CRISPR interference to interrogate genes that control biofilm formation in Pseudomonas fluorescens

Noirot-Gros, Marie-Francoise; Forrester, Sara; Malato, Grace; Larsen, Peter E.; Noirot, Philippe

doi:10.1038/s41598-019-52400-5

Title: CRISPR interference to interrogate genes that control biofilm formation in Pseudomonas fluorescens

Journal Article · Mon Nov 04 00:00:00 EST 2019 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-019-52400-5· OSTI ID:1578041

^[1]; Forrester, Sara ^[1]; Malato, Grace ^[1]; Larsen, Peter E. ^[2]; Noirot, Philippe ^[1]

Argonne National Lab. (ANL), Argonne, IL (United States)
Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of Illinois, Chicago, IL (United States)

Bacterial biofilm formation involves signaling and regulatory pathways that control the transition from motile to sessile lifestyle, production of extracellular polymeric matrix, and maturation of the biofilm 3D structure. Biofilms are extensively studied because of their importance in biomedical, ecological and industrial settings. Gene inactivation is a powerful approach for functional studies but it is often labor intensive, limiting systematic gene surveys to the most tractable bacterial hosts. Here, we adapted the CRISPR interference (CRISPRi) system for use in diverse strain isolates of P. fluorescens, SBW25, WH6 and Pf0-1. We found that CRISPRi is applicable to study complex phenotypes such as cell morphology, motility and biofilm formation over extended periods of time. In SBW25, CRISPRi-mediated silencing of genes encoding the GacA/S two-component system and regulatory proteins associated with the cylic di-GMP signaling messenger produced swarming and biofilm phenotypes similar to those obtained after gene inactivation. Combined with detailed confocal microscopy of biofilms, our study also revealed novel phenotypes associated with extracellular matrix biosynthesis as well as the potent inhibition of SBW25 biofilm formation mediated by the PFLU1114 operon. We conclude that CRISPRi is a reliable and scalable approach to investigate gene networks in the diverse P. fluorescens group.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1578041

Journal Information:: Scientific Reports, Vol. 9, Issue 1; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 17 works

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References (90)

The bacterial divisome: ready for its close-up Rowlett, Veronica W.; Margolin, William Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1679 https://doi.org/10.1098/rstb.2015.0028	journal	October 2015
Adaptive evolution by spontaneous domain fusion and protein relocalization Farr, Andrew D.; Remigi, Philippe; Rainey, Paul B. Nature Ecology & Evolution, Vol. 1, Issue 10 https://doi.org/10.1038/s41559-017-0283-7	journal	August 2017
Redefining the roles of the FtsZ-ring in bacterial cytokinesis Xiao, Jie; Goley, Erin D. Current Opinion in Microbiology, Vol. 34 https://doi.org/10.1016/j.mib.2016.08.008	journal	December 2016
The GacS/GacA signal transduction system of Pseudomonas aeruginosa acts exclusively through its control over the transcription of the RsmY and RsmZ regulatory small RNAs Brencic, Anja; McFarland, Kirsty A.; McManus, Heather R. Molecular Microbiology, Vol. 73, Issue 3 https://doi.org/10.1111/j.1365-2958.2009.06782.x	journal	August 2009
The Standard European Vector Architecture (SEVA): a coherent platform for the analysis and deployment of complex prokaryotic phenotypes Silva-Rocha, Rafael; Martínez-García, Esteban; Calles, Belén Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1119	journal	November 2012
