J.M. Raaijmakers

Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, Gelderland, Netherlands

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Publications (177)398.28 Total impact

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    ABSTRACT: Lipopeptides (LP) are structurally diverse compounds with potent surfactant and broad-spectrum antibiotic activities. In Pseudomonas and other bacterial genera, LP biosynthesis is governed by large multimodular nonribosomal peptide synthetases (NRPS). To date, relatively little is known about the regulatory genetic network of LP biosynthesis. This study provides evidence that the chaperone ClpA, together with the serine protease ClpP, regulates the biosynthesis of the LP massetolide in Pseudomonas fluorescens SS101. Whole-genome transcriptome analyses of clpA and clpP mutants showed their involvement in the transcription of the NRPS genes massABC and the transcriptional regulator massAR. In addition, transcription of genes associated with cell wall and membrane biogenesis, energy production and conversion, amino acid transport and metabolism, and pilus assembly were altered by mutations in clpA and clpP. Proteome analysis allowed the identification of additional cellular changes associated to clpA and clpP mutations. The expression of proteins of the citrate cycle and the heat shock proteins DnaK and DnaJ were particularly affected. Combined with previous findings, these results suggest that the ClpAP complex regulates massetolide biosynthesis via the pathway-specific, LuxR-type regulator MassAR, the heat shock proteins DnaK and DnaJ, and proteins of the TCA cycle. Combining transcriptome and proteome analyses provided new insights into the regulation of LP biosynthesis in P. fluorescens and led to the identification of specific missing links in the regulatory pathways.
    BMC Microbiology 12/2015; 15(1):367. DOI:10.1186/s12866-015-0367-y · 2.98 Impact Factor
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    ABSTRACT: Volatile organic compounds (VOCs) from plant growth-promoting rhizobacteria (PGPR) play key roles in modulating plant growth and induced systemic resistance (ISR) to pathogens. Despite their significance, the physiological functions of the specific VOCs produced by Pseudomonas fluorescens SS101 (Pf.SS101) have not been precisely elucidated. The effects of Pf.SS101 and its VOCs on augmentation of plant growth promotion were investigated in vitro and in planta. Significant growth promotion was observed in plants exposed Pf.SS101 under both conditions, suggesting its VOCs play a key role in promoting plant growth. Solid-phase micro-extraction (SPME) and a gas chromatography-mass spectrophotometer (GC-MS) system were used to characterize the VOCs emitted by Pf.SS101 and 11 different compounds were detected in samples inoculated this bacterium, including 13-Tetradecadien-1-ol, 2-butanone and 2-Methyl-n-1-tridecene. Application of these compounds resulted in enhanced plant growth. This study suggests that Pf.SS101 promotes the growth of plants via the release of VOCs including 13-Tetradecadien-1-ol, 2-butanone and 2-Methyl-n-1-tridecene, thus increasing understanding of the role of VOCs in plant-bacterial inter-communication. Copyright © 2015. Published by Elsevier Inc.
    Biochemical and Biophysical Research Communications 04/2015; 461(2). DOI:10.1016/j.bbrc.2015.04.039 · 2.28 Impact Factor
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    ABSTRACT: Endophytic Pseudomonas poae strain RE*1-1-14 was originally isolated from internal root tissue of sugar beet plants and shown to suppress growth of the fungal pathogen Rhizoctonia solani both in vitro and in the field. To identify genes involved in its biocontrol activity, RE*1-1-14 random mutagenesis and sequencing led to the identification of a nonribosomal peptide synthetase (NRPS) gene cluster predicted to encode a lipopeptide (LP) with a 10-amino acid peptide moiety. The two unlinked gene clusters consisted of three NRPS genes, designated poaA (cluster 1), and poaB and poaC (cluster 2), spanning approximately 33.7 kb. In silico analysis followed by chemical analyses revealed that the encoded LP designated poaeamide, is a structurally new member of the orfamide family. Poaeamide inhibited mycelial growth of R. solani and different oomycetes including Phytophthora capsici, Ph. infestans, and Pythium ultimum. The novel LP was shown to be essential for swarming motility of strain RE*1-1-14 and had an impact on root colonization of sugar beet seedlings The poaeamide-deficient mutant colonized the rhizosphere and upper plant cortex at higher densities and with more scattered colonization patterns than the wildtype. Collectively these results indicate that P. poae RE*1-1-14 produces a structurally new LP that is relevant for its antagonistic activity against soil-borne plant pathogens and for colonization of sugar beet roots.
