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 »
- Authors:
-
[1];
- Univ. of North Carolina, Chapel Hill, NC (United States)
- Univ. of Washington, Seattle, WA (United States)
- Massachusetts General Hospital, Boston, MA (United States)
- Publication Date:
- Research Org.:
- University of North Carolina, Chapel Hill, NC (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- 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. https://doi.org/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. https://doi.org/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}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 46 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Control of cell fate by the formation of an architecturally complex bacterial community
journal, April 2008
- Vlamakis, H.; Aguilar, C.; Losick, R.
- Genes & Development, Vol. 22, Issue 7
Bacterial volatiles promote growth in Arabidopsis
journal, April 2003
- Ryu, C. -M.; Farag, M. A.; Hu, C. -H.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 8
The ydaO motif is an ATP-sensing riboswitch in Bacillus subtilis
journal, October 2012
- Watson, Peter Y.; Fedor, Martha J.
- Nature Chemical Biology, Vol. 8, Issue 12
Plant-Growth-Promoting Rhizobacteria
journal, October 2009
- Lugtenberg, Ben; Kamilova, Faina
- Annual Review of Microbiology, Vol. 63, Issue 1
c-di-AMP Is a New Second Messenger in Staphylococcus aureus with a Role in Controlling Cell Size and Envelope Stress
journal, September 2011
- Corrigan, Rebecca M.; Abbott, James C.; Burhenne, Heike
- PLoS Pathogens, Vol. 7, Issue 9
Construction of a single-copy integration vector and its use in analysis of regulation of the trp operon of Bacillus subtilis
journal, January 1986
- Hidenori, Shimotsu; Henner, Dennis J.
- Gene, Vol. 43, Issue 1-2
Systematic identification of conserved bacterial c-di-AMP receptor proteins
journal, May 2013
- Corrigan, R. M.; Campeotto, I.; Jeganathan, T.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 22
Bacterial Volatiles Induce Systemic Resistance in Arabidopsis
journal, February 2004
- Ryu, Choong-Min; Farag, Mohamed A.; Hu, Chia-Hui
- Plant Physiology, Vol. 134, Issue 3
Induced Systemic Resistance and Promotion of Plant Growth by Bacillus spp.
journal, November 2004
- Kloepper, Joseph W.; Ryu, Choong-Min; Zhang, Shouan
- Phytopathology, Vol. 94, Issue 11
Great Times for Small Molecules: c-di-AMP, a Second Messenger Candidate in Bacteria and Archaea
journal, August 2008
- Romling, U.
- Science Signaling, Vol. 1, Issue 33
A jack of all trades: the multiple roles of the unique essential second messenger cyclic di-AMP: C-di-AMP signaling in bacteria
journal, May 2015
- Commichau, Fabian M.; Dickmanns, Achim; Gundlach, Jan
- Molecular Microbiology, Vol. 97, Issue 2
Cyclic di-AMP mediates biofilm formation: c-di-AMP mediates biofilm formation
journal, December 2015
- Peng, Xian; Zhang, Yang; Bai, Guangchun
- Molecular Microbiology, Vol. 99, Issue 5
Substrate flow in the rhizosphere
journal, December 1990
- Lynch, J. M.; Whipps, J. M.
- Plant and Soil, Vol. 129, Issue 1
Bacillus subtilis biofilm induction by plant polysaccharides
journal, April 2013
- Beauregard, P. B.; Chai, Y.; Vlamakis, H.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 17
An HD-domain phosphodiesterase mediates cooperative hydrolysis of c-di-AMP to affect bacterial growth and virulence
journal, January 2015
- Huynh, TuAnh Ngoc; Luo, Shukun; Pensinger, Daniel
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 7
Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation
journal, August 2012
- Chen, Yun; Yan, Fang; Chai, Yunrong
- Environmental Microbiology, Vol. 15, Issue 3
Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively
journal, April 1998
- Vogel, J. P.; Woeste, K. E.; Theologis, A.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 8
Deletion of the cyclic di-AMP phosphodiesterase gene ( cnpB ) in M ycobacterium tuberculosis leads to reduced virulence in a mouse model of infection
journal, May 2014
- Yang, Jun; Bai, Yinlan; Zhang, Yang
- Molecular Microbiology, Vol. 93, Issue 1
Control of the Diadenylate Cyclase CdaS in Bacillus subtilis : AN AUTOINHIBITORY DOMAIN LIMITS CYCLIC DI-AMP PRODUCTION
journal, June 2014
- Mehne, Felix M. P.; Schröder-Tittmann, Kathrin; Eijlander, Robyn T.
