Cyclic di-AMP Acts as an Extracellular Signal That Impacts <italic toggle="yes">Bacillus subtilis</italic> Biofilm Formation and Plant Attachment

ABSTRACT There is a growing appreciation for the impact that bacteria have on higher organisms. Plant roots often harbor beneficial microbes, such as the Gram-positive rhizobacterium Bacillus subtilis, that influence their growth and susceptibility to disease. The ability to form surface-attached mi...

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Autores principales:	Loni Townsley, Sarah M. Yannarell, Tuanh Ngoc Huynh, Joshua J. Woodward, Elizabeth A. Shank
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Arabidopsis thaliana Bacillus subtilis biofilms cell-cell interaction cyclic di-AMP plant-microbe interactions Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/12d99e2d31b84efd9a303e5d23a632c7
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spelling	oai:doaj.org-article:12d99e2d31b84efd9a303e5d23a632c72021-11-15T15:53:27ZCyclic di-AMP Acts as an Extracellular Signal That Impacts <italic toggle="yes">Bacillus subtilis</italic> Biofilm Formation and Plant Attachment10.1128/mBio.00341-182150-7511https://doaj.org/article/12d99e2d31b84efd9a303e5d23a632c72018-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00341-18https://doaj.org/toc/2150-7511ABSTRACT There is a growing appreciation for the impact that bacteria have on higher organisms. Plant roots often harbor beneficial microbes, such as the Gram-positive rhizobacterium Bacillus subtilis, that influence their growth and susceptibility to disease. The ability to form surface-attached microbial communities called biofilms is crucial for the ability of B. subtilis to adhere to and protect plant roots. In this study, strains harboring deletions of the B. subtilis genes known to synthesize and degrade the second messenger cyclic di-adenylate monophosphate (c-di-AMP) were examined for their involvement in biofilm formation and plant attachment. We found that intracellular production of c-di-AMP impacts colony biofilm architecture, biofilm gene expression, and plant attachment in B. subtilis. We also show that B. subtilis secretes c-di-AMP and that putative c-di-AMP transporters impact biofilm formation and plant root colonization. Taken together, our data describe a new role for c-di-AMP as a chemical signal that affects important cellular processes in the environmentally and agriculturally important soil bacterium B. subtilis. These results suggest that the “intracellular” signaling molecule c-di-AMP may also play a previously unappreciated role in interbacterial cell-cell communication within plant microbiomes. IMPORTANCE Plants harbor bacterial communities on their roots that can significantly impact their growth and pathogen resistance. In most cases, however, the signals that mediate host-microbe and microbe-microbe interactions within these communities are unknown. A detailed understanding of these interaction mechanisms could facilitate the manipulation of these communities for agricultural or environmental purposes. Bacillus subtilis is a plant-growth-promoting bacterium that adheres to roots by forming biofilms. We therefore began by exploring signals that might impact its biofilm formation. We found that B. subtilis secretes c-di-AMP and that the ability to produce, degrade, or transport cyclic di-adenylate monophosphate (c-di-AMP; a common bacterial second messenger) affects B. subtilis biofilm gene expression and plant attachment. To our knowledge, this is the first demonstration of c-di-AMP impacting a mutualist host-microbe association and suggests that c-di-AMP may function as a previously unappreciated extracellular signal able to mediate interactions within plant microbiomes.Loni TownsleySarah M. YannarellTuanh Ngoc HuynhJoshua J. WoodwardElizabeth A. ShankAmerican Society for MicrobiologyarticleArabidopsis thalianaBacillus subtilisbiofilmscell-cell interactioncyclic di-AMPplant-microbe interactionsMicrobiologyQR1-502ENmBio, Vol 9, Iss 2 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Arabidopsis thaliana Bacillus subtilis biofilms cell-cell interaction cyclic di-AMP plant-microbe interactions Microbiology QR1-502