    Molecular Plant-Microbe Interactions 03/2015; DOI:10.1094/MPMI-12-14-0406-R · 4.46 Impact Factor
  • Rodrigo Mendes, Jos M Raaijmakers
    The ISME Journal 02/2015; DOI:10.1038/ismej.2015.7 · 9.27 Impact Factor
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    ABSTRACT: The rhizobacterium Pseudomonas fluorescens SS101 inhibits growth of oomycete and fungal pathogens, and induces resistance in plants against pathogens and insects. To unravel regulatory pathways of secondary metabolite production in SS101, we conducted a genome-wide search for sRNAs and performed transcriptomic analyses to identify genes associated with the Rsm (repressor of secondary metabolites) regulon. In silico analysis led to the identification of 16 putative sRNAs in the SS101 genome. In frame deletion of the sRNAs rsmY and rsmZ showed that the Rsm system regulates the biosynthesis of the lipopeptide massetolide A and involves the two repressor proteins RsmA and RsmE, with the LuxR-type transcriptional regulator MassAR as their most likely target. Transcriptome analyses of the rsmYZ mutant further revealed that genes associated with iron acquisition, motility and chemotaxis were significantly upregulated, whereas genes of the type VI secretion system were downregulated. Comparative transcriptomic analyses showed that most, but not all, of the genes controlled by RsmY/RsmZ are also controlled by the GacS/GacA two-component system. We conclude that the Rsm regulon of P. fluorescens SS101 plays a critical role in the regulation of lipopeptide biosynthesis and controls the expression of other genes involved in motility, competition and survival in the plant rhizosphere. © 2014 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology.
    Microbial Biotechnology 12/2014; 8(2). DOI:10.1111/1751-7915.12190 · 3.02 Impact Factor
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    ABSTRACT: Certain bacterial species produce antimicrobial compounds only in the presence of a competing species. However little is known on the frequency of interaction-mediated induction of antibiotic compound production in natural communities of soil bacteria. Here we developed a high-throughput method to screen for the production of antimicrobial activity by monocultures and pair-wise combinations of 146 phylogenetically different bacteria isolated from similar soil habitats. Growth responses of two human pathogenic model organisms, Escherichia coli WA321 and Staphylococcus aureus 533R4, were used to monitor antimicrobial activity. From all isolates, 33% showed antimicrobial activity only in monoculture and 42% showed activity only when tested in interactions. More bacterial isolates were active against S. aureus than against E. coli. The frequency of interaction-mediated induction of antimicrobial activity was 6% (154 interactions out of 2798) indicating that only a limited set of species combinations showed such activity. The screening revealed also interaction-mediated suppression of antimicrobial activity for 22% of all combinations tested. Whereas all patterns of antimicrobial activity (non-induced production, induced production and suppression) were seen for various bacterial classes, interaction-mediated induction of antimicrobial activity was more frequent for combinations of Flavobacteria and alpha- Proteobacteria. The results of our study give a first indication on the frequency of interference competitive interactions in natural soil bacterial communities which may forms a basis for selection of bacterial groups that are promising for the discovery of novel, cryptic antibiotics.
    Frontiers in Microbiology 10/2014; 5(567). DOI:10.3389/fmicb.2014.00567t · 3.94 Impact Factor
  • Xu Cheng, Menno van der Voort, Jos M. Raaijmakers
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    ABSTRACT: In Pseudomonas species, production of secondary metabolites and exoenzymes is regulated by the GacS/GacA two-component regulatory system. In P. fluorescens SBW25, mutations in the Gac-system cause major transcriptional changes and abolished production of the lipopeptide viscosin and of an exoprotease. In contrast to many other Pseudomonas species and strains, inactivation of the Gac-system in strain SBW25 significantly enhanced its antimicrobial activities against oomycete, fungal and bacterial pathogens. Here, random plasposon mutagenesis of the gacS mutant led to the identification of seven mutants with reduced or loss of antimicrobial activity. In four mutants, the plasposon insertion was located in genes of the pyrroloquinoline quinone (PQQ) biosynthesis pathway. Genetic complementation, ectopic expression, activity bioassays and RP-HPLC analyses revealed that a gacS mutation in SBW25 leads to enhanced expression of pqq genes, resulting in an increase in gluconic and 2-ketogluconic acid production, which in turn acidified the extracellular medium to levels that inhibit growth of other microorganisms. We also showed that PQQ-mediated acidification comes with a growth penalty for the gacS mutant in the stationary phase. In conclusion, PQQ-mediated acidification compensates for the loss of several antimicrobial traits in P. fluorescens SBW25 and may help gac mutants to withstand competitors.