MreB Orientation Correlates with Cell Diameter in Escherichia coli Ouzounov, Nikolay; Nguyen, Jeffrey P.; Bratton, Benjamin P. Biophysical Journal, Vol. 111, Issue 5 https://doi.org/10.1016/j.bpj.2016.07.017	journal	September 2016
Genome Comparison of Pseudomonas fluorescens UM270 with Related Fluorescent Strains Unveils Genes Involved in Rhizosphere Competence and Colonization Hernández-Salmerón, Julie E.; Moreno-Hagelsieb, Gabriel; Santoyo, Gustavo Journal of Genomics, Vol. 5 https://doi.org/10.7150/jgen.21588	journal	January 2017
bifA Regulates Biofilm Development of Pseudomonas putida MnB1 as a Primary Response to H2O2 and Mn2+ Zheng, Yanjing; Li, Yumei; Long, Hongyan Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01490	journal	July 2018
The Phosphodiesterase DipA (PA5017) Is Essential for Pseudomonas aeruginosa Biofilm Dispersion Roy, A. B.; Petrova, O. E.; Sauer, K. Journal of Bacteriology, Vol. 194, Issue 11 https://doi.org/10.1128/jb.05346-11	journal	April 2012
The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases Caspi, Ron; Billington, Richard; Ferrer, Luciana Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1164	journal	November 2015
A Comprehensive, CRISPR-based Functional Analysis of Essential Genes in Bacteria Peters, Jason M.; Colavin, Alexandre; Shi, Handuo Cell, Vol. 165, Issue 6 https://doi.org/10.1016/j.cell.2016.05.003	journal	June 2016
Development of non-pathogenic bacterial biofilms on the surface of stainless steel which are inhibitory to Salmonella enterica Kim, Yoonbin; Kim, Hoikyung; Beuchat, Larry R. Food Microbiology, Vol. 69 https://doi.org/10.1016/j.fm.2017.08.003	journal	February 2018
The Pseudomonas fluorescens SBW25 wrinkly spreader biofilm requires attachment factor, cellulose fibre and LPS interactions to maintain strength and integrity Spiers, A. J. Microbiology, Vol. 151, Issue 9 https://doi.org/10.1099/mic.0.27984-0	journal	September 2005
Giving structure to the biofilm matrix: an overview of individual strategies and emerging common themes Hobley, Laura; Harkins, Catriona; MacPhee, Cait E. FEMS Microbiology Reviews, Vol. 39, Issue 5 https://doi.org/10.1093/femsre/fuv015	journal	April 2015
Specific Control of Pseudomonas aeruginosa Surface-Associated Behaviors by Two c-di-GMP Diguanylate Cyclases Merritt, Judith H.; Ha, Dae-Gon; Cowles, Kimberly N. mBio, Vol. 1, Issue 4 https://doi.org/10.1128/mBio.00183-10	journal	October 2010
RsmY, a small regulatory RNA, is required in concert with RsmZ for GacA-dependent expression of biocontrol traits in Pseudomonas fluorescens CHA0: Small regulatory RNAs of P. fluorescens Valverde, Claudio; Heeb, Stephan; Keel, Christoph Molecular Microbiology, Vol. 50, Issue 4 https://doi.org/10.1046/j.1365-2958.2003.03774.x	journal	October 2003
The role of biofilms as environmental reservoirs of antibiotic resistance Balcázar, José L.; Subirats, Jéssica; Borrego, Carles M. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01216	journal	October 2015
Dimeric c-di-GMP Is Required for Post-translational Regulation of Alginate Production in Pseudomonas aeruginosa Whitney, John C.; Whitfield, Gregory B.; Marmont, Lindsey S. Journal of Biological Chemistry, Vol. 290, Issue 20 https://doi.org/10.1074/jbc.m115.645051	journal	March 2015
Pleiotropic Effects of GacA on Pseudomonas fluorescens Pf0-1 In Vitro and in Soil Seaton, Sarah C.; Silby, Mark W.; Levy, Stuart B. Applied and Environmental Microbiology, Vol. 79, Issue 17 https://doi.org/10.1128/AEM.00819-13	journal	June 2013