- Journal of Biological Chemistry, Vol. 289, Issue 30
Second Messenger Signaling in Bacillus subtilis: Accumulation of Cyclic di-AMP Inhibits Biofilm Formation
journal, May 2016
- Gundlach, Jan; Rath, Hermann; Herzberg, Christina
- Frontiers in Microbiology, Vol. 7
Root-Secreted Malic Acid Recruits Beneficial Soil Bacteria
journal, September 2008
- Rudrappa, Thimmaraju; Czymmek, Kirk J.; Paré, Paul W.
- Plant Physiology, Vol. 148, Issue 3
NIH Image to ImageJ: 25 years of image analysis
journal, June 2012
- Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
- Nature Methods, Vol. 9, Issue 7
Interspecies Chemical Communication in Bacterial Development
journal, October 2009
- Straight, Paul D.; Kolter, Roberto
- Annual Review of Microbiology, Vol. 63, Issue 1
Structural Biochemistry of a Bacterial Checkpoint Protein Reveals Diadenylate Cyclase Activity Regulated by DNA Recombination Intermediates
journal, April 2008
- Witte, Gregor; Hartung, Sophia; Büttner, Katharina
- Molecular Cell, Vol. 30, Issue 2
New shuttle vectors for ectopic insertion of genes into Bacillus subtilis
journal, May 2004
- Middleton, Rebecca; Hofmeister, Antje
- Plasmid, Vol. 51, Issue 3
YybT Is a Signaling Protein That Contains a Cyclic Dinucleotide Phosphodiesterase Domain and a GGDEF Domain with ATPase Activity
journal, November 2009
- Rao, Feng; See, Rui Yin; Zhang, Dongwei
- Journal of Biological Chemistry, Vol. 285, Issue 1
c-di-AMP Secreted by Intracellular Listeria monocytogenes Activates a Host Type I Interferon Response
journal, May 2010
- Woodward, J. J.; Iavarone, A. T.; Portnoy, D. A.
- Science, Vol. 328, Issue 5986
Cyclic diguanylate regulation of Bacillus cereus group biofilm formation : c-di-GMP regulation of
journal, June 2016
- Fagerlund, Annette; Smith, Veronika; Røhr, Åsmund K.
- Molecular Microbiology, Vol. 101, Issue 3
Too much of a good thing: regulated depletion of c-di-AMP in the bacterial cytoplasm
journal, April 2016
- Huynh, TuAnh Ngoc; Woodward, Joshua J.
- Current Opinion in Microbiology, Vol. 30
Cyclic di-GMP: the First 25 Years of a Universal Bacterial Second Messenger
journal, March 2013
- Romling, U.; Galperin, M. Y.; Gomelsky, M.
- Microbiology and Molecular Biology Reviews, Vol. 77, Issue 1
Cyclic di-AMP: another second messenger enters the fray
journal, July 2013
- Corrigan, Rebecca M.; Gründling, Angelika
- Nature Reviews Microbiology, Vol. 11, Issue 8
Functional Characterization of Core Components of the Bacillus subtilis Cyclic-Di-GMP Signaling Pathway
journal, July 2013
- Gao, X.; Mukherjee, S.; Matthews, P. M.
- Journal of Bacteriology, Vol. 195, Issue 21
Isolation and characterization of antagonistic Bacillus subtilis strains from the avocado rhizoplane displaying biocontrol activity: Characterization of antagonistic Bacillus
journal, June 2007
- Cazorla, F. M.; Romero, D.; Pérez-García, A.
- Journal of Applied Microbiology, Vol. 103, Issue 5
Amyloid fibers provide structural integrity to Bacillus subtilis biofilms
journal, January 2010
- Romero, D.; Aguilar, C.; Losick, R.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 5
A Checkpoint Protein That Scans the Chromosome for Damage at the Start of Sporulation in Bacillus subtilis
journal, May 2006
- Bejerano-Sagie, Michal; Oppenheimer-Shaanan, Yaara; Berlatzky, Idit
- Cell, Vol. 125, Issue 4
The rhizosphere microbiome and plant health
journal, August 2012
- Berendsen, Roeland L.; Pieterse, Corné M. J.; Bakker, Peter A. H. M.
