Publications by authors named "Yvan Moënne-Loccoz"

62 Publications

Co-occurrence of rhizobacteria with nitrogen fixation and/or 1-aminocyclopropane-1-carboxylate deamination abilities in the maize rhizosphere.

FEMS Microbiol Ecol 2020 05;96(5)

Univ Lyon, Université Claude Bernard Lyon 1, CNRS, INRAE, VetAgro Sup, UMR5557 Ecologie Microbienne, 43 bd du 11 novembre 1918, F-69622 Villeurbanne, France.

The plant microbiota may differ depending on soil type, but these microbiota probably share the same functions necessary for holobiont fitness. Thus, we tested the hypothesis that phytostimulatory microbial functional groups are likely to co-occur in the rhizosphere, using groups corresponding to nitrogen fixation (nifH) and 1-aminocyclopropane-1-carboxylate deamination (acdS), i.e. two key modes of action in plant-beneficial rhizobacteria. The analysis of three maize fields in two consecutive years showed that quantitative PCR numbers of nifH and of acdS alleles differed according to field site, but a positive correlation was found overall when comparing nifH and acdS numbers. Metabarcoding analyses in the second year indicated that the diversity level of acdS but not nifH rhizobacteria in the rhizosphere differed across fields. Furthermore, between-class analysis showed that the three sites differed from one another based on nifH or acdS sequence data (or rrs data), and the bacterial genera contributing most to field differentiation were not the same for the three bacterial groups. However, co-inertia analysis indicated that the genetic structures of both functional groups and of the whole bacterial community were similar across the three fields. Therefore, results point to co-selection of rhizobacteria harboring nitrogen fixation and/or 1-aminocyclopropane-1-carboxylate deamination abilities.
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http://dx.doi.org/10.1093/femsec/fiaa062DOI Listing
May 2020

Bacterial, archaeal and micro-eukaryotic communities characterize a disease-suppressive or conducive soil and a cultivar resistant or susceptible to common scab.

Sci Rep 2019 10 16;9(1):14883. Epub 2019 Oct 16.

Crop Research Institute, Epidemiology and Ecology of Microorganisms, Drnovská 509, 161 06, Prague 6, Czech Republic.

Control of common scab disease can be reached by resistant cultivars or suppressive soils. Both mechanisms are likely to translate into particular potato microbiome profiles, but the relative importance of each is not known. Here, microbiomes of bulk and tuberosphere soil and of potato periderm were studied in one resistant and one susceptible cultivar grown in a conducive and a suppressive field. Disease severity was suppressed similarly by both means yet, the copy numbers of txtB gene (coding for a pathogenicity determinant) were similar in both soils but higher in periderms of the susceptible cultivar from conducive soil. Illumina sequencing of 16S rRNA genes for bacteria (completed by 16S rRNA microarray approach) and archaea, and of 18S rRNA genes for micro-eukarytes showed that in bacteria, the more important was the effect of cultivar and diversity decreased from resistant cultivar to bulk soil to susceptible cultivar. The major changes occurred in proportions of Actinobacteria, Chloroflexi, and Proteobacteria. In archaea and micro-eukaryotes, differences were primarily due to the suppressive and conducive soil. The effect of soil suppressiveness × cultivar resistance depended on the microbial community considered, but differed also with respect to soil and plant nutrient contents particularly in N, S and Fe.
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http://dx.doi.org/10.1038/s41598-019-51570-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6796001PMC
October 2019

Ancient wheat varieties have a higher ability to interact with plant growth-promoting rhizobacteria.

Plant Cell Environ 2020 01 21;43(1):246-260. Epub 2019 Oct 21.

Univ Lyon, Université Claude Bernard Lyon 1, CNRS, INRA, VetAgro Sup, UMR5557 Ecologie Microbienne, F-69622 Villeurbanne, France.