A Symphony of Cyclases: Specificity in Diguanylate Cyclase Signaling Dahlstrom, Kurt M.; O'Toole, George A. Annual Review of Microbiology, Vol. 71, Issue 1 https://doi.org/10.1146/annurev-micro-090816-093325	journal	September 2017
Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose: Biofilm formation by P. fluorescens SBW25 Spiers, Andrew J.; Bohannon, John; Gehrig, Stefanie M. Molecular Microbiology, Vol. 50, Issue 1 https://doi.org/10.1046/j.1365-2958.2003.03670.x	journal	August 2003
Proteomic Analysis of a Global Regulator GacS Sensor Kinase in the Rhizobacterium, Pseudomonas chlororaphis O6 Kim, Chul Hong; Kim, Yong Hwan; Anderson, Anne J. The Plant Pathology Journal, Vol. 30, Issue 2 https://doi.org/10.5423/ppj.nt.02.2014.0012	journal	June 2014
Sensor complexes regulating two-component signal transduction Szurmant, Hendrik; White, Robert A.; Hoch, James A. Current Opinion in Structural Biology, Vol. 17, Issue 6 https://doi.org/10.1016/j.sbi.2007.08.019	journal	December 2007
Genome-wide CRISPR-dCas9 screens in E. coli identify essential genes and phage host factors Rousset, François; Cui, Lun; Siouve, Elise PLOS Genetics, Vol. 14, Issue 11 https://doi.org/10.1371/journal.pgen.1007749	journal	November 2018
Adaptive Divergence in Experimental Populations of Pseudomonas fluorescens . IV. Genetic Constraints Guide Evolutionary Trajectories in a Parallel Adaptive Radiation McDonald, Michael J.; Gehrig, Stefanie M.; Meintjes, Peter L. Genetics, Vol. 183, Issue 3 https://doi.org/10.1534/genetics.109.107110	journal	August 2009
The Gac regulon of Pseudomonas fluorescens SBW25 : The Gac regulon of SBW25 Cheng, Xu; de Bruijn, Irene; van der Voort, Menno Environmental Microbiology Reports, Vol. 5, Issue 4 https://doi.org/10.1111/1758-2229.12061	journal	April 2013
Investigating essential gene function in Mycobacterium tuberculosis using an efficient CRISPR interference system Singh, Atul K.; Carette, Xavier; Potluri, Lakshmi-Prasad Nucleic Acids Research, Vol. 44, Issue 18 https://doi.org/10.1093/nar/gkw625	journal	July 2016
Biofilms: an emergent form of bacterial life Flemming, Hans-Curt; Wingender, Jost; Szewzyk, Ulrich Nature Reviews Microbiology, Vol. 14, Issue 9 https://doi.org/10.1038/nrmicro.2016.94	journal	August 2016
The mycorrhiza helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N Deveau, A.; Palin, B.; Delaruelle, C. New Phytologist, Vol. 175, Issue 4 https://doi.org/10.1111/j.1469-8137.2007.02148.x	journal	September 2007
Genetic and phenotypic analysis of the GacS/GacA system in the moderate halophile Halomonas anticariensis Tahrioui, A.; Quesada, E.; Llamas, I. Microbiology, Vol. 159, Issue Pt_3 https://doi.org/10.1099/mic.0.061721-0	journal	January 2013
The keepers of the ring: regulators of FtsZ assembly Ortiz, Cristina; Natale, Paolo; Cueto, Laura FEMS Microbiology Reviews, Vol. 40, Issue 1 https://doi.org/10.1093/femsre/fuv040	journal	September 2015
Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens Silby, Mark W.; Cerdeño-Tárraga, Ana M.; Vernikos, Georgios S. Genome Biology, Vol. 10, Issue 5 https://doi.org/10.1186/gb-2009-10-5-r51	journal	January 2009
Influence of heterologous MreB proteins on cell morphology of Bacillus subtilis Schirner, K.; Errington, J. Microbiology, Vol. 155, Issue 11 https://doi.org/10.1099/mic.0.030692-0	journal	July 2009
