Transcriptional and antagonistic responses of Pseudomonas fluorescens Pf0-1 to phylogenetically different bacterial competitors

The ability of soil bacteria to successfully compete with a range of other microbial species is crucial for their growth and survival in the nutrient-limited soil environment. In the present work, we studied the behavior and transcriptional responses of soil-inhabiting Pseudomonas fluorescens strain...

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Published inThe ISME Journal Vol. 5; no. 6; pp. 973 - 985
Main Authors Garbeva, Paolina, Silby, Mark W, Raaijmakers, Jos M, Levy, Stuart B, Boer, Wietse de
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.06.2011
Oxford University Press
Nature Publishing Group
Subjects
Online AccessGet full text
ISSN1751-7362
1751-7370
1751-7370
DOI10.1038/ismej.2010.196

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Abstract The ability of soil bacteria to successfully compete with a range of other microbial species is crucial for their growth and survival in the nutrient-limited soil environment. In the present work, we studied the behavior and transcriptional responses of soil-inhabiting Pseudomonas fluorescens strain Pf0-1 on nutrient-poor agar to confrontation with strains of three phylogenetically different bacterial genera, that is, Bacillus , Brevundimonas and Pedobacter . Competition for nutrients was apparent as all three bacterial genera had a negative effect on the density of P. fluorescens Pf0-1; this effect was most strong during the interaction with Bacillus . Microarray-based analyses indicated strong differences in the transcriptional responses of Pf0-1 to the different competitors. There was higher similarity in the gene expression response of P. fluorescens Pf0-1 to the Gram-negative bacteria as compared with the Gram-positive strain. The Gram-negative strains did also trigger the production of an unknown broad-spectrum antibiotic in Pf0-1. More detailed analysis indicated that expression of specific Pf0-1 genes involved in signal transduction and secondary metabolite production was strongly affected by the competitors’ identity, suggesting that Pf0-1 can distinguish among different competitors and fine-tune its competitive strategies. The results presented here demonstrate that P. fluorescens Pf0-1 shows a species-specific transcriptional and metabolic response to bacterial competitors and provide new leads in the identification of specific cues in bacteria–bacteria interactions and of novel competitive strategies, antimicrobial traits and genes.
AbstractList The ability of soil bacteria to successfully compete with a range of other microbial species is crucial for their growth and survival in the nutrient-limited soil environment. In the present work, we studied the behavior and transcriptional responses of soil-inhabiting Pseudomonas fluorescens strain Pf0-1 on nutrient-poor agar to confrontation with strains of three phylogenetically different bacterial genera, that is, Bacillus, Brevundimonas and Pedobacter. Competition for nutrients was apparent as all three bacterial genera had a negative effect on the density of P. fluorescens Pf0-1; this effect was most strong during the interaction with Bacillus. Microarray-based analyses indicated strong differences in the transcriptional responses of Pf0-1 to the different competitors. There was higher similarity in the gene expression response of P. fluorescens Pf0-1 to the Gram-negative bacteria as compared with the Gram-positive strain. The Gram-negative strains did also trigger the production of an unknown broad-spectrum antibiotic in Pf0-1. More detailed analysis indicated that expression of specific Pf0-1 genes involved in signal transduction and secondary metabolite production was strongly affected by the competitors' identity, suggesting that Pf0-1 can distinguish among different competitors and fine-tune its competitive strategies. The results presented here demonstrate that P. fluorescens Pf0-1 shows a species-specific transcriptional and metabolic response to bacterial competitors and provide new leads in the identification of specific cues in bacteria-bacteria interactions and of novel competitive strategies, antimicrobial traits and genes.
The ability of soil bacteria to successfully compete with a range of other microbial species is crucial for their growth and survival in the nutrient-limited soil environment. In the present work, we studied the behavior and transcriptional responses of soil-inhabiting Pseudomonas fluorescens strain Pf0-1 on nutrient-poor agar to confrontation with strains of three phylogenetically different bacterial genera, that is, Bacillus , Brevundimonas and Pedobacter . Competition for nutrients was apparent as all three bacterial genera had a negative effect on the density of P. fluorescens Pf0-1; this effect was most strong during the interaction with Bacillus . Microarray-based analyses indicated strong differences in the transcriptional responses of Pf0-1 to the different competitors. There was higher similarity in the gene expression response of P. fluorescens Pf0-1 to the Gram-negative bacteria as compared with the Gram-positive strain. The Gram-negative strains did also trigger the production of an unknown broad-spectrum antibiotic in Pf0-1. More detailed analysis indicated that expression of specific Pf0-1 genes involved in signal transduction and secondary metabolite production was strongly affected by the competitors' identity, suggesting that Pf0-1 can distinguish among different competitors and fine-tune its competitive strategies. The results presented here demonstrate that P. fluorescens Pf0-1 shows a species-specific transcriptional and metabolic response to bacterial competitors and provide new leads in the identification of specific cues in bacteria–bacteria interactions and of novel competitive strategies, antimicrobial traits and genes.