spellingShingle	Arabidopsis thaliana Bacillus subtilis biofilms cell-cell interaction cyclic di-AMP plant-microbe interactions Microbiology QR1-502 Loni Townsley Sarah M. Yannarell Tuanh Ngoc Huynh Joshua J. Woodward Elizabeth A. Shank Cyclic di-AMP Acts as an Extracellular Signal That Impacts <italic toggle="yes">Bacillus subtilis</italic> Biofilm Formation and Plant Attachment
description	ABSTRACT There is a growing appreciation for the impact that bacteria have on higher organisms. Plant roots often harbor beneficial microbes, such as the Gram-positive rhizobacterium Bacillus subtilis, that influence their growth and susceptibility to disease. The ability to form surface-attached microbial communities called biofilms is crucial for the ability of B. subtilis to adhere to and protect plant roots. In this study, strains harboring deletions of the B. subtilis genes known to synthesize and degrade the second messenger cyclic di-adenylate monophosphate (c-di-AMP) were examined for their involvement in biofilm formation and plant attachment. We found that intracellular production of c-di-AMP impacts colony biofilm architecture, biofilm gene expression, and plant attachment in B. subtilis. We also show that B. subtilis secretes c-di-AMP and that putative c-di-AMP transporters impact biofilm formation and plant root colonization. Taken together, our data describe a new role for c-di-AMP as a chemical signal that affects important cellular processes in the environmentally and agriculturally important soil bacterium B. subtilis. These results suggest that the “intracellular” signaling molecule c-di-AMP may also play a previously unappreciated role in interbacterial cell-cell communication within plant microbiomes. IMPORTANCE Plants harbor bacterial communities on their roots that can significantly impact their growth and pathogen resistance. In most cases, however, the signals that mediate host-microbe and microbe-microbe interactions within these communities are unknown. A detailed understanding of these interaction mechanisms could facilitate the manipulation of these communities for agricultural or environmental purposes. Bacillus subtilis is a plant-growth-promoting bacterium that adheres to roots by forming biofilms. We therefore began by exploring signals that might impact its biofilm formation. We found that B. subtilis secretes c-di-AMP and that the ability to produce, degrade, or transport cyclic di-adenylate monophosphate (c-di-AMP; a common bacterial second messenger) affects B. subtilis biofilm gene expression and plant attachment. To our knowledge, this is the first demonstration of c-di-AMP impacting a mutualist host-microbe association and suggests that c-di-AMP may function as a previously unappreciated extracellular signal able to mediate interactions within plant microbiomes.
format	article
author	Loni Townsley Sarah M. Yannarell Tuanh Ngoc Huynh Joshua J. Woodward Elizabeth A. Shank
author_facet	Loni Townsley Sarah M. Yannarell Tuanh Ngoc Huynh Joshua J. Woodward Elizabeth A. Shank
author_sort	Loni Townsley
title	Cyclic di-AMP Acts as an Extracellular Signal That Impacts <italic toggle="yes">Bacillus subtilis</italic> Biofilm Formation and Plant Attachment
title_short	Cyclic di-AMP Acts as an Extracellular Signal That Impacts <italic toggle="yes">Bacillus subtilis</italic> Biofilm Formation and Plant Attachment
title_full	Cyclic di-AMP Acts as an Extracellular Signal That Impacts <italic toggle="yes">Bacillus subtilis</italic> Biofilm Formation and Plant Attachment
title_fullStr	Cyclic di-AMP Acts as an Extracellular Signal That Impacts <italic toggle="yes">Bacillus subtilis</italic> Biofilm Formation and Plant Attachment
title_full_unstemmed	Cyclic di-AMP Acts as an Extracellular Signal That Impacts <italic toggle="yes">Bacillus subtilis</italic> Biofilm Formation and Plant Attachment
title_sort	cyclic di-amp acts as an extracellular signal that impacts <italic toggle="yes">bacillus subtilis</italic> biofilm formation and plant attachment
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/12d99e2d31b84efd9a303e5d23a632c7
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Cyclic di-AMP Acts as an Extracellular Signal That Impacts <italic toggle="yes">Bacillus subtilis</italic> Biofilm Formation and Plant Attachment

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