Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens

Mark W. Silby, Ana M. Cerdeño-Tárraga, Georgios S. Vernikos, Stephen R. Giddens, Robert W. Jackson, Gail M. Preston, Xue-Xian Zhang, Christina D. Moon, Stefanie M. Gehrig, Scott A. C. Godfrey, Christopher G. Knight, Jacob G. Malone, Zena Robinson, Andrew J. Spiers, Simon Harris, Gregory L. Challis, Alice M Yaxley, David Harris, Kathy Seeger, Lee Murphy & 14 others Simon Rutter, Rob Squares, Michael A. Quail, Elizabeth Saunders, Konstantinos Mavromatis, Thomas S. Brettin, Stephen D. Bentley, Joanne Hothersall, Elton Stephens, Christopher M. Thomas, Julian Parkhill, Stuart B. Levy, Paul B. Rainey, Nicholas R. Thomson

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Abstract

Background: Pseudomonas fluorescens are common soil bacteria that can improve plant health through nutrient cycling, pathogen antagonism and induction of plant defenses. The genome sequences of strains SBW25 and Pf0-1 were determined and compared to each other and with P. fluorescens Pf-5. A functional genomic in vivo expression technology (IVET) screen provided insight into genes used by P. fluorescens in its natural environment and an improved understanding of the ecological significance of diversity within this species. Results: Comparisons of three P. fluorescens genomes (SBW25, Pf0-1, Pf-5) revealed considerable divergence: 61% of genes are shared, the majority located near the replication origin. Phylogenetic and average amino acid identity analyses showed a low overall relationship. A functional screen of SBW25 defined 125 plant-induced genes including a range of functions specific to the plant environment. Orthologues of 83 of these exist in Pf0-1 and Pf-5, with 73 shared by both strains. The P. fluorescens genomes carry numerous complex repetitive DNA sequences, some resembling Miniature Inverted-repeat Transposable Elements (MITEs). In SBW25, repeat density and distribution revealed 'repeat deserts' lacking repeats, covering approximately 40% of the genome. Conclusions: P. fluorescens genomes are highly diverse. Strain-specific regions around the replication terminus suggest genome compartmentalization. The genomic heterogeneity among the three strains is reminiscent of a species complex rather than a single species. That 42% of plantinducible genes were not shared by all strains reinforces this conclusion and shows that ecological success requires specialized and core functions. The diversity also indicates the significant size of genetic information within the Pseudomonas pan genome.
Original languageEnglish
Article numberR51
Number of pages16
JournalGenome Biology
Volume10
DOIs
StatePublished - May 2009

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Pseudomonas fluorescens
genome
genes
genomics
miniature inverted repeat transposable elements
replication origin
plant health
soil bacteria
Pseudomonas
biogeochemical cycles
deserts
nucleotide sequences
amino acids
pathogens
phylogeny

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Silby, M. W., Cerdeño-Tárraga, A. M., Vernikos, G. S., Giddens, S. R., Jackson, R. W., Preston, G. M., ... Thomson, N. R. (2009). Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biology, 10, [R51]. DOI: 10.1186/gb-2009-10-5-r51

Silby, Mark W.; Cerdeño-Tárraga, Ana M.; Vernikos, Georgios S.; Giddens, Stephen R.; Jackson, Robert W.; Preston, Gail M.; Zhang, Xue-Xian; Moon, Christina D.; Gehrig, Stefanie M.; Godfrey, Scott A. C.; Knight, Christopher G.; Malone, Jacob G.; Robinson, Zena; Spiers, Andrew J.; Harris, Simon; Challis, Gregory L.; Yaxley, Alice M; Harris, David; Seeger, Kathy; Murphy, Lee; Rutter, Simon; Squares, Rob; Quail, Michael A.; Saunders, Elizabeth; Mavromatis, Konstantinos; Brettin, Thomas S.; Bentley, Stephen D.; Hothersall, Joanne; Stephens, Elton; Thomas, Christopher M.; Parkhill, Julian; Levy, Stuart B.; Rainey, Paul B.; Thomson, Nicholas R. / Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens.

In: Genome Biology, Vol. 10, R51, 05.2009.