The ability of soil bacteria to successfully compete with a range of other microbial species is crucial for their growth and survival in the nutrient-limited soil environment. In the present work, we studied the behavior and transcriptional responses of soil-inhabiting Pseudomonas fluorescens strain Pf0-1 on nutrient-poor agar to confrontation with strains of three phylogenetically different bacterial genera, that is, Bacillus, Brevundimonas and Pedobacter. Competition for nutrients was apparent as all three bacterial genera had a negative effect on the density of P. fluorescens Pf0-1; this effect was most strong during the interaction with Bacillus. Microarray-based analyses indicated strong differences in the transcriptional responses of Pf0-1 to the different competitors. There was higher similarity in the gene expression response of P. fluorescens Pf0-1 to the Gram-negative bacteria as compared with the Gram-positive strain. The Gram-negative strains did also trigger the production of an unknown broad-spectrum antibiotic in Pf0-1. More detailed analysis indicated that expression of specific Pf0-1 genes involved in signal transduction and secondary metabolite production was strongly affected by the competitors' identity, suggesting that Pf0-1 can distinguish among different competitors and fine-tune its competitive strategies. The results presented here demonstrate that P. fluorescens Pf0-1 shows a species-specific transcriptional and metabolic response to bacterial competitors and provide new leads in the identification of specific cues in bacteria-bacteria interactions and of novel competitive strategies, antimicrobial traits and genes.The ability of soil bacteria to successfully compete with a range of other microbial species is crucial for their growth and survival in the nutrient-limited soil environment. In the present work, we studied the behavior and transcriptional responses of soil-inhabiting Pseudomonas fluorescens strain Pf0-1 on nutrient-poor agar to confrontation with strains of three phylogenetically different bacterial genera, that is, Bacillus, Brevundimonas and Pedobacter. Competition for nutrients was apparent as all three bacterial genera had a negative effect on the density of P. fluorescens Pf0-1; this effect was most strong during the interaction with Bacillus. Microarray-based analyses indicated strong differences in the transcriptional responses of Pf0-1 to the different competitors. There was higher similarity in the gene expression response of P. fluorescens Pf0-1 to the Gram-negative bacteria as compared with the Gram-positive strain. The Gram-negative strains did also trigger the production of an unknown broad-spectrum antibiotic in Pf0-1. More detailed analysis indicated that expression of specific Pf0-1 genes involved in signal transduction and secondary metabolite production was strongly affected by the competitors' identity, suggesting that Pf0-1 can distinguish among different competitors and fine-tune its competitive strategies. The results presented here demonstrate that P. fluorescens Pf0-1 shows a species-specific transcriptional and metabolic response to bacterial competitors and provide new leads in the identification of specific cues in bacteria-bacteria interactions and of novel competitive strategies, antimicrobial traits and genes.
Author Silby, Mark W
Levy, Stuart B
Raaijmakers, Jos M
Garbeva, Paolina
Boer, Wietse de
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  givenname: Mark W
  surname: Silby
  fullname: Silby, Mark W
  organization: Department of Biology, University of Massachusetts Dartmouth
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  surname: Raaijmakers
  fullname: Raaijmakers, Jos M
  organization: Laboratory of Phytopathology, Wageningen University
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  givenname: Stuart B
  surname: Levy
  fullname: Levy, Stuart B
  organization: Department of Molecular Biology and Microbiology, Center for Adaptation Genetics and Drug Resistance, Tufts University School of Medicine
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  givenname: Wietse de
  surname: Boer
  fullname: Boer, Wietse de
  organization: Netherlands institute of Ecology (NIOO-KNAW), Center for Terrestrial Ecology
BackLink https://www.ncbi.nlm.nih.gov/pubmed/21228890$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
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Issue 6
Keywords inter-specific interactions
transcriptional responses
bacterial competition
antibiosis
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Snippet The ability of soil bacteria to successfully compete with a range of other microbial species is crucial for their growth and survival in the nutrient-limited...
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SubjectTerms 631/158/853
631/208/199
631/326/2565/855
631/326/41
aeruginosa
Agar
Alphaproteobacteria - growth & development
Amino Acids - metabolism
Anti-Bacterial Agents - biosynthesis
Antibiosis
Antibiotics
Antimicrobial agents
Bacillus
Bacillus - growth & development
Bacteria
Bacterial Proteins - genetics
Bacteroidetes - growth & development
Biomedical and Life Sciences
biosynthesis
Brevundimonas
chemical communication
Competition
corynebacterium-glutamicum
DNA microarrays
Ecology
Evolutionary Biology
Gene expression
Gene Expression Regulation, Bacterial
Gram-negative bacteria
growth
Life Sciences
Metabolic response
Metabolites
microarray analyses
microbial community composition
Microbial Ecology
Microbial Genetics and Genomics
Microbiology
natural environments
Nutrients
Original
original-article
Pedobacter
Phylogeny
Pseudomonas fluorescens
Pseudomonas fluorescens - genetics
Pseudomonas fluorescens - growth & development
Pseudomonas fluorescens - metabolism
Ribosomal Proteins - genetics
Secondary metabolites
Signal Transduction
Soil
soil bacteria
Soil environment
Soil Microbiology
Soil microorganisms
Soils
Survival
Transcription
Transcription, Genetic
Title Transcriptional and antagonistic responses of Pseudomonas fluorescens Pf0-1 to phylogenetically different bacterial competitors
URI https://link.springer.com/article/10.1038/ismej.2010.196
https://www.ncbi.nlm.nih.gov/pubmed/21228890
https://www.proquest.com/docview/867336677
https://www.proquest.com/docview/867718967
https://www.proquest.com/docview/904468692
https://pubmed.ncbi.nlm.nih.gov/PMC3131853
http://www.narcis.nl/publication/RecordID/oai:library.wur.nl:wurpubs%2F407270
Volume 5
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