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Title: The Phenazine 2-Hydroxy-Phenazine-1-Carboxylic Acid Promotes Extracellular DNA Release and Has Broad Transcriptomic Consequences in Pseudomonas chlororaphis 30–84

Journal Article · · PLoS ONE
 [1];  [2];  [2];  [2];  [2]
  1. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  2. Texas A & M Univ., College Station, TX (United States)

Enhanced production of 2-hydroxy-phenazine-1-carboxylic acid (2-OH-PCA) by the biological control strain Pseudomonas chlororaphis 30–84 derivative 30-84O* was shown previously to promote cell adhesion and alter the three-dimensional structure of surfaceattached biofilms compared to the wild type. The current study demonstrates that production of 2-OH-PCA promotes the release of extracellular DNA, which is correlated with the production of structured biofilm matrix. Moreover, the essential role of the extracellular DNA in maintaining the mass and structure of the 30–84 biofilm matrix is demonstrated. To better understand the role of different phenazines in biofilm matrix production and gene expression, transcriptomic analyses were conducted comparing gene expression patterns of populations of wild type, 30-84O* and a derivative of 30–84 producing only PCA (30-84PCA) to a phenazine defective mutant (30-84ZN) when grown in static cultures. RNA-Seq analyses identified a group of 802 genes that were differentially expressed by the phenazine producing derivatives compared to 30-84ZN, including 240 genes shared by the two 2-OH-PCA producing derivatives, the wild type and 30-84O*. A gene cluster encoding a bacteriophage- derived pyocin and its lysis cassette was upregulated in 2-OH-PCA producing derivatives. A holin encoded in this gene cluster was found to contribute to the release of eDNA in 30–84 biofilm matrices, demonstrating that the influence of 2-OH-PCA on eDNA production is due in part to cell autolysis as a result of pyocin production and release. The results expand the current understanding of the functions different phenazines play in the survival of bacteria in biofilm-forming communities.

Research Organization:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Organization:
USDOE
Grant/Contract Number:
AC52-06NA25396
OSTI ID:
1239267
Report Number(s):
LA-UR-14-28021
Journal Information:
PLoS ONE, Vol. 11, Issue 1; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 21 works
Citation information provided by
Web of Science

References (47)