Differential Regulation of Genes for Cyclic-di-GMP Metabolism Orchestrates Adaptive Changes During Rhizosphere Colonization by Pseudomonas fluorescens Little, Richard H.; Woodcock, Stuart D.; Campilongo, Rosaria Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01089	journal	May 2019
The biofilm matrix Flemming, Hans-Curt; Wingender, Jost Nature Reviews Microbiology, Vol. 8, Issue 9 https://doi.org/10.1038/nrmicro2415	journal	August 2010
CRISPR interference (CRISPRi) for gene regulation and succinate production in cyanobacterium S. elongatus PCC 7942 Huang, Chun-Hung; Shen, Claire R.; Li, Hung Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-016-0595-3	journal	November 2016
The Sensor Kinase GacS Negatively Regulates Flagellar Formation and Motility in a Biocontrol Bacterium, Pseudomonas chlororaphis O6 Kim, Ji Soo; Kim, Yong Hwan; Anderson, Anne J. The Plant Pathology Journal, Vol. 30, Issue 2 https://doi.org/10.5423/ppj.nt.11.2013.0109	journal	June 2014
Specificity of plant-microbe interactions in the tree mycorrhizosphere biome and consequences for soil C cycling Churchland, Carolyn; Grayston, Sue J. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00261	journal	June 2014
Evolution of Ecological Diversity in Biofilms of Pseudomonas aeruginosa by Altered Cyclic Diguanylate Signaling Flynn, Kenneth M.; Dowell, Gabrielle; Johnson, Thomas M. Journal of Bacteriology, Vol. 198, Issue 19 https://doi.org/10.1128/jb.00048-16	journal	March 2016
A bright monomeric green fluorescent protein derived from Branchiostoma lanceolatum Shaner, Nathan C.; Lambert, Gerard G.; Chammas, Andrew Nature Methods, Vol. 10, Issue 5 https://doi.org/10.1038/nmeth.2413	journal	March 2013
Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression Qi, Lei S.; Larson, Matthew H.; Gilbert, Luke A. Cell, Vol. 184, Issue 3 https://doi.org/10.1016/j.cell.2021.01.019	journal	February 2021
Efficient rhizosphere colonization by Pseudomonas fluorescens f113 mutants unable to form biofilms on abiotic surfaces: Biofilm formation and rhizosphere colonization Barahona, Emma; Navazo, Ana; Yousef-Coronado, Fátima Environmental Microbiology, Vol. 12, Issue 12 https://doi.org/10.1111/j.1462-2920.2010.02291.x	journal	December 2010
BifA, a Cyclic-Di-GMP Phosphodiesterase, Inversely Regulates Biofilm Formation and Swarming Motility by Pseudomonas aeruginosa PA14 Kuchma, S. L.; Brothers, K. M.; Merritt, J. H. Journal of Bacteriology, Vol. 189, Issue 22 https://doi.org/10.1128/jb.00586-07	journal	June 2007
Two-Component Signal Transduction Stock, Ann M.; Robinson, Victoria L.; Goudreau, Paul N. Annual Review of Biochemistry, Vol. 69, Issue 1 https://doi.org/10.1146/annurev.biochem.69.1.183	journal	June 2000
Adaptive Divergence in Experimental Populations of Pseudomonas fluorescens . V. Insight into the Niche Specialist Fuzzy Spreader Compels Revision of the Model Pseudomonas Radiation Ferguson, Gayle C.; Bertels, Frederic; Rainey, Paul B. Genetics, Vol. 195, Issue 4 https://doi.org/10.1534/genetics.113.154948	journal	September 2013
Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal McDougald, Diane; Rice, Scott A.; Barraud, Nicolas Nature Reviews Microbiology, Vol. 10, Issue 1 https://doi.org/10.1038/nrmicro2695	journal	November 2011
Dispersion by Pseudomonas aeruginosa requires an unusual posttranslational modification of BdlA Petrova, O. E.; Sauer, K. Proceedings of the National Academy of Sciences, Vol. 109, Issue 41 https://doi.org/10.1073/pnas.1207832109	journal	September 2012