- Trends in Plant Science, Vol. 17, Issue 8
BslA(YuaB) forms a hydrophobic layer on the surface of Bacillus subtilis biofilms: Bacillus subtilis BslA
journal, May 2012
- Kobayashi, Kazuo; Iwano, Megumi
- Molecular Microbiology, Vol. 85, Issue 1
Plant methyl salicylate induces defense responses in the rhizobacterium B acillus subtilis : MeSA induces defense responses in
journal, October 2014
- Kobayashi, Kazuo
- Environmental Microbiology, Vol. 17, Issue 4
Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis
journal, December 2008
- Lopez, D.; Fischbach, M. A.; Chu, F.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 1
Bacillus subtilis Early Colonization of Arabidopsis thaliana Roots Involves Multiple Chemotaxis Receptors
journal, November 2016
- Allard-Massicotte, Rosalie; Tessier, Laurence; Lécuyer, Frédéric
- mBio, Vol. 7, Issue 6
c-di-AMP reports DNA integrity during sporulation in Bacillus subtilis
journal, May 2011
- Oppenheimer-Shaanan, Yaara; Wexselblatt, Ezequiel; Katzhendler, Jehoshua
- EMBO reports, Vol. 12, Issue 6
Extracellular DNA Release by Undomesticated Bacillus subtilis Is Regulated by Early Competence
journal, November 2012
- Zafra, Olga; Lamprecht-Grandío, María; de Figueras, Carolina González
- PLoS ONE, Vol. 7, Issue 11
Control of potassium homeostasis is an essential function of the second messenger cyclic di-AMP in Bacillus subtilis
journal, April 2017
- Gundlach, Jan; Herzberg, Christina; Kaever, Volkhard
- Science Signaling, Vol. 10, Issue 475
Factors other than root secreted malic acid that contributes toward Bacillus subtilis FB17 colonization on Arabidopsis roots
journal, November 2013
- Lakshmanan, Venkatachalam; Bais, Harsh P.
- Plant Signaling & Behavior, Vol. 8, Issue 11
Characteristics of an inulinase produced by Bacillus subtilis 430A, a strain isolated from the rhizosphere of Vernonia herbacea (Vell Rusby).
journal, January 1991
- Vullo, D. L.; Coto, C. E.; Siñeriz, F.
- Applied and Environmental Microbiology, Vol. 57, Issue 8
YybT is a signaling protein that contains a cyclic dinucleotide phosphodiesterase domain and a GGDEF domain with ATPase activity.
journal, August 2011
- Rao, Feng; See, Rui Yin; Zhang, Dongwei
- Journal of Biological Chemistry, Vol. 286, Issue 33
Control of cell fate by the formation of an architecturally complex bacterial community
text, January 2008
- Vlamakis, H.; Aguilar, C.; Losick, R.
- Cold Spring Harbor Laboratory Press
Drilling accurate nanopores for biosensors by energetic multi-wall carbon nanotubes: a molecular dynamics investigation
journal, September 2022
- Li, Changsheng; Wang, Zilin; Ma, Lei
- Journal of Molecular Modeling, Vol. 28, Issue 10
Construction of a single-copy integration vector and its use in analysis of regulation of the trp operon of Bacillus subtilis
journal, January 1986
- Hidenori, Shimotsu; Henner, Dennis J.
- Gene, Vol. 43, Issue 1-2
Too much of a good thing: regulated depletion of c-di-AMP in the bacterial cytoplasm
journal, April 2016
- Huynh, TuAnh Ngoc; Woodward, Joshua J.
- Current Opinion in Microbiology, Vol. 30
Structural Biochemistry of a Bacterial Checkpoint Protein Reveals Diadenylate Cyclase Activity Regulated by DNA Recombination Intermediates
journal, April 2008
- Witte, Gregor; Hartung, Sophia; Büttner, Katharina
- Molecular Cell, Vol. 30, Issue 2
New shuttle vectors for ectopic insertion of genes into Bacillus subtilis
journal, May 2004
- Middleton, Rebecca; Hofmeister, Antje
- Plasmid, Vol. 51, Issue 3
The rhizosphere microbiome and plant health
journal, August 2012
- Berendsen, Roeland L.; Pieterse, Corné M. J.; Bakker, Peter A. H. M.