    Environmental Microbiology Reports 10/2014; 7(1). DOI:10.1111/1758-2229.12231 · 3.26 Impact Factor
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    ABSTRACT: Habitat bioaugmentation and introduction of protective microbiota have been proposed as potential conservation strategies to rescue endangered mammals and amphibians from emerging diseases. For both strategies, insight into the microbiomes of the endangered species and their habitats is essential. Here, we sampled nests of the endangered sea turtle species Eretmochelys imbricata that were infected with the fungal pathogen Fusarium falciforme. Metagenomic analysis of the bacterial communities associated with the shells of the sea turtle eggs revealed approximately 16,664 operational taxonomic units, with Proteobacteria, Actinobacteria, Firmicutes and Bacteroidetes as the most dominant phyla. Subsequent isolation of Actinobacteria from the eggshells led to the identification of several genera (Streptomyces, Amycolaptosis, Micromomospora Plantactinospora and Solwaraspora) that inhibit hyphal growth of the pathogen F. falciforme. These bacterial genera constitute a first set of microbial indicators to evaluate the potential role of microbiota in conservation of endangered sea turtle species.
    PLoS ONE 04/2014; 9(4):e95206. DOI:10.1371/journal.pone.0095206 · 3.53 Impact Factor
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    ABSTRACT: Animals and plants are increasingly suffering from diseases caused by fungi and oomycetes. These emerging pathogens are now recognized as a global threat to biodiversity and food security. Among oomycetes, Saprolegnia species cause significant declines in fish and amphibian populations. Fish eggs have an immature adaptive immune system and depend on nonspecific innate defences to ward off pathogens. Here, meta-taxonomic analyses revealed that Atlantic salmon eggs are home to diverse fungal, oomycete and bacterial communities. Although virulent Saprolegnia isolates were found in all salmon egg samples, a low incidence of Saprolegniosis was strongly correlated with a high richness and abundance of specific commensal Actinobacteria, with the genus Frondihabitans (Microbacteriaceae) effectively inhibiting attachment of Saprolegniato salmon eggs. These results highlight that fundamental insights into microbial landscapes of fish eggs may provide new sustainable means to mitigate emerging diseases.The ISME Journal advance online publication, 27 March 2014; doi:10.1038/ismej.2014.44.
    The ISME Journal 03/2014; 8(10). DOI:10.1038/ismej.2014.44 · 9.27 Impact Factor
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    ABSTRACT: The antifungal activity of bacteria from the genus Collimonas has been well documented, but the chemistry and gene functions that underlie this phenotype are still poorly understood. Screening of a random plasposon insertion library of Collimonas fungivorans Ter331 for loss-of-function mutants revealed the importance of gene cluster K, which is annotated to code for the biosynthesis of a secondary metabolite and which features genes for fatty acid desaturases and polyketide synthases. Mutants in gene cluster K had lost the ability to inhibit hyphal growth of the fungus Aspergillus niger and were no longer able to produce and secrete several metabolites that after extraction and partial purification from wildtype strain Ter331 were shown to share a putative ene-triyne moiety. Some but not all of these metabolites were able to inhibit growth of A. niger, indicating functional variation within this group of Collimonas-produced polyyne-like 'collimomycins'. PCR analysis of isolates representing different Collimonas species indicated that the possession of cluster K genes correlated positively with antifungal ability, further strengthening the notion that this cluster is involved in collimomycin production. We discuss our findings in the context of other bacterially produced polyynes and the potential use of collimomycins for the control of harmful fungi.
