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Efficient Rhizosphere Colonization by Pseudomonas Fluorescens F113

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Efficient Rhizosphere Colonization by Pseudomonas Fluorescens F113 Environmental Microbiology (2010) 12(12), 3185–3195 doi:10.1111/j.1462-2920.2010.02291.x Efficient rhizosphere colonization by Pseudomonas fluorescens f113 mutants unable to form biofilms on CORE Metadata, citation and similar papers at core.ac.uk Provided by Digital.CSICabiotic surfacesemi_2291 3185..3195 Emma Barahona,1† Ana Navazo,1† mucigel that seems to be plant produced. Therefore, Fátima Yousef-Coronado,2 Daniel Aguirre de Cárcer,1 the ability to form biofilms on abiotic surfaces does Francisco Martínez-Granero,1 not necessarily correlates with efficient rhizosphere Manuel Espinosa-Urgel,2 Marta Martín1 and colonization or competitive colonization. Rafael Rivilla1* 1Departamento de Biología, Universidad Autónoma de Introduction Madrid, 28049 Madrid, Spain. 2Departamento de Protección Ambiental, Estación The rhizosphere is the portion of soil that is influenced by Experimental del Zaidín, CSIC, 18008 Granada, Spain. plant roots and is characterized by harbouring a higher number of microorganisms than bulk soil (Hiltner, 1904). Numerous bacteria, generally termed rhizobacteria, are Summary adapted to this ecosystem. Rhizobacteria can affect plant Motility is a key trait for rhizosphere colonization by fitness and are also important in biotechnological applica- Pseudomonas fluorescens. Mutants with reduced tions based on integrated plant–bacteria systems. The motility are poor competitors, and hypermotile, more fluorescent pseudomonads group include several species competitive phenotypic variants are selected in the of rhizobacteria that have been used as model strains for rhizosphere. Flagellar motility is a feature associated rhizosphere colonization experiments (Lugtenberg and to planktonic, free-living single cells, and although it Dekkers, 1999; Lugtenberg et al., 2001) and for applica- is necessary for the initial steps of biofilm formation, tions such as biocontrol (Haas and Defago, 2005) and bacteria in biofilm lack flagella. To test the correlation rhizoremediation (Yee et al., 1998). Pseudomonas fluore- between biofilm formation and rhizosphere coloniza- scens F113 was isolated from the sugar-beet rhizosphere tion, we have used P. fluorescens F113 hypermotile and is able to protect plants against the oomycete derivatives and mutants affected in regulatory genes Pythium ultimum by means of the production of the fun- which in other bacteria modulate biofilm develop- gicide 2, 4-diacetylphloroglucinol (DAPG) (Shanahan ment, namely gacS (G), sadB (S) and wspR (W). et al., 1992). It has also been genetically modified for PCB Mutants affected in these three genes and a hypermo- degradation and tested in rhizoremediation experiments tile variant (V35) isolated from the rhizosphere were (Brazil et al., 1995; Villacieros et al., 2005; Aguirre de impaired in biofilm formation on abiotic surfaces, but Cárcer et al., 2007a,b). Pseudomonas fluorescens F113 colonized the alfalfa root apex as efficiently as the has been shown to colonize the rhizosphere of a variety of wild-type strain, indicating that biofilm formation on plants including pea (Naseby and Lynch, 1999), tomato abiotic surfaces and rhizosphere colonization follow (Dekkers et al., 2000), willow (Aguirre de Cárcer et al., different regulatory pathways in P. fluorescens. Fur- 2007a) and alfalfa (Villacieros et al., 2003). Colonization thermore, a triple mutant gacSsadBwspR (GSW) and studies on alfalfa have shown that this bacterium estab- V35 were more competitive than the wild-type strain lishes on the rhizoplane (root surface) forming extensive for root-tip colonization, suggesting that motility is microcolonies (Villacieros et al., 2003). This type of colo- more relevant in this environment than the ability nization pattern has also been observed for other fluores- to form biofilms on abiotic surfaces. Microscopy cent pseudomonads on tomato roots (Chin-A-Woeng showed the same root colonization pattern for P. fluo- et al., 1997). rescens F113 and all the derivatives: extensive micro- The transition between the sessile lifestyle that biofilms colonies, apparently held to the rhizoplane by a represent and a planktonic, motile lifestyle is controlled in numerous bacteria by the levels of the second messenger cyclic di-GMP. These levels are in turn regulated by the Received 10 February, 2010; accepted 25 May, 2010. *For corre- spondence. E-mail [email protected]; Tel. (+34) 914 978 188; Fax activity of proteins containing diguanilate cyclase (+34) 914 978 344. †E.B and A.N. contributed equally to this work. (GGDEF domains) and phosphodiesterase (EAL or © 2010 Society for Applied Microbiology and Blackwell Publishing Ltd 3186 E. Barahona et al. HD-GYP domains) activities (for a recent review see