Colonization pattern of primary tomato roots by Pseudomonas fluorescens A6RI characterized by dilution plating, flow cytometry, fluorescence, confocal and scanning electron microscopy Gamalero, Elisa; Lingua, Guido; Giusy CaprÃ¬, Flavia FEMS Microbiology Ecology, Vol. 48, Issue 1 https://doi.org/10.1016/j.femsec.2003.12.012	journal	April 2004
The actin-like MreB proteins in Bacillus subtilis a new turn Carballido-Lopez, Rut Frontiers in Bioscience, Vol. S4, Issue 4 https://doi.org/10.2741/s354	journal	January 2012
Enrichment of Root Endophytic Bacteria from Populus deltoides and Single-Cell-Genomics Analysis Utturkar, Sagar M.; Cude, W. Nathan; Robeson, Michael S. Applied and Environmental Microbiology, Vol. 82, Issue 18 https://doi.org/10.1128/AEM.01285-16	journal	July 2016
Quick change: post-transcriptional regulation in Pseudomonas Grenga, Lucia; Little, Richard H.; Malone, Jacob G. FEMS Microbiology Letters, Vol. 364, Issue 14 https://doi.org/10.1093/femsle/fnx125	journal	June 2017
Multi‐input CRISPR / C as genetic circuits that interface host regulatory networks Nielsen, Alec AK; Voigt, Christopher A. Molecular Systems Biology, Vol. 10, Issue 11 https://doi.org/10.15252/msb.20145735	journal	November 2014
Repurposing CRISPR as an RNA-Guided Platform for Sequence-Specific Control of Gene Expression Qi, Lei S.; Larson, Matthew H.; Gilbert, Luke A. Cell, Vol. 152, Issue 5, p. 1173-1183 https://doi.org/10.1016/j.cell.2013.02.022	journal	February 2013
Adaptive Remodeling of the Bacterial Proteome by Specific Ribosomal Modification Regulates Pseudomonas Infection and Niche Colonisation Little, Richard H.; Grenga, Lucia; Saalbach, Gerhard PLOS Genetics, Vol. 12, Issue 2 https://doi.org/10.1371/journal.pgen.1005837	journal	February 2016
Signal integration in bacterial two-component regulatory systems Mitrophanov, A. Y.; Groisman, E. A. Genes & Development, Vol. 22, Issue 19 https://doi.org/10.1101/gad.1700308	journal	October 2008
Pseudomonas fluorescens Transportome Is Linked to Strain-Specific Plant Growth Promotion in Aspen Seedlings under Nutrient Stress Shinde, Shalaka; Cumming, Jonathan R.; Collart, Frank R. Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00348	journal	March 2017
Experimental evolution reveals hidden diversity in evolutionary pathways Lind, Peter A.; Farr, Andrew D.; Rainey, Paul B. eLife, Vol. 4 https://doi.org/10.7554/eLife.07074	journal	March 2015
Modeling the Pseudomonas Sulfur Regulome by Quantifying the Storage and Communication of Information Larsen, Peter E.; Zerbs, Sarah; Laible, Philip D. mSystems, Vol. 3, Issue 3 https://doi.org/10.1128/mSystems.00189-17	journal	June 2018
Regulatory Roles of the GacS/GacA Two-Component System in Plant-Associated and Other Gram-Negative Bacteria Heeb, Stephan; Haas, Dieter Molecular Plant-Microbe Interactions, Vol. 14, Issue 12 https://doi.org/10.1094/mpmi.2001.14.12.1351	journal	December 2001
Functional analyses of the RsmY and RsmZ small noncoding regulatory RNAs in Pseudomonas aeruginosa K. H., Janssen,; W., Sanders,; M. C., Wolfgang, American Society for Microbiology https://doi.org/10.17615/p0e9-ky39	text	January 2018
Alg44, a unique protein required for alginate biosynthesis in Pseudomonas aeruginosa Remminghorst, Uwe; Rehm, Bernd H. A. FEBS Letters, Vol. 580, Issue 16 https://doi.org/10.1016/j.febslet.2006.05.077	journal	June 2006
The Pseudomonas aeruginosa Diguanylate Cyclase GcbA, a Homolog of P. fluorescens GcbA, Promotes Initial Attachment to Surfaces, but Not Biofilm Formation, via Regulation of Motility Petrova, O. E.; Cherny, K. E.; Sauer, K. Journal of Bacteriology, Vol. 196, Issue 15 https://doi.org/10.1128/JB.01628-14	journal	June 2014