    Environmental Microbiology 03/2014; 16(5). DOI:10.1111/1462-2920.12440 · 6.24 Impact Factor
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    ABSTRACT: The antimetabolite mangotoxin is a key factor in virulence of Pseudomonas syringae pv. syringae strains which cause apical necrosis of mango trees. Previous studies showed that mangotoxin biosynthesis is governed by the mbo operon. Random mutagenesis led to the identification of two other gene clusters that affect mangotoxin biosynthesis. These are the gacS/gacA genes and mgo operon which harbors the four genes mgoBCAD. The current study shows that disruption of the nonribosomal peptide synthetase (NRPS) gene mgoA resulted in loss of mangotoxin production and reduced virulence on tomato leaves. Transcriptional analyses by qPCR and promoter reporter fusions revealed that mbo expression is regulated by both gacS/gacA and mgo genes. Also, expression of the mgo operon was shown to be regulated by gacS/gacA. Heterologous expression under the native promoter of the mbo operon resulted in mangotoxin production in non-producing P. syringae strains, but not in other Pseudomonas species. Also introduction of the mbo and mgo operons in nonproducing P. protegens Pf-5 did not confer mangotoxin production but did enhance transcription of the mbo promoter. From the data obtained in this study, we conclude that both mbo and mgo operons are under the control of the gacS/gacA two-component system and that the MgoA product acts as a positive regulator of mangotoxin biosynthesis.
    BMC Microbiology 02/2014; 14(1):46. DOI:10.1186/1471-2180-14-46 · 2.98 Impact Factor
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    ABSTRACT: Pseudomonas fluorescens SS101 produces the cyclic lipopeptide massetolide with diverse functions in antimicrobial activity, motility and biofilm formation. To understand how massetolide biosynthesis is genetically regulated in SS101, approximately 8,000 random plasposon mutants were screened for reduced or loss of massetolide production. Out of a total of 58 putative mutants, 45 had a mutation in one of the three massetolide biosynthesis genes massA, massB or massC. For 5 mutants, the insertions were located in the known regulatory genes gacS, gacA, and clpP. For the remaining 8 mutants, insertions were located in clpA, encoding the ClpP chaperone, in phgdh, encoding D-3-phosphoglycerate dehydrogenase, in the heat shock protein encoding dnaK, or in the transmembrane regulatory gene prtR. Genetic, chemical and phenotypic analyses showed that phgdh, dnaK and prtR are indeed involved in the regulation of massetolide biosynthesis, most likely by transcriptional repression of the LuxR-type regulator genes massAR and massBCR. In addition to their role in massetolide biosynthesis, dnaK and prtR were found to affect siderophore and extracellular protease(s) production, respectively. The identification of new regulatory genes substantially extended insights into the signal transduction pathways of lipopeptide biosynthesis in P. fluorescens and into regulation of other traits that may contribute to its life-style in the rhizosphere. This article is protected by copyright. All rights reserved.
    FEMS Microbiology Letters 02/2014; 356(2). DOI:10.1111/1574-6968.12404 · 2.72 Impact Factor
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    ABSTRACT: Within the framework of our genome-based program to discover new antibiotic lipopeptides from Pseudomonads, brabantamides A-C were isolated from plant-associated Pseudomonas sp. SH-C52. Brabantamides A-C displayed moderate to high in vitro activities against Gram-positive bacterial pathogens. Their shared structure is unique in that they contain a 5,5-bicyclic carbamate scaffold. Here, the biosynthesis of brabantamide A (SB-253514) was studied by a combination of bioinformatics, feeding experiments with isotopically labelled precursors and in vivo and in vitro functional analysis of enzymes encoded in the biosynthetic pathway. The studies resulted in the deduction of all biosynthetic building blocks of brabantamide A and revealed an unusual feature of this metabolite: its biosynthesis occurs via an initially formed linear di-lipopeptide that is subsequently rearranged by a novel FAD-dependent Baeyer-Villiger monooxygenase.
    ChemBioChem 01/2014; 15(2). DOI:10.1002/cbic.201300527 · 3.06 Impact Factor
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    ABSTRACT: The rhizosphere is the interface between plant roots and soil where interactions among a myriad of microorganisms and invertebrates affect biogeochemical cycling, plant growth and tolerance to biotic and abiotic stress. The rhizosphere is intriguingly complex and dynamic, and understanding its ecology and evolution is key to enhancing plant productivity and ecosystem functioning. Novel insights into key factors and evolutionary processes shaping the rhizosphere microbiome will greatly benefit from integrating reductionist and systems-based approaches in both agricultural and natural ecosystems. Here, we discuss recent developments in rhizosphere research in relation to assessing the contribution of the micro- and macroflora to sustainable agriculture, nature conservation, the development of bio-energy crops and the mitigation of climate change.