Pyocyanin Facilitates Extracellular DNA Binding to Pseudomonas aeruginosa Influencing Cell Surface Properties and Aggregation journal March 2013
OxyR regulated the expression of two major catalases, KatA and KatB, along with peroxiredoxin, AhpC in Pseudomonas putida journal December 2006
The Pseudomonas aeruginosa Transcriptome in Planktonic Cultures and Static Biofilms Using RNA Sequencing journal February 2012
Phenazine Compounds in Fluorescent Pseudomonas Spp. Biosynthesis and Regulation journal September 2006
The Orphan Gene ybjN Conveys Pleiotropic Effects on Multicellular Behavior and Survival of Escherichia coli journal September 2011
Adaptation Genomics of a Small-Colony Variant in a Pseudomonas chlororaphis 30-84 Biofilm journal November 2014
Assembly and Development of the Pseudomonas aeruginosa Biofilm Matrix journal March 2009
Molecular Control of Bacterial Death and Lysis journal March 2008
Roles of the Gac-Rsm pathway in the regulation of phenazine biosynthesis in Pseudomonas chlororaphis 30-84 journal April 2013
Phenotypes of Non-Attached Pseudomonas aeruginosa Aggregates Resemble Surface Attached Biofilm journal November 2011
Transcriptome profiling reveals links between ParS/ParR, MexEF-OprN, and quorum sensing in the regulation of adaptation and virulence in Pseudomonas aeruginosa journal September 2013
The R-type pyocin of Pseudomonas aeruginosa is related to P2 phage, and the F-type is related to lambda phage journal October 2000
Differential regulation of phenazine biosynthesis by RpeA and RpeB in Pseudomonas chlororaphis 30-84 journal July 2012
Pyocyanin Promotes Extracellular DNA Release in Pseudomonas aeruginosa journal October 2012
Antifungal mechanisms by which a novel Pseudomonas aeruginosa phenazine toxin kills Candida albicans in biofilms: Antifungal effects of a P. aeruginosa phenazine toxin journal October 2010
NIH Image to ImageJ: 25 years of image analysis journal June 2012
Phenazine virulence factor binding to extracellular DNA is important for Pseudomonas aeruginosa biofilm formation journal February 2015
OxyR is involved in the expression of thioredoxin reductase TrxB in Pseudomonas putida journal December 2008
The biofilm matrix journal August 2010
Biological control of soil-borne pathogens by fluorescent pseudomonads journal March 2005
The phzI gene of Pseudomonas aureofaciens 30–84 is responsible for the production of a diffusible signal required for phenazine antibiotic production journal January 1996
Quorum Sensing and Phenazines are Involved in Biofilm Formation by Pseudomonas chlororaphis (aureofaciens) Strain 30-84 journal August 2006
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data journal November 2009
Cell Death in Pseudomonas aeruginosa Biofilm Development journal July 2003
Phenazine antibiotic biosynthesis in Pseudomonas aureofaciens 30-84 is regulated by PhzR in response to cell density. journal July 1994
Characterization of MexE–MexF–OprN, a positively regulated multidrug efflux system of Pseudomonas aeruginosa journal January 1997
Comparative Genomics of Plant-Associated Pseudomonas spp.: Insights into Diversity and Inheritance of Traits Involved in Multitrophic Interactions journal July 2012
AmyR Is a Novel Negative Regulator of Amylovoran Production in Erwinia amylovora journal September 2012
Holins: The Protein Clocks of Bacteriophage Infections journal October 2000
A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms journal February 2006
Detection of multiple extracytoplasmic function (ECF) sigma factors in the genome of Pseudomonas putida KT2440 and their counterparts in Pseudomonas aeruginosa PA01 journal December 2002
The small RNA PhrS stimulates synthesis of the Pseudomonas aeruginosa quinolone signal: The small RNA PhrS activates translation of pqsR journal March 2011
A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants journal May 1998
Targeting redox metabolism: the perfect storm induced by acrylamide poisoning in the brain journal January 2020
Genome-Wide Identification of Genes Regulated by the Rcs Phosphorelay System in Erwinia amylovora journal January 2012
Cloning and Heterologous Expression of the Phenazine Biosynthetic Locus from Pseudomonas aureofaciens 30-84 journal January 1992
Improved gfp and inaZ Broad-Host-Range Promoter-Probe Vectors journal November 2000
Molecular analysis of genes encoding phenazine biosynthesis in the biological control bacteriumPseudomonas aureofaciens30–84 journal December 1995
Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. journal January 1992
A Second Quorum-Sensing System Regulates Cell Surface Properties but Not Phenazine Antibiotic Production in Pseudomonas aureofaciens journal September 2001
Sticky Situations: Key Components That Control Bacterial Surface Attachment journal March 2012
Altering the Ratio of Phenazines in Pseudomonas chlororaphis (aureofaciens) Strain 30-84: Effects on Biofilm Formation and Pathogen Inhibition journal February 2008
Influence of the MexAB-OprM Multidrug Efflux System on Quorum Sensing in Pseudomonas aeruginosa journal October 1998
The Staphylococcus aureus lrgAB Operon Modulates Murein Hydrolase Activity and Penicillin Tolerance journal January 2000
phzO, a Gene for Biosynthesis of 2-Hydroxylated Phenazine Compounds in Pseudomonas aureofaciens 30-84 journal January 2001
Functional Analysis of Genes for Biosynthesis of Pyocyanin and Phenazine-1-Carboxamide from Pseudomonas aeruginosa PAO1 journal November 2001
Biofilm Formation by Hyperpiliated Mutants of Pseudomonas aeruginosa journal April 2003

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