Research output: Contribution to journalArticle

@article{e73b59d76c07441a82dae5864748674b,
title = "Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens",
abstract = "Background: Pseudomonas fluorescens are common soil bacteria that can improve plant health through nutrient cycling, pathogen antagonism and induction of plant defenses. The genome sequences of strains SBW25 and Pf0-1 were determined and compared to each other and with P. fluorescens Pf-5. A functional genomic in vivo expression technology (IVET) screen provided insight into genes used by P. fluorescens in its natural environment and an improved understanding of the ecological significance of diversity within this species. Results: Comparisons of three P. fluorescens genomes (SBW25, Pf0-1, Pf-5) revealed considerable divergence: 61% of genes are shared, the majority located near the replication origin. Phylogenetic and average amino acid identity analyses showed a low overall relationship. A functional screen of SBW25 defined 125 plant-induced genes including a range of functions specific to the plant environment. Orthologues of 83 of these exist in Pf0-1 and Pf-5, with 73 shared by both strains. The P. fluorescens genomes carry numerous complex repetitive DNA sequences, some resembling Miniature Inverted-repeat Transposable Elements (MITEs). In SBW25, repeat density and distribution revealed 'repeat deserts' lacking repeats, covering approximately 40% of the genome. Conclusions: P. fluorescens genomes are highly diverse. Strain-specific regions around the replication terminus suggest genome compartmentalization. The genomic heterogeneity among the three strains is reminiscent of a species complex rather than a single species. That 42% of plantinducible genes were not shared by all strains reinforces this conclusion and shows that ecological success requires specialized and core functions. The diversity also indicates the significant size of genetic information within the Pseudomonas pan genome.",
author = "Silby, {Mark W.} and Cerdeño-Tárraga, {Ana M.} and Vernikos, {Georgios S.} and Giddens, {Stephen R.} and Jackson, {Robert W.} and Preston, {Gail M.} and Xue-Xian Zhang and Moon, {Christina D.} and Gehrig, {Stefanie M.} and Godfrey, {Scott A. C.} and Knight, {Christopher G.} and Malone, {Jacob G.} and Zena Robinson and Spiers, {Andrew J.} and Simon Harris and Challis, {Gregory L.} and Yaxley, {Alice M} and David Harris and Kathy Seeger and Lee Murphy and Simon Rutter and Rob Squares and Quail, {Michael A.} and Elizabeth Saunders and Konstantinos Mavromatis and Brettin, {Thomas S.} and Bentley, {Stephen D.} and Joanne Hothersall and Elton Stephens and Thomas, {Christopher M.} and Julian Parkhill and Levy, {Stuart B.} and Rainey, {Paul B.} and Thomson, {Nicholas R.}",
year = "2009",
month = "5",
doi = "10.1186/gb-2009-10-5-r51",
volume = "10",
journal = "Genome Biology",
issn = "1465-6906",

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Silby, MW, Cerdeño-Tárraga, AM, Vernikos, GS, Giddens, SR, Jackson, RW, Preston, GM, Zhang, X-X, Moon, CD, Gehrig, SM, Godfrey, SAC, Knight, CG, Malone, JG, Robinson, Z, Spiers, AJ, Harris, S, Challis, GL, Yaxley, AM, Harris, D, Seeger, K, Murphy, L, Rutter, S, Squares, R, Quail, MA, Saunders, E, Mavromatis, K, Brettin, TS, Bentley, SD, Hothersall, J, Stephens, E, Thomas, CM, Parkhill, J, Levy, SB, Rainey, PB & Thomson, NR 2009, 'Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens' Genome Biology, vol 10, R51. DOI: 10.1186/gb-2009-10-5-r51

Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. / Silby, Mark W.; Cerdeño-Tárraga, Ana M.; Vernikos, Georgios S.; Giddens, Stephen R.; Jackson, Robert W.; Preston, Gail M.; Zhang, Xue-Xian; Moon, Christina D.; Gehrig, Stefanie M.; Godfrey, Scott A. C.; Knight, Christopher G.; Malone, Jacob G.; Robinson, Zena; Spiers, Andrew J.; Harris, Simon; Challis, Gregory L.; Yaxley, Alice M; Harris, David; Seeger, Kathy; Murphy, Lee; Rutter, Simon; Squares, Rob; Quail, Michael A.; Saunders, Elizabeth; Mavromatis, Konstantinos; Brettin, Thomas S.; Bentley, Stephen D.; Hothersall, Joanne; Stephens, Elton; Thomas, Christopher M.; Parkhill, Julian; Levy, Stuart B.; Rainey, Paul B.; Thomson, Nicholas R.

In: Genome Biology, Vol. 10, R51, 05.2009.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens

AU - Silby,Mark W.

AU - Cerdeño-Tárraga,Ana M.

AU - Vernikos,Georgios S.

AU - Giddens,Stephen R.

AU - Jackson,Robert W.

AU - Preston,Gail M.

AU - Zhang,Xue-Xian

AU - Moon,Christina D.