Plant interactions with plant growth-promoting rhizobacteria (PGPR) are highly dependent on plant genotype. Modern plant breeding has largely sought to improve crop performance but with little focus on the optimization of plant × PGPR interactions. The interactions of the model PGPR strain Pseudomonas kilonensis F113 were therefore compared in 199 ancient and modern wheat genotypes. A reporter system, in which F113 colonization and expression of 2,4-diacetylphloroglucinol biosynthetic genes (phl) were measured on roots was used to quantify F113 × wheat interactions under gnotobiotic conditions. Thereafter, eight wheat accessions that differed in their ability to interact with F113 were inoculated with F113 and grown in greenhouse in the absence or presence of stress. F113 colonization was linked to improved stress tolerance. Moreover, F113 colonization and phl expression were higher overall on ancient genotypes than modern genotypes. F113 colonization improved wheat performance in the four genotypes that showed the highest level of phl expression compared with the four genotypes in which phl expression was lowest. Taken together, these data suggest that recent wheat breeding strategies have had a negative impact on the ability of the plants to interact with PGPR.
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http://dx.doi.org/10.1111/pce.13652DOI Listing
January 2020

Anthropization level of Lascaux Cave microbiome shown by regional-scale comparisons of pristine and anthropized caves.

Mol Ecol 2019 07 24;28(14):3383-3394. Epub 2019 Jul 24.

Université Claude Bernard Lyon 1, CNRS, INRA, VetAgro Sup, UMR5557 Ecologie Microbienne, University de Lyon, Villeurbanne, France.

Limestone areas across the world develop karstic caves, which are populated by a wide range of macro- and microorganisms. Many of these caves display Paleolithic art or outstanding speleothems, and in the last century they have been subjected to anthropization due to touristic management and intense human frequentation. Despite their cultural importance and associated conservation issues, the impact of anthropization on cave biodiversity is not known. Here, we show that anthropization is associated with specific cave biota modifications. We compared diversity in four pristine caves, four anthropized show caves, and the iconic Lascaux Cave with even stronger anthropization. The predominant microbial higher taxa were the same in all caves, but the most anthropized cave (Lascaux) was unique as it differed from the eight others by a higher proportion of Bacteroidetes bacteria and the absence of Euryarchaeota and Woesearchaeota archaea. Anthropization resulted in lower diversity and altered community structure for bacteria and archaea on cave walls, especially in Lascaux, but with a more limited effect on microeukaryotes and arthropods. Our findings fill a key gap in our understanding of the response of karstic communities to anthropization, by revealing that tourism-related anthropization impacts on the prokaryotic microbiome rather than on eukaryotic residents, and that it shapes cave biota irrespective of cave natural features.
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http://dx.doi.org/10.1111/mec.15144DOI Listing
July 2019

Genomic, phylogenetic and catabolic re-assessment of the Pseudomonas putida clade supports the delineation of Pseudomonas alloputida sp. nov., Pseudomonas inefficax sp. nov., Pseudomonas persica sp. nov., and Pseudomonas shirazica sp. nov.

Syst Appl Microbiol 2019 Jul 2;42(4):468-480. Epub 2019 May 2.

Univ. Lyon, Université Claude Bernard Lyon 1, CNRS, INRA, VetAgro Sup, UMR5557 Ecologie Microbienne, F-69622 Villeurbanne, France. Electronic address:

Bacteria of the Pseudomonas putida group are studied for a large panel of properties ranging from plant growth promotion and bioremediation to pathogenicity. To date, most of the classification of individual pseudomonads from this group relies on 16S RNA gene analysis, which is insufficient for accurate taxonomic characterization within bacterial species complexes of the Pseudomonas putida group. Here, a collection of 20 of these bacteria, isolated from various soils, was assessed via multi-locus sequence analysis of rpoD, gyrB and rrs genes. The 20 strains clustered in 7 different clades of the P. putida group. One strain per cluster was sequenced and results were compared to complete genome sequences of type strains of the P. putida group. Phylogenetic analyses, average nucleotide identity data and digital DNA hybridizations, combined to phenotypic characteristics, resulted in the proposition and description of four new species i.e. Pseudomonas alloputida Kh7 (= LMG 29756  = CFBP 8484 ) sp. nov., Pseudomonas inefficax JV551A3 (= DSM108619 = CFBP 8493 ) sp. nov., Pseudomonas persica RUB6 (= LMG 29757 = CFBP 8486 ) sp. nov. and Pseudomonas shirazica VM14 (= LMG 29953 = CFBP 8487 ) sp. nov.
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http://dx.doi.org/10.1016/j.syapm.2019.04.004DOI Listing
July 2019

Draft Genome Sequence of Plant Growth-Promoting Bacillus altitudinis Strain PAE4.