- Trends in Plant Science, Vol. 17, Issue 8
The ydaO motif is an ATP-sensing riboswitch in Bacillus subtilis
journal, October 2012
- Watson, Peter Y.; Fedor, Martha J.
- Nature Chemical Biology, Vol. 8, Issue 12
Cyclic di-AMP: another second messenger enters the fray
journal, July 2013
- Corrigan, Rebecca M.; Gründling, Angelika
- Nature Reviews Microbiology, Vol. 11, Issue 8
Bacterial volatiles promote growth in Arabidopsis
journal, April 2003
- Ryu, C. -M.; Farag, M. A.; Hu, C. -H.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 8
Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis
journal, December 2008
- Lopez, D.; Fischbach, M. A.; Chu, F.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 1
Amyloid fibers provide structural integrity to Bacillus subtilis biofilms
journal, January 2010
- Romero, D.; Aguilar, C.; Losick, R.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 5
Bacillus subtilis biofilm induction by plant polysaccharides
journal, April 2013
- Beauregard, P. B.; Chai, Y.; Vlamakis, H.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 17
Systematic identification of conserved bacterial c-di-AMP receptor proteins
journal, May 2013
- Corrigan, R. M.; Campeotto, I.; Jeganathan, T.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 22
An HD-domain phosphodiesterase mediates cooperative hydrolysis of c-di-AMP to affect bacterial growth and virulence
journal, January 2015
- Huynh, TuAnh Ngoc; Luo, Shukun; Pensinger, Daniel
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 7
Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively
journal, April 1998
- Vogel, J. P.; Woeste, K. E.; Theologis, A.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 8
YybT is a signaling protein that contains a cyclic dinucleotide phosphodiesterase domain and a GGDEF domain with ATPase activity.
journal, August 2011
- Rao, Feng; See, Rui Yin; Zhang, Dongwei
- Journal of Biological Chemistry, Vol. 286, Issue 33
Identification, Characterization, and Structure Analysis of the Cyclic di-AMP-binding P II -like Signal Transduction Protein DarA
journal, November 2014
- Gundlach, Jan; Dickmanns, Achim; Schröder-Tittmann, Kathrin
- Journal of Biological Chemistry, Vol. 290, Issue 5
Structural and Biochemical Analysis of the Essential Diadenylate Cyclase CdaA from Listeria monocytogenes
journal, January 2015
- Rosenberg, Jonathan; Dickmanns, Achim; Neumann, Piotr
- Journal of Biological Chemistry, Vol. 290, Issue 10
Root-Secreted Malic Acid Recruits Beneficial Soil Bacteria
journal, September 2008
- Rudrappa, Thimmaraju; Czymmek, Kirk J.; Paré, Paul W.
- Plant Physiology, Vol. 148, Issue 3
Plant methyl salicylate induces defense responses in the rhizobacterium B acillus subtilis : MeSA induces defense responses in
journal, October 2014
- Kobayashi, Kazuo
- Environmental Microbiology, Vol. 17, Issue 4
Cyclic diguanylate regulation of Bacillus cereus group biofilm formation : c-di-GMP regulation of
journal, June 2016
- Fagerlund, Annette; Smith, Veronika; Røhr, Åsmund K.
- Molecular Microbiology, Vol. 101, Issue 3
c-di-AMP Secreted by Intracellular Listeria monocytogenes Activates a Host Type I Interferon Response
journal, May 2010
- Woodward, J. J.; Iavarone, A. T.; Portnoy, D. A.
- Science, Vol. 328, Issue 5986
Control of potassium homeostasis is an essential function of the second messenger cyclic di-AMP in Bacillus subtilis
journal, April 2017
- Gundlach, Jan; Herzberg, Christina; Kaever, Volkhard
- Science Signaling, Vol. 10, Issue 475
The Characterization of a Cyclic-Di-GMP (c-Di-GMP) Pathway Leads to a New Tool for Studying c-Di-GMP Metabolic Genes
journal, November 2013
- Tamayo, Rita
- Journal of Bacteriology, Vol. 195, Issue 21
Evidence for Cyclic Di-GMP-Mediated Signaling in Bacillus subtilis
journal, July 2012
- Chen, Yun; Chai, Yunrong; Guo, Jian-hua
- Journal of Bacteriology, Vol. 194, Issue 18
KtrAB and KtrCD: Two K+ Uptake Systems in Bacillus subtilis and Their Role in Adaptation to Hypertonicity
journal, February 2003
- Holtmann, G.; Bakker, E. P.; Uozumi, N.
