Literature DB >> 27637885

Pseudomonas brassicacearum strain DF41 kills Caenorhabditis elegans through biofilm-dependent and biofilm-independent mechanisms.

Munmun Nandi1, Chrystal Berry2, Ann Karen C Brassinga1, Mark F Belmonte3, W G Dilantha Fernando4, Peter C Loewen1, Teresa R de Kievit5.   

Abstract

Pseudomonas brassicacearum DF41 is a biocontrol agent that suppresses disease caused by the fungal pathogen Sclerotinia sclerotiorum A number of exometabolites are produced by DF41 including the lipopeptide sclerosin, hydrogen cyanide (HCN) and degradative enzymes. Production of these compounds is controlled at both the transcriptional and posttranscriptional level by quorum sensing (QS) and the Gac-two component regulatory system. In order to be successful, a biocontrol agent must persist in the environment at levels sufficient for pathogen control. Bacterivorous predators, including nematodes, represent a challenge to the establishment of introduced microorganisms. In the current study, DF41 was investigated for its ability to resist predation by Caenorhabditis elegans. We discovered that this bacterium is capable of killing C. elegans through two different mechanisms: the first involves exposure to toxic metabolites; and the second entails biofilm formation on the nematode head blocking the buccal cavity. Biofilm formation on nematodes, which has only been reported for Yersinia spp. and Xenorhabdus nematophila, is dependent upon the Gac system. Biofilms were not observed when bacteria were grown on NaCl-containing media, and on C. elegans biofilm-resistant mutants. Co-culturing with nematodes lead to increased expression of the pdfRI-rfiA QS genes and hcnA which is under QS control. HCN was the most nematicidal of the exometabolites, suggesting that this bacterium can respond to predator cues and upregulate expression of toxins accordingly. In summary, DF41 is able to respond to the presence of C. elegans and through two distinct mechanisms it can escape predation. IMPORTANCE: Pseudomonas brassicacearum DF41 can suppress fungal pathogens through a process known as biocontrol. To be successful, a biocontrol agent must be able to persist in the environment at levels sufficient for pathogen control. Predators including the nematode Caenorhabditis elegans represent a threat to persistence. The aim of the current study was to investigate the DF41-C. elegans interaction. We discovered that DF41 is able to escape predation through two distinct mechanisms. The first involves exposure to toxic bacterial metabolites and the second entails formation of a sticky coating on the nematode head, called a biofilm, which blocks feeding and causes starvation. This is the first report of a pseudomonad forming biofilms on the C. elegans surface. When grown with C. elegans, DF41 exhibits altered gene expression and metabolite production indicating that this bacterium can sense the presence of these predators and adjust its physiology accordingly.
Copyright © 2016, American Society for Microbiology. All Rights Reserved.

Entities:  

Year:  2016        PMID: 27637885      PMCID: PMC5103088          DOI: 10.1128/AEM.02199-16

Source DB:  PubMed          Journal:  Appl Environ Microbiol        ISSN: 0099-2240            Impact factor:   4.792


  46 in total

1.  Diverse bacteria are pathogens of Caenorhabditis elegans.

Authors:  Carole Couillault; Jonathan J Ewbank
Journal:  Infect Immun       Date:  2002-08       Impact factor: 3.441

Review 2.  The ecological significance of biofilm formation by plant-associated bacteria.

Authors:  Cindy E Morris; Jean-Michel Monier
Journal:  Annu Rev Phytopathol       Date:  2003-04-29       Impact factor: 13.078

Review 3.  Regulation of antibiotic production in root-colonizing Peudomonas spp. and relevance for biological control of plant disease.

Authors:  Dieter Haas; Christoph Keel
Journal:  Annu Rev Phytopathol       Date:  2003-04-29       Impact factor: 13.078

4.  Predator-prey chemical warfare determines the expression of biocontrol genes by rhizosphere-associated Pseudomonas fluorescens.

Authors:  Alexandre Jousset; Laurène Rochat; Stefan Scheu; Michael Bonkowski; Christoph Keel
Journal:  Appl Environ Microbiol       Date:  2010-06-04       Impact factor: 4.792

5.  Repression of the antifungal activity of Pseudomonas sp. strain DF41 by the stringent response.

Authors:  Jerrylynn Manuel; Chrystal Berry; Carrie Selin; W G Dilantha Fernando; Teresa R de Kievit
Journal:  Appl Environ Microbiol       Date:  2011-06-24       Impact factor: 4.792

6.  Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli.

Authors:  Debra W Jackson; Kazushi Suzuki; Lawrence Oakford; Jerry W Simecka; Mark E Hart; Tony Romeo
Journal:  J Bacteriol       Date:  2002-01       Impact factor: 3.490

7.  Diversity and functional analysis of LuxR-type transcriptional regulators of cyclic lipopeptide biosynthesis in Pseudomonas fluorescens.

Authors:  I de Bruijn; J M Raaijmakers
Journal:  Appl Environ Microbiol       Date:  2009-05-15       Impact factor: 4.792

8.  Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa.

Authors:  S E West; H P Schweizer; C Dall; A K Sample; L J Runyen-Janecky
Journal:  Gene       Date:  1994-10-11       Impact factor: 3.688

9.  Chemical and biological characterization of sclerosin, an antifungal lipopeptide.

Authors:  Chrystal L Berry; Ann Karen C Brassinga; Lynda J Donald; W G Dilantha Fernando; Peter C Loewen; Teresa R de Kievit
Journal:  Can J Microbiol       Date:  2012-08       Impact factor: 2.419

Review 10.  Characterization of mediators of microbial virulence and innate immunity using the Caenorhabditis elegans host-pathogen model.

Authors:  Rosanna A Alegado; Marianne C Campbell; Will C Chen; Sandra S Slutz; Man-Wah Tan
Journal:  Cell Microbiol       Date:  2003-07       Impact factor: 3.715

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Journal:  Genetics       Date:  2019-05-03       Impact factor: 4.562

3.  An Enterotoxin-Like Binary Protein from Pseudomonas protegens with Potent Nematicidal Activity.

Authors:  Jun-Zhi Wei; Daniel L Siehl; Zhenglin Hou; Barbara Rosen; Jarred Oral; Christopher G Taylor; Gusui Wu
Journal:  Appl Environ Microbiol       Date:  2017-09-15       Impact factor: 4.792

4.  Horizontally Acquired Cellulases Assist the Expansion of Dietary Range in Pristionchus Nematodes.

Authors:  Ziduan Han; Bogdan Sieriebriennikov; Vladislav Susoy; Wen-Sui Lo; Catia Igreja; Chuanfu Dong; Aileen Berasategui; Hanh Witte; Ralf J Sommer
Journal:  Mol Biol Evol       Date:  2022-02-03       Impact factor: 16.240

5.  Biofilm-associated toxin and extracellular protease cooperatively suppress competitors in Bacillus subtilis biofilms.

Authors:  Kazuo Kobayashi; Yukako Ikemoto
Journal:  PLoS Genet       Date:  2019-10-17       Impact factor: 5.917

  5 in total

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