AU - Gehrig,Stefanie M.

AU - Godfrey,Scott A. C.

AU - Knight,Christopher G.

AU - Malone,Jacob G.

AU - Robinson,Zena

AU - Spiers,Andrew J.

AU - Harris,Simon

AU - Challis,Gregory L.

AU - Yaxley,Alice M

AU - Harris,David

AU - Seeger,Kathy

AU - Murphy,Lee

AU - Rutter,Simon

AU - Squares,Rob

AU - Quail,Michael A.

AU - Saunders,Elizabeth

AU - Mavromatis,Konstantinos

AU - Brettin,Thomas S.

AU - Bentley,Stephen D.

AU - Hothersall,Joanne

AU - Stephens,Elton

AU - Thomas,Christopher M.

AU - Parkhill,Julian

AU - Levy,Stuart B.

AU - Rainey,Paul B.

AU - Thomson,Nicholas R.

PY - 2009/5

Y1 - 2009/5

N2 - Background: Pseudomonas fluorescens are common soil bacteria that can improve plant health through nutrient cycling, pathogen antagonism and induction of plant defenses. The genome sequences of strains SBW25 and Pf0-1 were determined and compared to each other and with P. fluorescens Pf-5. A functional genomic in vivo expression technology (IVET) screen provided insight into genes used by P. fluorescens in its natural environment and an improved understanding of the ecological significance of diversity within this species. Results: Comparisons of three P. fluorescens genomes (SBW25, Pf0-1, Pf-5) revealed considerable divergence: 61% of genes are shared, the majority located near the replication origin. Phylogenetic and average amino acid identity analyses showed a low overall relationship. A functional screen of SBW25 defined 125 plant-induced genes including a range of functions specific to the plant environment. Orthologues of 83 of these exist in Pf0-1 and Pf-5, with 73 shared by both strains. The P. fluorescens genomes carry numerous complex repetitive DNA sequences, some resembling Miniature Inverted-repeat Transposable Elements (MITEs). In SBW25, repeat density and distribution revealed 'repeat deserts' lacking repeats, covering approximately 40% of the genome. Conclusions: P. fluorescens genomes are highly diverse. Strain-specific regions around the replication terminus suggest genome compartmentalization. The genomic heterogeneity among the three strains is reminiscent of a species complex rather than a single species. That 42% of plantinducible genes were not shared by all strains reinforces this conclusion and shows that ecological success requires specialized and core functions. The diversity also indicates the significant size of genetic information within the Pseudomonas pan genome.

AB - Background: Pseudomonas fluorescens are common soil bacteria that can improve plant health through nutrient cycling, pathogen antagonism and induction of plant defenses. The genome sequences of strains SBW25 and Pf0-1 were determined and compared to each other and with P. fluorescens Pf-5. A functional genomic in vivo expression technology (IVET) screen provided insight into genes used by P. fluorescens in its natural environment and an improved understanding of the ecological significance of diversity within this species. Results: Comparisons of three P. fluorescens genomes (SBW25, Pf0-1, Pf-5) revealed considerable divergence: 61% of genes are shared, the majority located near the replication origin. Phylogenetic and average amino acid identity analyses showed a low overall relationship. A functional screen of SBW25 defined 125 plant-induced genes including a range of functions specific to the plant environment. Orthologues of 83 of these exist in Pf0-1 and Pf-5, with 73 shared by both strains. The P. fluorescens genomes carry numerous complex repetitive DNA sequences, some resembling Miniature Inverted-repeat Transposable Elements (MITEs). In SBW25, repeat density and distribution revealed 'repeat deserts' lacking repeats, covering approximately 40% of the genome. Conclusions: P. fluorescens genomes are highly diverse. Strain-specific regions around the replication terminus suggest genome compartmentalization. The genomic heterogeneity among the three strains is reminiscent of a species complex rather than a single species. That 42% of plantinducible genes were not shared by all strains reinforces this conclusion and shows that ecological success requires specialized and core functions. The diversity also indicates the significant size of genetic information within the Pseudomonas pan genome.

U2 - 10.1186/gb-2009-10-5-r51

DO - 10.1186/gb-2009-10-5-r51

M3 - Article

VL - 10

JO - Genome Biology

T2 - Genome Biology

JF - Genome Biology

SN - 1465-6906

M1 - R51

ER -

Silby MW, Cerdeño-Tárraga AM, Vernikos GS, Giddens SR, Jackson RW, Preston GM et al. Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biology. 2009 May;10. R51. Available from, DOI: 10.1186/gb-2009-10-5-r51