    Nature Reviews Microbiology 09/2013; 11(11). DOI:10.1038/nrmicro3109 · 23.32 Impact Factor
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    ABSTRACT: Transcriptome analysis of Pseudomonas fluorescens SBW25 showed that 702 genes were differentially regulated in a gacS::Tn5 mutant, with 300 and 402 genes up- and downregulated respectively. Similar to the Gac regulon of other Pseudomonas species, genes involved in motility, biofilm formation, siderophore biosynthesis and oxidative stress were differentially regulated in the gacS mutant of SBW25. Our analysis also revealed, for the first time, that transcription of 19 rhizosphere-induced genes and of genes involved in type II secretion, (exo)polysaccharide and pectate lyase biosynthesis, twitching motility and an orphan non-ribosomal peptide synthetase (NRPS) were significantly affected in the gacS mutant. Furthermore, the gacS mutant inhibited growth of oomycete, fungal and bacterial pathogens significantly more than wild type SBW25. Since RP-HPLC analysis did not reveal any potential candidate metabolites, we focused on the Gac-regulated orphan NRPS gene cluster that was predicted to encode an eight-amino-acid ornicorrugatin-like peptide. Site-directed mutagenesis indicated that the encoded peptide is not involved in the enhanced antimicrobial activity of the gacS mutant but may function as a siderophore. Collectively, this genome-wide analysis revealed that a mutation in the GacS/A two-component regulatory system causes major transcriptional changes in SBW25 and significantly enhances its antimicrobial activities by yet unknown mechanisms.
    Environmental Microbiology Reports 08/2013; 5(4):608-19. DOI:10.1111/1758-2229.12061 · 3.26 Impact Factor
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    Rodrigo Mendes, Paolina Garbeva, Jos M Raaijmakers
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    ABSTRACT: Microbial communities play a pivotal role in the functioning of plants by influencing their physiology and development. While many members of the rhizosphere microbiome are beneficial to plant growth, also plant pathogenic microorganisms colonize the rhizosphere striving to break through the protective microbial shield and to overcome the innate plant defense mechanisms in order to cause disease. A third group of microorganisms that can be found in the rhizosphere are the true and opportunistic human pathogenic bacteria, which can be carried on or in plant tissue and may cause disease when introduced into debilitated humans. Although the importance of the rhizosphere microbiome for plant growth has been widely recognized, for the vast majority of rhizosphere microorganisms no knowledge exists. To enhance plant growth and health, it is essential to know who is present in the rhizosphere microbiome and what they are doing. Here, we review the main functions of rhizosphere microorganisms and how they impact on health and disease. We discuss the mechanisms involved in the multitrophic interactions and chemical dialogues that occur in the rhizosphere. Finally, we highlight several strategies to re-direct or re-shape the rhizosphere microbiome in favour of microbes that are beneficial to plant growth and health. This article is protected by copyright. All rights reserved.
    FEMS microbiology reviews 06/2013; 37(5). DOI:10.1111/1574-6976.12028 · 13.81 Impact Factor
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    ABSTRACT: Endophytic Pseudomonas aeruginosa strain BP35 was originally isolated from black pepper grown in the rain forest in Kerala, India. Strain PaBP35 was shown to provide significant protection to black pepper against infections by Phytophthora capsici and Radopholus similis. For registration and implementation in disease management programmes, several traits of PaBP35 were investigated including its endophytic behaviour, biocontrol activity, phylogeny and toxicity to mammals. The results showed that PaBP35 efficiently colonized black pepper shoots and displayed a typical spatiotemporal pattern in its endophytic movement with concomitant suppression of Phytophthora rot. Confocal laser scanning microscopy revealed high populations of PaBP35::gfp2 inside tomato plantlets, supporting its endophytic behaviour in other plant species. Polyphasic approaches to genotype PaBP35, including BOX-PCR, recN sequence analysis, multilocus sequence typing and comparative genome hybridization analysis, revealed its uniqueness among P. aeruginosa strains representing clinical habitats. However, like other P. aeruginosa strains, PaBP35 exhibited resistance to antibiotics, grew at 25-41°C and produced rhamnolipids and phenazines. PaBP35 displayed strong type II secretion effectors-mediated cytotoxicity on mammalian A549 cells. Coupled with pathogenicity in a murine airway infection model, we conclude that this plant endophytic strain is as virulent as clinical P. aeruginosa strains. Safety issues related to the selection of plant endophytic bacteria for crop protection are discussed.
