly known as biofilm formation. Cyclic GMP-AMP (cGAMP), synthesized by the dinucleotide cyclase DncV, is a newly discovered cDN second messenger involved in virulence and chemotaxis in Vibrio cholerae O1 biovar El Tor. Here we report a novel role for horizontally transferred DncV in cGAMP production and regulation of biofilm formation and motility in the animal commensal strain Escherichia coli ECOR31. ECOR31 expresses a semiconstitutive temperature-independent rdar (red, dry, and rough) morphotype on Congo red agar plates characterized by the extracellular matrix components cellulose and curli fimbriae which requires activation by the major biofilm regulator CsgD and cyclic di-GMP signaling. In contrast, C-terminal His-tagged DncV negatively regulates the rdar biofilm morphotype and cell aggregation via downregulation of csgD mRNA steady-state level. Furthermore, DncV sequentially promotes and inhibits adhesion to the abiotic surface after 24 h and 48 h of growth, respectively. DncV also suppresses swimming and swarming motility posttranscriptional of the class 1 flagellum regulon gene flhD. Purified DncV produced different cDNs, cyclic di-GMP, cyclic di-AMP, an unknown product(s), and the dominant species 3′3′-cGAMP. In vivo, only the 3′3′-cGAMP concentration was elevated upon short-term overexpression of dncV, making this work a first report on cGAMP production in E. coli. Regulation of rdar biofilm formation and motility upon overexpression of untagged DncV in combination with three adjacent cotransferred gene products suggests a novel temperature-dependent cGAMP signaling module in E. coli ECOR31. IMPORTANCE The ability of bacteria to sense and respond to environmental signals is critical for survival. Bacteria use cyclic dinucleotides as second messengers to regulate a number of physiological processes, such as the fundamental life style transition between motility and sessility (biofilm formation). cGAMP, which is synthesized by a dinucleotide cyclase called DncV, is a newly discovered second messenger involved in virulence and chemotaxis in the Vibrio cholerae biovar El Tor causing the current 7th cholera pandemic. However, to what extent cGAMP exists and participates in physiological processes in other bacteria is still unknown. In this study, we found an elevated cGAMP level to possibly regulate biofilm formation and motility in the animal commensal E. coli strain ECOR31. Thus, we detected a novel role for cGAMP signaling in regulation of physiological processes other than those previously reported in proteobacterial species.Fengyang LiAnnika CimdinsManfred RohdeLothar JänschVolkhard KaeverManfred NimtzUte RömlingAmerican Society for MicrobiologyarticleCsgDDncVbiofilm formationcGAMPcyclic di-GMPmotilityMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	CsgD DncV biofilm formation cGAMP cyclic di-GMP motility Microbiology QR1-502
spellingShingle	CsgD DncV biofilm formation cGAMP cyclic di-GMP motility Microbiology QR1-502 Fengyang Li Annika Cimdins Manfred Rohde Lothar Jänsch Volkhard Kaever Manfred Nimtz Ute Römling DncV Synthesizes Cyclic GMP-AMP and Regulates Biofilm Formation and Motility in <italic toggle="yes">Escherichia coli</italic> ECOR31
description	ABSTRACT Cyclic dinucleotides (cDNs) act as intracellular second messengers, modulating bacterial physiology to regulate the fundamental life style transition between motility and sessility commonly known as biofilm formation. Cyclic GMP-AMP (cGAMP), synthesized by the dinucleotide cyclase DncV, is a newly discovered cDN second messenger involved in virulence and chemotaxis in Vibrio cholerae O1 biovar El Tor. Here we report a novel role for horizontally transferred DncV in cGAMP production and regulation of biofilm formation and motility in the animal commensal strain Escherichia coli ECOR31. ECOR31 expresses a semiconstitutive temperature-independent rdar (red, dry, and rough) morphotype on Congo red agar plates characterized by the extracellular matrix components cellulose and curli fimbriae which requires activation by the major biofilm regulator CsgD and cyclic di-GMP signaling. In contrast, C-terminal His-tagged DncV negatively regulates the rdar biofilm morphotype and cell aggregation via downregulation of csgD mRNA steady-state level. Furthermore, DncV sequentially promotes and inhibits adhesion to the abiotic surface after 24 h and 48 h of growth, respectively. DncV also suppresses swimming and swarming motility posttranscriptional of the class 1 flagellum regulon gene flhD. Purified DncV produced different cDNs, cyclic di-GMP, cyclic di-AMP, an unknown product(s), and the dominant species 3′3′-cGAMP. In vivo, only the 3′3′-cGAMP concentration was elevated upon short-term overexpression of dncV, making this work a first report on cGAMP production in E. coli. Regulation of rdar biofilm formation and motility upon overexpression of untagged DncV in combination with three adjacent cotransferred gene products suggests a novel temperature-dependent cGAMP signaling module in E. coli ECOR31. IMPORTANCE The ability of bacteria to sense and respond to environmental signals is critical for survival. Bacteria use cyclic dinucleotides as second messengers to regulate a number of physiological processes, such as the fundamental life style transition between motility and sessility (biofilm formation). cGAMP, which is synthesized by a dinucleotide cyclase called DncV, is a newly discovered second messenger involved in virulence and chemotaxis in the Vibrio cholerae biovar El Tor causing the current 7th cholera pandemic. However, to what extent cGAMP exists and participates in physiological processes in other bacteria is still unknown. In this study, we found an elevated cGAMP level to possibly regulate biofilm formation and motility in the animal commensal E. coli strain ECOR31. Thus, we detected a novel role for cGAMP signaling in regulation of physiological processes other than those previously reported in proteobacterial species.
format	article
author	Fengyang Li Annika Cimdins Manfred Rohde Lothar Jänsch Volkhard Kaever Manfred Nimtz Ute Römling
author_facet	Fengyang Li Annika Cimdins Manfred Rohde Lothar Jänsch Volkhard Kaever Manfred Nimtz Ute Römling
author_sort	Fengyang Li
title	DncV Synthesizes Cyclic GMP-AMP and Regulates Biofilm Formation and Motility in <italic toggle="yes">Escherichia coli</italic> ECOR31
title_short	DncV Synthesizes Cyclic GMP-AMP and Regulates Biofilm Formation and Motility in <italic toggle="yes">Escherichia coli</italic> ECOR31
title_full	DncV Synthesizes Cyclic GMP-AMP and Regulates Biofilm Formation and Motility in <italic toggle="yes">Escherichia coli</italic> ECOR31
title_fullStr	DncV Synthesizes Cyclic GMP-AMP and Regulates Biofilm Formation and Motility in <italic toggle="yes">Escherichia coli</italic> ECOR31
title_full_unstemmed	DncV Synthesizes Cyclic GMP-AMP and Regulates Biofilm Formation and Motility in <italic toggle="yes">Escherichia coli</italic> ECOR31
title_sort	dncv synthesizes cyclic gmp-amp and regulates biofilm formation and motility in <italic toggle="yes">escherichia coli</italic> ecor31
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/e081f232e0af4931a7aca242428c4f4d
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DncV Synthesizes Cyclic GMP-AMP and Regulates Biofilm Formation and Motility in <italic toggle="yes">Escherichia coli</italic> ECOR31

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