. (2009) Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biology (Online), Vol.10 (No.5). R51. ISSN 1474-760X

Preview

PDF WRAP_Challis_gb-2009-10-5-r51.pdf - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader Download (3383Kb)

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 plant-inducible 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.

Item Type:	Journal Article
Subjects:	S Agriculture > SB Plant culture Q Science > QR Microbiology
Divisions:	Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010) Faculty of Science > Chemistry
Library of Congress Subject Headings (LCSH):	Pseudomonas fluorescens, Bacterial genetics -- Research, Gram-negative bacteria, Plant-microbe relationships
Journal or Publication Title:	Genome Biology (Online)
Publisher:	BioMed Central Ltd.
ISSN:	1474-760X
Date:	11 May 2009
Volume:	Vol.10
Number:	No.5
Number of Pages:	16
Page Range:	R51
Identification Number:	10.1186/gb-2009-10-5-r51
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Funder:	Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), Wellcome Trust (London, England), United States. Dept. of Energy. Office of Biological and Environmental Research, Lawrence Livermore Laboratory (LLL), Lawrence Berkeley National Laboratory (LBNL), Los Alamos National Laboratory (LANL), United States. Dept. of Agriculture, Foundation for Research, Science & Technology (N.Z.) (FRST)
Grant number:	104/P16729 (BBSRC), P15257 (BBSRC), W-7405-Eng-48 (LLL), DE-AC03-76SF00098 (LBNL), W-7405-ENG-36 (LANL), 2006-35604-16673 (USDA)
References:	# Naseby DC, Way JA, Bainton NJ, Lynch JM: Biocontrol of Pythium in the pea rhizosphere by antifungal metabolite producing and non-producing Pseudomonas strains. J Appl Microbiol 2001, 90:421-429. # Rodriguez F, Pfender WF: Antibiosis and antagonism of Sclerotinia homoeocarpa and Drechslera poae by Pseudomonas fluorescens Pf-5 in vitro and in planta. Phytopathology 1997, 87:614-621. # de Bruijn I, de Kock MJ, Yang M, de Waard P, van Beek TA, Raaijmakers JM: Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide antibiotics in Pseudomonas species. Mol Microbiol 2007, 63:417-428. # Haas D, Defago G: Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 2005, 3:307-319. # Rainey PB: Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ Microbiol 1999, 1:243-257. # Gal M, Preston GM, Massey RC, Spiers AJ, Rainey PB: Genes encoding a cellulosic polymer contribute toward the ecological success of Pseudomonas fluorescens SBW25 on plant surfaces. Mol Ecol 2003, 12:3109-3121. # Silby MW, Levy SB: Use of in vivo expression technology to identify genes important in growth and survival of Pseudomonas fluorescens Pf0-1 in soil: discovery of expressed sequences with novel genetic organization. J Bacteriol 2004, 186:7411-7419. # Yang S, Perna NT, Cooksey DA, Okinaka Y, Lindow SE, Ibekwe AM, Keen NT, Yang CH: Genome-wide identification of plant-upregulated genes of Erwinia chrysanthemi 3937 using a GFP-based IVET leaf array. Mol Plant Microbe Interact 2004, 17:999-1008. # Rediers H, Bonnecarrere V, Rainey PB, Hamonts K, Vanderleyden J, De Mot R: Development and application of a dapB-based in vivo expression technology system to study colonization of rice by the endophytic nitrogen-fixing bacterium Pseudomonas stutzeri A15. Appl Environ Microbiol 2003, 69:6864-6874. # Preston GM, Bertrand N, Rainey PB: Type III secretion in plant growth-promoting Pseudomonas fluorescens SBW25. Mol Microbiol 2001, 41:999-1014. # Jackson RW, Preston GM, Rainey PB: Genetic characterization of Pseudomonas fluorescens SBW25 rsp gene expression in the phytosphere and in vitro. J Bacteriol 2005, 187:8477-8488. # Giddens SR, Jackson RW, Moon CD, Jacobs MA, Zhang XX, Gehrig SM, Rainey PB: Mutational activation of niche-specific genes provides insight into regulatory networks and bacterial function in a complex environment. Proc Natl Acad Sci USA 2007, 104:18247-18252. # Zhang XX, Rainey PB: Regulation of copper homeostasis in Pseudomonas fluorescens SBW25. Environ Microbiol 2008, 10:3284-3294. # Zhang XX, Scott K, Meffin R, Rainey PB: Genetic characterization of psp encoding the DING protein in Pseudomonas fluorescens SBW25. BMC Microbiol 2007, 7:114. # Zhang XX, George A, Bailey MJ, Rainey PB: The histidine utilization (hut) genes of Pseudomonas fluorescens SBW25 are active on plant surfaces, but are not required for competitive colonization of sugar beet seedlings. Microbiology 2006, 152:1867-1875. # Howden AJ, Harrison CJ, Preston GM: A conserved mechanism for nitrile metabolism in bacteria and plants. Plant J 2009, 57:243-253. # Moon CD, Zhang XX, Matthijs S, Schafer M, Budzikiewicz H, Rainey PB: Genomic, genetic and structural analysis of pyoverdine-mediated iron acquisition in the plant growth-promoting bacterium Pseudomonas fluorescens SBW25. BMC Microbiol 2008, 8:7. # Paulsen IT, Press CM, Ravel J, Kobayashi DY, Myers GS, Mavrodi DV, DeBoy RT, Seshadri R, Ren Q, Madupu R, Dodson RJ, Durkin AS, Brinkac LM, Daugherty SC, Sullivan SA, Rosovitz MJ, Gwinn ML, Zhou L, Schneider DJ, Cartinhour SW, Nelson WC, Weidman J, Watkins K, Tran K, Khouri H, Pierson EA, Pierson LS 3rd, Thomashow LS, Loper JE: Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nat Biotechnol 2005, 23:873-878. # Rainey PB, Bailey MJ: Physical and genetic map of the Pseudomonas fluorescens SBW25 chromosome. Mol Microbiol 1996, 19:521-533. # Rainey PB, Travisano M: Adaptive radiation in a heterogeneous environment. Nature 1998, 394:69-72. # Bantinaki E, Kassen R, Knight CG, Robinson Z, Spiers AJ, Rainey PB: Adaptive divergence in experimental populations of Pseudomonas fluorescens. III. Mutational origins of wrinkly spreader diversity. Genetics 2007, 176:441-453. # Compeau G, Al-Achi BJ, Platsouka E, Levy SB: Survival of rifampin-resistant mutants of Pseudomonas fluorescens and Pseudomonas putida in soil systems. Appl Environ Microbiol 1988, 54:2432-2438. # Mathee K, Narasimhan G, Valdes C, Qiu X, Matewish JM, Koehrsen M, Rokas A, Yandava CN, Engels R, Zeng E, Olavarietta R, Doud M, Smith RS, Montgomery P, White JR, Godfrey PA, Kodira C, Birren B, Galagan JE, Lory S: Dynamics of Pseudomonas aeruginosa genome evolution. Proc Natl Acad Sci USA 2008, 105:3100-3105. # Hughes D: Evaluating genome dynamics: the constraints on rearrangements within bacterial genomes. Genome Biol 2000, 1:REVIEWS0006. # Tett A, Spiers AJ, Crossman LC, Ager D, Ciric L, Dow JM, Fry JC, Harris D, Lilley A, Oliver A, Parkhill J, Quail MA, Rainey PB, Saunders NJ, Seeger K, Snyder LA, Squares R, Thomas CM, Turner SL, Zhang XX, Field D, Bailey MJ: Sequence-based analysis of pQBR103; a representative of a unique, transfer-proficient mega plasmid resident in the microbial community of sugar beet. ISME J 2007, 1:331-340. # Lilley AK, Bailey MJ: The acquisition of indigenous plasmids by a genetically marked pseudomonad population colonizing the sugar beet phytosphere is related to local environmental conditions. Appl Environ Microbiol 1997, 63:1577-1583. # Bentley SD, Chater KF, Cerdeño-Tárraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S, Huang CH, Kieser T, Larke L, Murphy L, Oliver K, O'Neil S, Rabbinowitsch E, Rajandream MA, Rutherford K, et al.: Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 2002, 417:141-147. # Daubin V, Ochman H: Bacterial genomes as new gene homes: the genealogy of ORFans in E. coli. Genome Res 2004, 14:1036-1042. # Dykhuizen DE, Green L: Recombination in Escherichia coli and the definition of biological species. J Bacteriol 1991, 173:7257-7268. # Curran B, Jonas D, Grundmann H, Pitt T, Dowson CG: Development of a multilocus sequence typing scheme for the opportunistic pathogen Pseudomonas aeruginosa. J Clin Microbiol 2004, 42:5644-5649. # Haubold B, Rainey PB: Genetic and ecotypic structure of a fluorescent Pseudomonas population. Mol Ecol 1996, 5:747-761. # Konstantinidis KT, Tiedje JM: Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr Opin Microbiol 2007, 10:504-509. # Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM: DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007, 57:81-91. # Yamamoto S, Kasai H, Arnold DL, Jackson RW, Vivian A, Harayama S: Phylogeny of the genus Pseudomonas: intrageneric structure reconstructed from the nucleotide sequences of gyrB and rpoD genes. Microbiology 2000, 146:2385-2394. # van Passel MW, Kuramae EE, Luyf AC, Bart A, Boekhout T: The reach of the genome signature in prokaryotes. BMC Evol Biol 2006, 6:84. # Cases I, de Lorenzo V, Ouzounis CA: Transcription regulation and environmental adaptation in bacteria. Trends Microbiol 2003, 11:248-253. # Ren Q, Paulsen IT: Comparative analyses of fundamental differences in membrane transport capabilities in prokaryotes and eukaryotes. PLoS Comput Biol 2005, 1:e27. # Zhang XX, Lilley AK, Bailey MJ, Rainey PB: The indigenous Pseudomonas plasmid pQBR103 encodes plant-inducible genes, including three putative helicases. FEMS Microbiol Ecol 2004, 51:9-17. # Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FS, Hufnagle WO, Kowalik DJ, Lagrou M, Garber RL, Goltry L, Tolentino E, Westbrock-Wadman S, Yuan Y, Brody LL, Coulter SN, Folger KR, Kas A, Larbig K, Lim R, Smith K, Spencer D, Wong GK, Wu Z, Paulsen IT, Reizer J, Saier MH, Hancock RE, Lory S, Olson MV: Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 2000, 406:959-964. # Silby MW, Rainey PB, Levy SB: IVET experiments in Pseudomonas fluorescens reveal cryptic promoters at loci associated with recognizable overlapping genes. Microbiology 2004, 150:518-520. # Silby MW, Levy SB: Overlapping protein-encoding genes in Pseudomonas fluorescens Pf0-1. PLoS Genet 2008, 4:e1000094. # Parkhill J, Wren BW, Thomson NR, Titball RW, Holden MT, Prentice MB, Sebaihia M, James KD, Churcher C, Mungall KL, Baker S, Basham D, Bentley SD, Brooks K, Cerdeño-Tárraga AM, Chillingworth T, Cronin A, Davies RM, Davis P, Dougan G, Feltwell T, Hamlin N, Holroyd S, Jagels K, Karlyshev AV, Leather S, Moule S, Oyston PC, Quail M, Rutherford K, et al.: Genome sequence of Yersinia pestis, the causative agent of plague. Nature 2001, 413:523-527. # Parkhill J, Sebaihia M, Preston A, Murphy LD, Thomson N, Harris DE, Holden MT, Churcher CM, Bentley SD, Mungall KL, Cerdeño-Tárraga AM, Temple L, James K, Harris B, Quail MA, Achtman M, Atkin R, Baker S, Basham D, Bason N, Cherevach I, Chillingworth T, Collins M, Cronin A, Davis P, Doggett J, Feltwell T, Goble A, Hamlin N, Hauser H, et al.: Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 2003, 35:32-40. # Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, Brownlie JC, McGraw EA, Martin W, Esser C, Ahmadinejad N, Wiegand C, Madupu R, Beanan MJ, Brinkac LM, Daugherty SC, Durkin AS, Kolonay JF, Nelson WC, Mohamoud Y, Lee P, Berry K, Young MB, Utterback T, Weidman J, Nierman WC, Paulsen IT, Nelson KE, Tettelin H, O'Neill SL, Eisen JA: Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2004, 2:E69. # Delihas N: Small mobile sequences in bacteria display diverse structure/function motifs. Mol Microbiol 2008, 67:475-481. # Aranda-Olmedo I, Tobes R, Manzanera M, Ramos JL, Marques S: Species-specific repetitive extragenic palindromic (REP) sequences in Pseudomonas putida. Nucleic Acids Res 2002, 30:1826-1833. # Jordan IK, Rogozin IB, Wolf YI, Koonin EV: Essential genes are more evolutionarily conserved than are nonessential genes in bacteria. Genome Res 2002, 12:962-968. # Shakhnovich BE, Koonin EV: Origins and impact of constraints in evolution of gene families. Genome Res 2006, 16:1529-1536. # Spiers AJ, Bohannon J, Gehrig SM, Rainey PB: Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol Microbiol 2003, 50:15-27. # Spiers AJ, Kahn SG, Bohannon J, Travisano M, Rainey PB: Adaptive divergence in experimental populations of Pseudomonas fluorescens. I. Genetic and phenotypic bases of wrinkly spreader fitness. Genetics 2002, 161:33-46. # Lawrence JG, Ochman H: Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci USA 1998, 95:9413-9417. # Mavrodi DV, Loper JE, Paulsen IT, Thomashow LS: Mobile genetic elements in the