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Title: Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial

Abstract

Pseudomonas aeruginosa is a ubiquitous environmental bacterium and an important opportunistic human pathogen. Generally, the acquisition of genes in the form of pathogenicity islands distinguishes pathogenic isolates from nonpathogens. We therefore sequenced a highly virulent strain of P. aeruginosa, PA14, and compared it with a previously sequenced (and less pathogenic) strain, PAO1, to identify novel virulence genes. The PA14 and PAO1 genomes are remarkably similar, although PA14 has a slightly larger genome (6.5 megabses [Mb]) than does PAO1 (6.3 Mb). We identified 58 PA14 gene clusters that are absent in PAO1 to determine which of these genes, if any, contribute to its enhanced virulence in a Caenorhabditis elegans pathogenicity model. First, we tested 18 additional diverse strains in the C. elegans model and observed a wide range of pathogenic potential; however, genotyping these strains using a custom microarray showed that the presence of PA14 genes that are absent in PAO1 did not correlate with the virulence of these strains. Second, we utilized a full-genome nonredundant mutant library of PA14 to identify five genes (absent in PAO1) required for C. elegans killing. Surprisingly, although these five genes are present in many other P. aeruginosa strains, they do not correlate with virulencemore » in C. elegans. Genes required for pathogenicity in one strain of P. aeruginosa are neither required for nor predictive of virulence in other strains. We therefore propose that virulence in this organism is both multifactorial and combinatorial, the result of a pool of pathogenicity-related genes that interact in various combinations in different genetic backgrounds.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [2];  [3];  [3];  [3];  [4];  [5];  [6];  [5];  [5];  [3];  [1]
+ Show Author Affiliations
  1. Massachusetts General Hospital, Boston, MA (United States); Harvard Medical School, Boston, MA (United States)
  2. Envivo Pharmaceuticals, Inc., Watertown, MA (United States)
  3. Harvard Medical School, Boston, MA (United States); Massachusetts General Hospital, Boston, MA (United States)
  4. Harvard Medical School, Boston, MA (United States)
  5. Cubist Pharmaceuticals, Inc., Lexington, MA (United States)
  6. Cubist Pharmaceuticals, Inc., Lexington, MA (United States); Harvard Medical School, Boston, MA (United States)
Publication Date:
Research Org.:
Harvard Medical School, Boston, MA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Jane Coffin Childs Memorial fund; Harvard-Partners Center for Genetics and Genomics
OSTI Identifier:
1626705
Grant/Contract Number:  
FG02-ER63445; U01 HL66678; R01 AI064332
Resource Type:
Accepted Manuscript
Journal Name:
GenomeBiology.com
Additional Journal Information:
Journal Volume: 7; Journal Issue: 10; Journal ID: ISSN 1465-6906
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; cystic fibrosis; additional data file; pathogenicity; genomic content; cystic fibrosis isolate