mutants are impaired in biofilm formation on both sur- Hengge, 2009). Low c-di-GMP levels are associated with faces, showing a substantial reduction on crystal violet a free living, motile phenotype while high c-di-GMP levels staining when compared with the wild-type strain. Double lead to biofilm formation and reduced motility. and triple mutants were also tested for biofilm formation Although flagella are required for the first steps of and an additive phenotype was observed (Fig. 1A), biofilm formation (O’Toole and Kolter, 1998a), flagella- except in the case of the double sadBgacS (SG) mutant, driven motility can be viewed as an opposing lifestyle to which shows an intermediate phenotype. However, the that of biofilms. In fact, expression of flagellar genes is additive phenotype of all other mutants, including the repressed in biofilms of P. aeruginosa or Bacillus subtilis triple gacSsadBwspR (GSW) mutant, suggests that (Lazazzera, 2005). Motility has been recognized as one of the three mutants were affected in different pathways the most important traits required for rhizosphere coloni- regulating biofilm formation. The GSW triple mutant was zation by P. fluorescens and other bacteria, since non- almost unable to form biofilms (five times reduction, as motile and non-chemotactic mutants are among the most compared with the wild-type strain) on these surfaces and impaired in competitive root colonization (de Weert et al., presented a swimming phenotype very similar to variant 2002), and a wild-type level of motility is required by P. 35 (V35) (Fig. 2A), a hypermotile phenotypic variant of fluorescens for competitive rhizosphere colonization F113 isolated from the alfalfa rhizosphere (Martinez- (Capdevila et al., 2004). The importance of motility for Granero et al., 2006). For this reason we also tested V35 rhizosphere colonization by P. fluorescens is highlighted for biofilm formation in the same systems resulting in an by the finding that the rhizosphere selects for phenotypic almost complete inability to form biofilms (five times variants (Sanchez-Contreras et al., 2002), which harbour reduction). It is interesting to note that according to this mutations in the genes encoding the two-component test, GSW and V35 are more affected in biofilm formation system GacA/GacS, and in other unidentified genes, than the non-motile, aflagellated mutant fliC (Capdevila resulting in a gradation of hypermotility phenotypes et al., 2004), a mutant affected in initial attachment (Martínez-Granero et al., 2006). because of the lack of flagella. In this work, we have used P. fluorescens F113 hyper- Biofilm formation ability of the wild-type strain and the motile phenotypic variants isolated from the rhizosphere most affected strains (V35 and the GSW mutant) was also and hypermotile mutants affected in the gacS, sadB and tested under flow conditions. Table 1 shows the param- wspR genes, which have been implicated in biofilm for- eters of the biofilms formed after 3 and 6 h by the three mation, to test its importance in root colonization and strains. Similarly to the static biofilm experiments, flow-cell competitive root colonization. biofilms formed by V35 and the triple mutant presented a more than 10 times reduction in biomass, average thick- ness and maximum thickness, compared with the wild- Results type strain, indicating again a severe defect on biofilm formation. According to these parameters, V35 was the Biofilm formation by hypermotile mutants and most affected strain, with values between 19- and phenotypic variants 49-folds lower than the wild-type strain, after 6 h. Confo- In a previous study investigating motility repressors we cal microscopy observation also showed that the wild- found that several of the hypermotile mutants isolated type strain (Fig. 1B) formed thick three-dimensional were affected in genes that had been described as impli- biofilms after 6 h. No three-dimensional structures, but cated in biofilm formation in different pseudomonads only isolated attached cells were observed for V35, while (Navazo et al., 2009). To investigate whether they had a the triple mutant attached forming small clusters of cells. similar role in P. fluorescens F113, the gacS, wspR and Differences were also evident at later time points. After sadB mutants were tested for biofilm formation on abiotic 24 h, the wild-type maintained a thicker, structured surfaces using a standard crystal violet test on two differ- biofilm, whereas V35 was the most affected strain and did ent plastic surfaces. As shown in Fig. 1A, the three not progress beyond a monolayer of cells on the surface. Fig. 1. Biofilm forming ability of P. fluorescens F113 and derivatives on abiotic surfaces. A. Static biofilm assay. Biofilms were measured as the amount of crystal violet absorbed by the biofilm formed on multi-well plates and determined by absorbance at 590 nm after de-staining
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