- Journal of Bacteriology, Vol. 185, Issue 4
STING-Dependent Recognition of Cyclic di-AMP Mediates Type I Interferon Responses during Chlamydia trachomatis Infection
journal, April 2013
- Barker, Jeffrey R.; Koestler, Benjamin J.; Carpenter, Victoria K.
- mBio, Vol. 4, Issue 3
Plant-Growth-Promoting Rhizobacteria
journal, October 2009
- Lugtenberg, Ben; Kamilova, Faina
- Annual Review of Microbiology, Vol. 63, Issue 1
c-di-AMP Is a New Second Messenger in Staphylococcus aureus with a Role in Controlling Cell Size and Envelope Stress
journal, September 2011
- Corrigan, Rebecca M.; Abbott, James C.; Burhenne, Heike
- PLoS Pathogens, Vol. 7, Issue 9
Factors other than root secreted malic acid that contributes toward Bacillus subtilis FB17 colonization on Arabidopsis roots
journal, November 2013
- Lakshmanan, Venkatachalam; Bais, Harsh P.
- Plant Signaling & Behavior, Vol. 8, Issue 11
Control of cell fate by the formation of an architecturally complex bacterial community
text, January 2008
- Vlamakis, H.; Aguilar, C.; Losick, R.
- Cold Spring Harbor Laboratory Press
Works referencing / citing this record:
Making and Breaking of an Essential Poison: the Cyclases and Phosphodiesterases That Produce and Degrade the Essential Second Messenger Cyclic di-AMP in Bacteria
journal, September 2018
- Commichau, Fabian M.; Heidemann, Jana L.; Ficner, Ralf
- Journal of Bacteriology, Vol. 201, Issue 1
Metabolic Remodeling during Biofilm Development of Bacillus subtilis
journal, May 2019
- Pisithkul, Tippapha; Schroeder, Jeremy W.; Trujillo, Edna A.
- mBio, Vol. 10, Issue 3
Enhanced uptake of potassium or glycine betaine or export of cyclic-di-AMP restores osmoresistance in a high cyclic-di-AMP Lactococcus lactis mutant
journal, August 2018
- Pham, Huong Thi; Nhiep, Nguyen Thi Hanh; Vu, Thu Ngoc Minh
- PLOS Genetics, Vol. 14, Issue 8
Homeostasis of Second Messenger Cyclic-di-AMP Is Critical for Cyanobacterial Fitness and Acclimation to Abiotic Stress
journal, May 2018
- Agostoni, Marco; Logan-Jackson, Alshaé R.; Heinz, Emily R.
- Frontiers in Microbiology, Vol. 9
Increased Intracellular Cyclic di-AMP Levels Sensitize Streptococcus gallolyticus subsp. gallolyticus to Osmotic Stress and Reduce Biofilm Formation and Adherence on Intestinal Cells
journal, January 2019
- Teh, Wooi Keong; Dramsi, Shaynoor; Tolker-Nielsen, Tim
- Journal of Bacteriology, Vol. 201, Issue 6
(p)ppGpp and CodY Promote Enterococcus faecalis Virulence in a Murine Model of Catheter-Associated Urinary Tract Infection
journal, July 2019
- Colomer-Winter, C.; Flores-Mireles, A. L.; Kundra, S.
- mSphere, Vol. 4, Issue 4
Increased Intracellular Cyclic di-AMP Levels Sensitize Streptococcus gallolyticus subsp. gallolyticus to Osmotic Stress and Reduce Biofilm Formation and Adherence on Intestinal Cells
journal, January 2019
- Teh, Wooi Keong; Dramsi, Shaynoor; Tolker-Nielsen, Tim
- Journal of Bacteriology, Vol. 201, Issue 6
Homeostasis of Second Messenger Cyclic-di-AMP Is Critical for Cyanobacterial Fitness and Acclimation to Abiotic Stress
journal, May 2018
- Agostoni, Marco; Logan-Jackson, Alshaé R.; Heinz, Emily R.
- Frontiers in Microbiology, Vol. 9