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Title: Cyclic di-AMP Acts as an Extracellular Signal That Impacts Bacillus subtilis Biofilm Formation and Plant Attachment

Abstract

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 rhizobacteriumBacillus subtilis, that influence their growth and susceptibility to disease. The ability to form surface-attached microbial communities called biofilms is crucial for the ability ofB. subtilisto adhere to and protect plant roots. In this study, strains harboring deletions of theB. subtilisgenes 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 inB. subtilis. We also show thatB. subtilissecretes 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 bacteriumB. 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. IMPORTANCEPlants 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 interactionsmore » 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 subtilisis 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 thatB. subtilissecretes c-di-AMP and that the ability to produce, degrade, or transport cyclic di-adenylate monophosphate (c-di-AMP; a common bacterial second messenger) affectsB. subtilisbiofilm 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.« less

Authors:
 [1];  [1];  [2];  [2]; ORCiD logo [1];  [3]
  1. Univ. of North Carolina, Chapel Hill, NC (United States)
  2. Univ. of Washington, Seattle, WA (United States)
  3. Massachusetts General Hospital, Boston, MA (United States)
Publication Date:
Research Org.:
Univ. of North Carolina, Chapel Hill, NC (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1510520
Grant/Contract Number:  
SC0013887
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 9; Journal Issue: 2; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Arabidopsis thaliana; Bacillus subtilis; biofilms; cell-cell interaction; cyclic di-AMP; plant-microbe interactions

Citation Formats

Townsley, Loni, Yannarell, Sarah M., Huynh, Tuanh Ngoc, Woodward, Joshua J., Shank, Elizabeth A., and Ausubel, Frederick M. Cyclic di-AMP Acts as an Extracellular Signal That Impacts Bacillus subtilis Biofilm Formation and Plant Attachment. United States: N. p., 2018. Web. doi:10.1128/mbio.00341-18.
Townsley, Loni, Yannarell, Sarah M., Huynh, Tuanh Ngoc, Woodward, Joshua J., Shank, Elizabeth A., & Ausubel, Frederick M. Cyclic di-AMP Acts as an Extracellular Signal That Impacts Bacillus subtilis Biofilm Formation and Plant Attachment. United States. doi:10.1128/mbio.00341-18.
Townsley, Loni, Yannarell, Sarah M., Huynh, Tuanh Ngoc, Woodward, Joshua J., Shank, Elizabeth A., and Ausubel, Frederick M. Tue . "Cyclic di-AMP Acts as an Extracellular Signal That Impacts Bacillus subtilis Biofilm Formation and Plant Attachment". United States. doi:10.1128/mbio.00341-18. https://www.osti.gov/servlets/purl/1510520.
@article{osti_1510520,
title = {Cyclic di-AMP Acts as an Extracellular Signal That Impacts Bacillus subtilis Biofilm Formation and Plant Attachment},
author = {Townsley, Loni and Yannarell, Sarah M. and Huynh, Tuanh Ngoc and Woodward, Joshua J. and Shank, Elizabeth A. and Ausubel, Frederick M.},
abstractNote = {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 rhizobacteriumBacillus subtilis, that influence their growth and susceptibility to disease. The ability to form surface-attached microbial communities called biofilms is crucial for the ability ofB. subtilisto adhere to and protect plant roots. In this study, strains harboring deletions of theB. subtilisgenes 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 inB. subtilis. We also show thatB. subtilissecretes 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 bacteriumB. 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. IMPORTANCEPlants 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 subtilisis 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 thatB. subtilissecretes c-di-AMP and that the ability to produce, degrade, or transport cyclic di-adenylate monophosphate (c-di-AMP; a common bacterial second messenger) affectsB. subtilisbiofilm 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.},
doi = {10.1128/mbio.00341-18},
journal = {mBio (Online)},
number = 2,
volume = 9,
place = {United States},
year = {2018},
month = {3}
}

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