Citation Formats

Lee, Daniel G., Urbach, Jonathan M., Wu, Gang, Liberati, Nicole T., Feinbaum, Rhonda L., Miyata, Sachiko, Diggins, Lenard T., He, Jianxin, Saucier, Maude, Deziel, Eric, Friedman, Lisa, Li, Li, Grills, George, Montgomery, Kate, Kucherlapati, Raju, Rahme, Laurence G., and Ausubel, Frederick M. Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. United States: N. p., 2006. Web. doi:10.1186/gb-2006-7-10-r90.
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Lee, Daniel G., Urbach, Jonathan M., Wu, Gang, Liberati, Nicole T., Feinbaum, Rhonda L., Miyata, Sachiko, Diggins, Lenard T., He, Jianxin, Saucier, Maude, Deziel, Eric, Friedman, Lisa, Li, Li, Grills, George, Montgomery, Kate, Kucherlapati, Raju, Rahme, Laurence G., & Ausubel, Frederick M. Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. United States. https://doi.org/10.1186/gb-2006-7-10-r90
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Lee, Daniel G., Urbach, Jonathan M., Wu, Gang, Liberati, Nicole T., Feinbaum, Rhonda L., Miyata, Sachiko, Diggins, Lenard T., He, Jianxin, Saucier, Maude, Deziel, Eric, Friedman, Lisa, Li, Li, Grills, George, Montgomery, Kate, Kucherlapati, Raju, Rahme, Laurence G., and Ausubel, Frederick M. Thu . "Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial". United States. https://doi.org/10.1186/gb-2006-7-10-r90. https://www.osti.gov/servlets/purl/1626705.
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@article{osti_1626705,
title = {Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial},
author = {Lee, Daniel G. and Urbach, Jonathan M. and Wu, Gang and Liberati, Nicole T. and Feinbaum, Rhonda L. and Miyata, Sachiko and Diggins, Lenard T. and He, Jianxin and Saucier, Maude and Deziel, Eric and Friedman, Lisa and Li, Li and Grills, George and Montgomery, Kate and Kucherlapati, Raju and Rahme, Laurence G. and Ausubel, Frederick M.},
abstractNote = {Pseudomonas aeruginosa is a ubiquitous environmental bacterium and an important opportunistic human pathogen. Generally, the acquisition of genes in the form of pathogenicity islands distinguishes pathogenic isolates from nonpathogens. We therefore sequenced a highly virulent strain of P. aeruginosa, PA14, and compared it with a previously sequenced (and less pathogenic) strain, PAO1, to identify novel virulence genes. The PA14 and PAO1 genomes are remarkably similar, although PA14 has a slightly larger genome (6.5 megabses [Mb]) than does PAO1 (6.3 Mb). We identified 58 PA14 gene clusters that are absent in PAO1 to determine which of these genes, if any, contribute to its enhanced virulence in a Caenorhabditis elegans pathogenicity model. First, we tested 18 additional diverse strains in the C. elegans model and observed a wide range of pathogenic potential; however, genotyping these strains using a custom microarray showed that the presence of PA14 genes that are absent in PAO1 did not correlate with the virulence of these strains. Second, we utilized a full-genome nonredundant mutant library of PA14 to identify five genes (absent in PAO1) required for C. elegans killing. Surprisingly, although these five genes are present in many other P. aeruginosa strains, they do not correlate with virulence in C. elegans. Genes required for pathogenicity in one strain of P. aeruginosa are neither required for nor predictive of virulence in other strains. We therefore propose that virulence in this organism is both multifactorial and combinatorial, the result of a pool of pathogenicity-related genes that interact in various combinations in different genetic backgrounds.},
doi = {10.1186/gb-2006-7-10-r90},
journal = {GenomeBiology.com},
number = 10,
volume = 7,
place = {United States},
year = {Thu Oct 12 00:00:00 EDT 2006},
month = {Thu Oct 12 00:00:00 EDT 2006}
}
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  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 47
  • DOI: 10.1073/pnas.1415712111

Comparative genomics of clinical strains of Pseudomonas aeruginosa strains isolated from different geographic sites
journal, October 2018

Reverse Genetic Systems for Pseudomonas aeruginosa Leviphages
journal, March 2019

  • Lee, Jae-Yeol; Ahn, Se-Jeong; Park, Chanseop
  • Methods and Protocols, Vol. 2, Issue 1
  • DOI: 10.3390/mps2010022

Mechanism of foreign DNA recognition by a CRISPR RNA-guided surveillance complex from Pseudomonas aeruginosa
journal, February 2015

  • Rollins, MaryClare F.; Schuman, Jason T.; Paulus, Kirra
  • Nucleic Acids Research, Vol. 43, Issue 4
  • DOI: 10.1093/nar/gkv094

New Life for an Old Drug: the Anthelmintic Drug Niclosamide Inhibits Pseudomonas aeruginosa Quorum Sensing
journal, December 2012

  • Imperi, F.; Massai, F.; Ramachandran Pillai, C.
  • Antimicrobial Agents and Chemotherapy, Vol. 57, Issue 2
  • DOI: 10.1128/aac.01952-12

The Two-Component Sensor KinB Acts as a Phosphatase To Regulate Pseudomonas aeruginosa Virulence
journal, December 2012

  • Chand, Nikhilesh S.; Clatworthy, Anne E.; Hung, Deborah T.
  • Journal of Bacteriology, Vol. 194, Issue 23
  • DOI: 10.1128/jb.01168-12

Role of Pseudomonas aeruginosa Peptidoglycan-Associated Outer Membrane Proteins in Vesicle Formation
journal, January 2013

  • Wessel, Aimee K.; Liew, Jean; Kwon, Taejoon
  • Journal of Bacteriology, Vol. 195, Issue 2
  • DOI: 10.1128/jb.01253-12

The Pseudomonas aeruginosa accessory genome elements influence virulence towards Caenorhabditis elegans
journal, December 2019

  • Vasquez-Rifo, Alejandro; Veksler-Lublinsky, Isana; Cheng, Zhenyu
  • Genome Biology, Vol. 20, Issue 1
  • DOI: 10.1186/s13059-019-1890-1

Exemplar Abstract for Pseudomonas aeruginosa (Schroeter 1872) Migula 1900 (Approved Lists 1980).
dataset, January 2013