Microtiter Dish Biofilm Formation Assay O'Toole, George A. Journal of Visualized Experiments, Issue 47 https://doi.org/10.3791/2437	journal	January 2011
Dynamics of Aspen Roots Colonization by Pseudomonads Reveals Strain-Specific and Mycorrhizal-Specific Patterns of Biofilm Formation Noirot-Gros, Marie-Francoise; Shinde, Shalaka; Larsen, Peter E. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00853	journal	May 2018
Biofilms and Cyclic di-GMP (c-di-GMP) Signaling: Lessons from Pseudomonas aeruginosa and Other Bacteria Valentini, Martina; Filloux, Alain Journal of Biological Chemistry, Vol. 291, Issue 24 https://doi.org/10.1074/jbc.R115.711507	journal	April 2016
Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria Hall, Clayton W.; Mah, Thien-Fah FEMS Microbiology Reviews, Vol. 41, Issue 3 https://doi.org/10.1093/femsre/fux010	journal	March 2017
An improved, high-quality draft genome sequence of the Germination-Arrest Factor-producing Pseudomonas fluorescens WH6 Kimbrel, Jeffrey A.; Givan, Scott A.; Halgren, Anne B. BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-522	journal	January 2010
CRISPR interference (CRISPRi) for sequence-specific control of gene expression Larson, Matthew H.; Gilbert, Luke A.; Wang, Xiaowo Nature Protocols, Vol. 8, Issue 11 https://doi.org/10.1038/nprot.2013.132	journal	October 2013
Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa Gooderham, W. James; Hancock, Robert E. W. FEMS Microbiology Reviews, Vol. 33, Issue 2 https://doi.org/10.1111/j.1574-6976.2008.00135.x	journal	March 2009
Systematic Analysis of Diguanylate Cyclases That Promote Biofilm Formation by Pseudomonas fluorescens Pf0-1 Newell, P. D.; Yoshioka, S.; Hvorecny, K. L. Journal of Bacteriology, Vol. 193, Issue 18 https://doi.org/10.1128/jb.05483-11	journal	July 2011
A Multimodal Strategy Used by a Large c-di-GMP Network Dahlstrom, Kurt M.; Collins, Alan J.; Doing, Georgia Journal of Bacteriology, Vol. 200, Issue 8 https://doi.org/10.1128/JB.00703-17	journal	January 2018
A Robust CRISPR Interference Gene Repression System in Pseudomonas Tan, Sue Zanne; Reisch, Christopher R.; Prather, Kristala L. J. Journal of Bacteriology, Vol. 200, Issue 7 https://doi.org/10.1128/JB.00575-17	journal	January 2018
The Diguanylate Cyclase GcbA Facilitates Pseudomonas aeruginosa Biofilm Dispersion by Activating BdlA Petrova, Olga E.; Cherny, Kathryn E.; Sauer, Karin Journal of Bacteriology, Vol. 197, Issue 1 https://doi.org/10.1128/jb.02244-14	journal	October 2014
Transient alginate gene expression by Pseudomonas putida biofilm residents under water-limiting conditions reflects adaptation to the local environment Li, Xiaohong; Nielsen, Lindsey; Nolan, Connor Environmental Microbiology https://doi.org/10.1111/j.1462-2920.2010.02186.x	journal	April 2010
Inactivation of the GacA response regulator in Pseudomonas fluorescens Pf-5 has far-reaching transcriptomic consequences: P. fluorescens GacA transcriptomic fingerprint Hassan, Karl A.; Johnson, Aaron; Shaffer, Brenda T. Environmental Microbiology, Vol. 12, Issue 4 https://doi.org/10.1111/j.1462-2920.2009.02134.x	journal	January 2010
A Programmable Dual-RNA-Guided DNA Endonuclease in Adaptive Bacterial Immunity Jinek, M.; Chylinski, K.; Fonfara, I. Science, Vol. 337, Issue 6096, p. 816-821 https://doi.org/10.1126/science.1225829	journal	June 2012