    Environmental Microbiology 10/2012; 15(3). DOI:10.1111/1462-2920.12031 · 6.24 Impact Factor
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    ABSTRACT: Systemic resistance induced in plants by non-pathogenic rhizobacteria is typically effective against multiple pathogens. Here, we show that root-colonizing Pseudomonas fluorescens strain SS101 (Pf.SS101) enhanced resistance in Arabidopsis against several bacterial pathogens, including Pseudomonas syringae pv. tomato (Pst), and the insect pest Spodoptera exigua. Transcriptomic analysis and bioassays with specific Arabidopsis mutants revealed that, unlike many other rhizobacteria, the Pf.SS101-induced resistance response to Pst is dependent on salicylic acid (SA) signaling and not on jasmonic acid (JA) and ethylene (ET) signaling. Genome-wide transcriptomic and untargeted metabolomic analyses showed that in roots and leaves of Arabidopsis plants treated with Pf.SS101, approximately 1910 genes and 50 metabolites were differentially regulated relative to untreated plants. Integration of both sets of 'omics data pointed to a prominent role of camalexin and glucosinolates in the Pf.SS101-induced resistance response. Subsequent bioassays with seven Arabidopsis mutants (myb51, cyp79B2cyp79B3, cyp81F2, pen2, cyp71A12, cyp71A13 and myb28myb29) disrupted in the biosynthesis pathways for these plant secondary metabolites showed that camalexin and glucosinolates are indeed required for the induction of Pst-resistance by Pf.SS101. Also for the insect S. exigua, the indolic glucosinolates appeared to play a role in the Pf.SS101-induced resistance response. This study provides, for the first time, insight into the substantial biochemical and temporal transcriptional changes in Arabidopsis associated with the SA-dependent resistance response induced by specific rhizobacteria.
    Plant physiology 10/2012; DOI:10.1104/pp.112.207324 · 7.39 Impact Factor
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    ABSTRACT: We provide here a comparative genome analysis of ten strains within the Pseudomonas fluorescens group including seven new genomic sequences. These strains exhibit a diverse spectrum of traits involved in biological control and other multitrophic interactions with plants, microbes, and insects. Multilocus sequence analysis placed the strains in three sub-clades, which was reinforced by high levels of synteny, size of core genomes, and relatedness of orthologous genes between strains within a sub-clade. The heterogeneity of the P. fluorescens group was reflected in the large size of its pan-genome, which makes up approximately 54% of the pan-genome of the genus as a whole, and a core genome representing only 45-52% of the genome of any individual strain. We discovered genes for traits that were not known previously in the strains, including genes for the biosynthesis of the siderophores achromobactin and pseudomonine and the antibiotic 2-hexyl-5-propyl-alkylresorcinol; novel bacteriocins; type II, III, and VI secretion systems; and insect toxins. Certain gene clusters, such as those for two type III secretion systems, are present only in specific sub-clades, suggesting vertical inheritance. Almost all of the genes associated with multitrophic interactions map to genomic regions present in only a subset of the strains or unique to a specific strain. To explore the evolutionary origin of these genes, we mapped their distributions relative to the locations of mobile genetic elements and repetitive extragenic palindromic (REP) elements in each genome. The mobile genetic elements and many strain-specific genes fall into regions devoid of REP elements (i.e., REP deserts) and regions displaying atypical tri-nucleotide composition, possibly indicating relatively recent acquisition of these loci. Collectively, the results of this study highlight the enormous heterogeneity of the P. fluorescens group and the importance of the variable genome in tailoring individual strains to their specific lifestyles and functional repertoire.
    PLoS Genetics 07/2012; 8(7):e1002784. DOI:10.1371/journal.pgen.1002784 · 8.17 Impact Factor

Publication Stats

5k Citations
398.28 Total Impact Points

Institutions

  • 2015
    • Netherlands Institute of Ecology (NIOO-KNAW)
      Wageningen, Gelderland, Netherlands
  • 2002–2014
    • Wageningen University
      • Department of Phytopathology
      Wageningen, Gelderland, Netherlands
  • 2009
    • Sonoma State University
      • Department of Biology
      Ронърт Парк, California, United States
  • 2007
    • University of São Paulo
      • Departamento de Genética (LGN) (ESALQ)
      San Paulo, São Paulo, Brazil
  • 2003
    • University of Burgundy
      Dijon, Bourgogne, France
  • 2001
    • Washington State University
      • Department of Plant Pathology
      Pullman, WA, United States
  • 1994–1995
    • Utrecht University
      Utrecht, Utrecht, Netherlands