genome of the beneficial rhizobacterium Pseudomonas fluorescens Pf-5. BMC Microbiol 2009, 9:8. # El-Sayed AK, Hothersall J, Cooper SM, Stephens E, Simpson TJ, Thomas CM: Characterization of the mupirocin biosynthesis gene cluster from Pseudomonas fluorescens NCIMB 10586. Chem Biol 2003, 10:419-430. # Burrus V, Waldor MK: Shaping bacterial genomes with integrative and conjugative elements. Res Microbiol 2004, 155:376-386. # Pitman AR, Jackson RW, Mansfield JW, Kaitell V, Thwaites R, Arnold DL: Exposure to host resistance mechanisms drives evolution of bacterial virulence in plants. Curr Biol 2005, 15:2230-2235. # Collyn F, Billault A, Mullet C, Simonet M, Marceau M: YAPI, a new Yersinia pseudotuberculosis pathogenicity island. Infect Immun 2004, 72:4784-4790. # Thomson NR, Howard S, Wren BW, Holden MT, Crossman L, Challis GL, Churcher C, Mungall K, Brooks K, Chillingworth T, Feltwell T, Abdellah Z, Hauser H, Jagels K, Maddison M, Moule S, Sanders M, Whitehead S, Quail MA, Dougan G, Parkhill J, Prentice MB: The complete genome sequence and comparative genome analysis of the high pathogenicity Yersinia enterocolitica strain 8081. PLoS Genet 2006, 2:e206. # Pickard D, Wain J, Baker S, Line A, Chohan S, Fookes M, Barron A, Gaora PO, Chabalgoity JA, Thanky N, Scholes C, Thomson N, Quail M, Parkhill J, Dougan G: Composition, acquisition, and distribution of the Vi exopolysaccharide-encoding Salmonella enterica pathogenicity island SPI-7. J Bacteriol 2003, 185:5055-5065. # Stanier RY, Palleroni NJ, Doudoroff M: The aerobic pseudomonads: a taxonomic study. J Gen Microbiol 1966, 43:159-271. # Rainey PB, Bailey MJ, Thompson IP: Phenotypic and genotypic diversity of fluorescent pseudomonads isolated from field-grown sugar beet. Microbiology 1994, 140:2315-2331. # Ravel J, Cornelis P: Genomics of pyoverdine-mediated iron uptake in pseudomonads. Trends Microbiol 2003, 11:195-200. # Parkhill J, Achtman M, James KD, Bentley SD, Churcher C, Klee SR, Morelli G, Basham D, Brown D, Chillingworth T, Davies RM, Davis P, Devlin K, Feltwell T, Hamlin N, Holroyd S, Jagels K, Leather S, Moule S, Mungall K, Quail MA, Rajandream MA, Rutherford KM, Simmonds M, Skelton J, Whitehead S, Spratt BG, Barrell BG: Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature 2000, 404:502-506. # Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B: Artemis: sequence visualization and annotation. Bioinformatics 2000, 16:944-945. # Pierce E, Xie G, Barabote RD, Saunders E, Han CS, Detter JC, Richardson P, Brettin TS, Das A, Ljungdahl LG, Ragsdale SW: The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum). Environ Microbiol 2008, 10:2550-2573. # Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J: ACT: the Artemis Comparison Tool. Bioinformatics 2005, 21:3422-3423. # Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J: DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 2009, 25:119-120. # Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797. # Castresana J: Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000, 17:540-552. # Stamatakis A: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690. # Price AL, Jones NC, Pevzner PA: De novo identification of repeat families in large genomes. Bioinformatics 2005, 21(Suppl 1):i351-358. # Higgins DG, Sharp PM: CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 1988, 73:237-244. # Clamp M, Cuff J, Searle SM, Barton GJ: The Jalview Java alignment editor. Bioinformatics 2004, 20:426-427. # Schuster-Bockler B, Schultz J, Rahmann S: HMM Logos for visualization of protein families. BMC Bioinformatics 2004, 5:7. # Vernikos GS, Parkhill J: Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 2006, 22:2196-2203. # Rainey PB, Heithoff DM, Mahan MJ: Single-step conjugative cloning of bacterial gene fusions involved in microbe-host interactions. Mol Gen Genet 1997, 256:84-87.
URI:	http://wrap.warwick.ac.uk/id/eprint/2214

Data sourced from Thomson Reuters' Web of Knowledge

Request changes to a record

Actions (login required)

View Item