  • Parker, Charles Thomas; Taylor, Dorothea; Garrity, George M.
  • DOI: 10.1601/ex.16926

Defining the Pseudomonas Genus: Where Do We Draw the Line with Azotobacter?
journal, August 2011

Parallel evolutionary paths to produce more than one Pseudomonas aeruginosa biofilm phenotype
journal, January 2020

  • Thöming, Janne G.; Tomasch, Jürgen; Preusse, Matthias
  • npj Biofilms and Microbiomes, Vol. 6, Issue 1
  • DOI: 10.1038/s41522-019-0113-6

Comparative genomics of clinical strains of Pseudomonas aeruginosa strains isolated from different geographic sites
journal, October 2018

Virulence Characteristics and an Action Mode of Antibiotic Resistance in Multidrug-Resistant Pseudomonas aeruginosa
journal, January 2019

Genomic characterization of a local epidemic Pseudomonas aeruginosa reveals specific features of the widespread clone ST395
journal, October 2017

  • Petitjean, Marie; Martak, Daniel; Silvant, Alicia
  • Microbial Genomics, Vol. 3, Issue 10
  • DOI: 10.1099/mgen.0.000129

Not all Pseudomonas aeruginosa are equal: strains from industrial sources possess uniquely large multireplicon genomes
journal, July 2019

  • Weiser, Rebecca; Green, Angharad E.; Bull, Matthew J.
  • Microbial Genomics, Vol. 5, Issue 7
  • DOI: 10.1099/mgen.0.000276

High-throughput detection of RNA processing in bacteria
posted_content, September 2016

  • Gill, Erin E.; Chan, Luisa S.; Winsor, Geoffrey L.
  • DOI: 10.1101/073791

Complete Genome Sequence of Pseudomonas aeruginosa PA1, Isolated from a Patient with a Respiratory Tract Infection
journal, December 2015

A Shift in Central Metabolism Accompanies Virulence Activation in Pseudomonas aeruginosa
journal, March 2020

A High-Content, Phenotypic Screen Identifies Fluorouridine as an Inhibitor of Pyoverdine Biosynthesis and Pseudomonas aeruginosa Virulence
journal, August 2016

  • Kirienko, Daniel R.; Revtovich, Alexey V.; Kirienko, Natalia V.
  • mSphere, Vol. 1, Issue 4
  • DOI: 10.1128/msphere.00217-16

Evaluation of a microarray-hybridization based method applicable for discovery of single nucleotide polymorphisms (SNPs) in the Pseudomonas aeruginosa genome
journal, January 2009

  • Dötsch, Andreas; Pommerenke, Claudia; Bredenbruch, Florian
  • BMC Genomics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2164-10-29

Evolutionary conservation of essential and highly expressed genes in Pseudomonas aeruginosa
journal, April 2010

Core and accessory genome architecture in a group of Pseudomonas aeruginosa Mu-like phages
journal, December 2014

  • Cazares, Adrián; Mendoza-Hernández, Guillermo; Guarneros, Gabriel
  • BMC Genomics, Vol. 15, Issue 1
  • DOI: 10.1186/1471-2164-15-1146

Pseudomonas aeruginosa clinical and environmental isolates constitute a single population with high phenotypic diversity
journal, January 2014

  • Grosso-Becerra, María-Victoria; Santos-Medellín, Christian; González-Valdez, Abigail
  • BMC Genomics, Vol. 15, Issue 1
  • DOI: 10.1186/1471-2164-15-318

Characterization of the core and accessory genomes of Pseudomonas aeruginosa using bioinformatic tools Spine and AGEnt
journal, January 2014

Antagonistic interactions peak at intermediate genetic distance in clinical and laboratory strains of Pseudomonas aeruginosa
journal, January 2012

  • Schoustra, Sijmen E.; Dench, Jonathan; Dali, Rola
  • BMC Microbiology, Vol. 12, Issue 1
  • DOI: 10.1186/1471-2180-12-40

Novel Tn4371-ICE like element in Ralstonia pickettiiand Genome mining for comparative elements
journal, November 2009

  • Ryan, Michael P.; Pembroke, J. Tony; Adley, Catherine C.
  • BMC Microbiology, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2180-9-242

Mobile genetic elements in the genome of the beneficial rhizobacterium Pseudomonas fluorescens Pf-5
journal, January 2009

  • Mavrodi, Dmitri V.; Loper, Joyce E.; Paulsen, Ian T.
  • BMC Microbiology, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2180-9-8

Comparative transcriptome analyses of Pseudomonas aeruginosa
journal, January 2009

Prevalence and analysis of Pseudomonas aeruginosa in chinchillas
journal, November 2010