Functional Analyses of the RsmY and RsmZ Small Noncoding Regulatory RNAs in Pseudomonas aeruginosa Janssen, Kayley H.; Diaz, Manisha R.; Golden, Matthew Journal of Bacteriology, Vol. 200, Issue 11 https://doi.org/10.1128/JB.00736-17	journal	February 2018
The Sigma Factor AlgU (AlgT) Controls Exopolysaccharide Production and Tolerance towards Desiccation and Osmotic Stress in the Biocontrol Agent Pseudomonas fluorescens CHA0 Schnider-Keel, U.; Lejbolle, K. B.; Baehler, E. Applied and Environmental Microbiology, Vol. 67, Issue 12 https://doi.org/10.1128/aem.67.12.5683-5693.2001	journal	December 2001
The c-di-GMP phosphodiesterase BifA regulates biofilm development in P seudomonas putida : c-di-GMP and BifA regulation of biofilm development Jiménez-Fernández, Alicia; López-Sánchez, Aroa; Calero, Patricia Environmental Microbiology Reports, Vol. 7, Issue 1 https://doi.org/10.1111/1758-2229.12153	journal	March 2014
Control of Rhizoctonia solani on Cotton Seedlings with Pseudomonas fluorescens and With an Antibiotic Produced by the Bacterium Howell, C. R. Phytopathology, Vol. 69, Issue 5 https://doi.org/10.1094/Phyto-69-480	journal	January 1979
A Mechanistic Explanation Linking Adaptive Mutation, Niche Change, and Fitness Advantage for the Wrinkly Spreader Spiers, Andrew J. International Journal of Evolutionary Biology, Vol. 2014 https://doi.org/10.1155/2014/675432	journal	January 2014
Diversity of Cyclic Di-GMP-Binding Proteins and Mechanisms Chou, Shan-Ho; Galperin, Michael Y. Journal of Bacteriology, Vol. 198, Issue 1 https://doi.org/10.1128/jb.00333-15	journal	June 2015
Identification of Genes in the σ22 Regulon of Pseudomonas aeruginosa Required for Cell Envelope Homeostasis in Either the Planktonic or the Sessile Mode of Growth Wood, Lynn F.; Ohman, Dennis E. mBio, Vol. 3, Issue 3 https://doi.org/10.1128/mBio.00094-12	journal	May 2012
Principles of c-di-GMP signalling in bacteria Hengge, Regine Nature Reviews Microbiology, Vol. 7, Issue 4 https://doi.org/10.1038/nrmicro2109	journal	April 2009
Small, Stable Shuttle Vectors Based on the Minimal pVS1 Replicon for Use in Gram-Negative, Plant-Associated Bacteria Heeb, Stephan; Itoh, Yoshifumi; Nishijyo, Takayuki Molecular Plant-Microbe Interactions, Vol. 13, Issue 2 https://doi.org/10.1094/mpmi.2000.13.2.232	journal	February 2000
Cyclic di-GMP: the First 25 Years of a Universal Bacterial Second Messenger Romling, U.; Galperin, M. Y.; Gomelsky, M. Microbiology and Molecular Biology Reviews, Vol. 77, Issue 1 https://doi.org/10.1128/mmbr.00043-12	journal	March 2013
Iron-Regulated Expression of Alginate Production, Mucoid Phenotype, and Biofilm Formation by Pseudomonas aeruginosa Wiens, Jacinta R.; Vasil, Adriana I.; Schurr, Michael J. mBio, Vol. 5, Issue 1 https://doi.org/10.1128/mbio.01010-13	journal	February 2014
The Gac-Rsm and SadB Signal Transduction Pathways Converge on AlgU to Downregulate Motility in Pseudomonas fluorescens Martínez-Granero, Francisco; Navazo, Ana; Barahona, Emma PLoS ONE, Vol. 7, Issue 2 https://doi.org/10.1371/journal.pone.0031765	journal	February 2012
Trigger phosphodiesterases as a novel class of c-di-GMP effector proteins Hengge, Regine Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 371, Issue 1707 https://doi.org/10.1098/rstb.2015.0498	journal	November 2016
Systematic Nomenclature for GGDEF and EAL Domain-Containing Cyclic Di-GMP Turnover Proteins of Escherichia coli: TABLE 1 Hengge, Regine; Galperin, Michael Y.; Ghigo, Jean-Marc Journal of Bacteriology, Vol. 198, Issue 1 https://doi.org/10.1128/jb.00424-15	journal	July 2015

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