  • Hirakawa, Yasuko; Sasaki, Hiraku; Kawamoto, Eiichi
  • BMC Veterinary Research, Vol. 6, Issue 1
  • DOI: 10.1186/1746-6148-6-52

G4PromFinder: an algorithm for predicting transcription promoters in GC-rich bacterial genomes based on AT-rich elements and G-quadruplex motifs
journal, February 2018

Isolation and characterization of HepP: a virulence-related Pseudomonas aeruginosa heparinase
journal, December 2017

  • Dzvova, Nyaradzo; Colmer-Hamood, Jane A.; Griswold, John A.
  • BMC Microbiology, Vol. 17, Issue 1
  • DOI: 10.1186/s12866-017-1141-0

The Pseudomonas aeruginosa accessory genome elements influence virulence towards Caenorhabditis elegans
journal, December 2019

  • Vasquez-Rifo, Alejandro; Veksler-Lublinsky, Isana; Cheng, Zhenyu
  • Genome Biology, Vol. 20, Issue 1
  • DOI: 10.1186/s13059-019-1890-1

Advances in understanding Pseudomonas
journal, February 2014

  • Tümmler, Burkhard; Wiehlmann, Lutz; Klockgether, Jens
  • F1000Prime Reports, Vol. 6
  • DOI: 10.12703/p6-9

Reconciling high-throughput gene essentiality data with metabolic network reconstructions
journal, April 2019

Activity and Impact on Resistance Development of Two Antivirulence Fluoropyrimidine Drugs in Pseudomonas aeruginosa
journal, March 2019

  • Imperi, Francesco; Fiscarelli, Ersilia V.; Visaggio, Daniela
  • Frontiers in Cellular and Infection Microbiology, Vol. 9
  • DOI: 10.3389/fcimb.2019.00049

Pseudomonas aeruginosa Genomic Structure and Diversity
journal, January 2011

Clinical utilization of genomics data produced by the international Pseudomonas aeruginosa consortium
journal, September 2015

Identification of Novel Genomic Islands in Liverpool Epidemic Strain of Pseudomonas aeruginosa Using Segmentation and Clustering
journal, August 2016

Fitness Cost of Fluoroquinolone Resistance in Clinical Isolates of Pseudomonas aeruginosa Differs by Type III Secretion Genotype
journal, October 2016

  • Agnello, Melissa; Finkel, Steven E.; Wong-Beringer, Annie
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.01591

Broth versus Surface-Grown Cells: Differential Regulation of RsmY/Z Small RNAs in Pseudomonas aeruginosa by the Gac/HptB System
journal, January 2017

1-((2,4-Dichlorophenethyl)Amino)-3-Phenoxypropan-2-ol Kills Pseudomonas aeruginosa through Extensive Membrane Damage
journal, February 2018

The Nif3-Family Protein YqfO03 from Pseudomonas syringae MB03 Has Multiple Nematicidal Activities against Caenorhabditis elegans and Meloidogyne incognita
journal, December 2018

  • Manan, Abdul; Bazai, Zahoor; Fan, Jin
  • International Journal of Molecular Sciences, Vol. 19, Issue 12
  • DOI: 10.3390/ijms19123915

Coping with Environmental Eukaryotes; Identification of Pseudomonas syringae Genes during the Interaction with Alternative Hosts or Predators
journal, April 2018

Model-Driven Controlled Alteration of Nanopillar Cap Architecture Reveals its Effects on Bactericidal Activity
journal, January 2020

Reverse Genetic Systems for Pseudomonas aeruginosa Leviphages
journal, March 2019

  • Lee, Jae-Yeol; Ahn, Se-Jeong; Park, Chanseop
  • Methods and Protocols, Vol. 2, Issue 1
  • DOI: 10.3390/mps2010022

Effect of Polymer Demixed Nanotopographies on Bacterial Adhesion and Biofilm Formation
journal, November 2019

  • Fleming, George; Aveyard, Jenny; Fothergill, Joanne L.
  • Polymers, Vol. 11, Issue 12
  • DOI: 10.3390/polym11121921

Nitric Oxide Releasing Polymeric Coatings for the Prevention of Biofilm Formation
journal, November 2017

  • Fleming, George; Aveyard, Jenny; Fothergill, Joanne
  • Polymers, Vol. 9, Issue 11
  • DOI: 10.3390/polym9110601

Exemplar Abstract for Pseudomonas aeruginosa (Schroeter 1872) Migula 1900 (Approved Lists 1980).
dataset, January 2013

  • Parker, Charles Thomas; Taylor, Dorothea; Garrity, George M.
  • DOI: 10.1601/ex.21651
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