Microbiol Resour Announc 2018 Oct 4;7(13). Epub 2018 Oct 4.

CNRS, Université de Lyon, Université Claude Bernard Lyon 1, INRA, VetAgro Sup, UMR 5557 Ecologie Microbienne, Villeurbanne, France.

We report here the draft genome of Bacillus altitudinis strain PAE4, a thermophilic plant growth-promoting rhizobacterium isolated from the coastal ridge of the Mediterranean Sea in Egypt. Besides heat shock protein genes, several genes encoding phytobeneficial properties were identified.
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http://dx.doi.org/10.1128/MRA.00962-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6256563PMC
October 2018

Rock substrate rather than black stain alterations drives microbial community structure in the passage of Lascaux Cave.

Microbiome 2018 12 5;6(1):216. Epub 2018 Dec 5.

Univ Lyon, Université Claude Bernard Lyon 1, CNRS, INRA, VetAgro Sup, UMR5557/1418 Ecologie Microbienne, 69622, Villeurbanne, France.

Background: The World-famous UNESCO heritage from the Paleolithic human society, Lascaux Cave (France), has endeavored intense microclimatic perturbations, in part due to high touristic pressure. These perturbations have resulted in numerous disturbances of the cave ecosystem, including on its microbial compartment, which resulted in the formation of black stains especially on the rock faces of the passage. We investigated the cave microbiome in this part of Lascaux by sampling three mineral substrates (soil, banks, and inclined planes) on and outside stains to assess current cave microbial assemblage and explore the possibility that pigmented microorganisms involved in stain development occur as microbial consortia.

Methods: Microbial abundance and diversity were assessed by means of quantitative PCR and high-throughput sequencing (Illumina MiSeq) of several DNA and cDNA taxonomic markers. Five sampling campaigns were carried out during winter and summer to embrace potential seasonal effect in this somewhat stable environment (based on measurements of temperature and CO concentration).

Results: While the season or type of mineral substrate did not affect the abundances of bacteria and micro-eukaryotes on or outside stains, mineral substrate rather than stain presence appears to be the most significant factor determining microbial diversity and structuring microbial community, regardless of whether DNA or cDNA markers were considered. A phylogenetic signal was also detected in relation to substrate types, presence of stains but not with season among the OTUs common to the three substrates. Co-occurrence network analyses showed that most bacterial and fungal interactions were positive regardless of the factor tested (season, substrate, or stain), but these networks varied according to ecological conditions and time. Microorganisms known to harbor pigmentation ability were well established inside but also outside black stains, which may be prerequisite for subsequent stain formation.

Conclusions: This first high throughput sequencing performed in Lascaux Cave showed that black stains were secondary to mineral substrate in determining microbiome community structure, regardless of whether total or transcriptionally active bacterial and micro-eukaryotic communities were considered. These results revealed the potential for new stain formation and highlight the need for careful microbiome management to avoid further cave wall degradation.
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http://dx.doi.org/10.1186/s40168-018-0599-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6282324PMC
December 2018

1-Aminocyclopropane-1-carboxylate deaminase producers associated to maize and other Poaceae species.

Microbiome 2018 06 20;6(1):114. Epub 2018 Jun 20.

Univ Lyon, Université Claude Bernard Lyon 1, CNRS, INRA, VetAgro Sup, UMR5557 Ecologie Microbienne, F-69622, Villeurbanne, France.

Background: Complex plant-microbe interactions have been established throughout evolutionary time, many of them with beneficial effects on the host in terms of plant growth, nutrition, or health. Some of the corresponding modes of action involve a modulation of plant hormonal balance, such as the deamination of the ethylene precursor 1-aminocyclopropane-1-carboxylate (ACC). Despite its ecological importance, our understanding of ACC deamination is impaired by a lack of direct molecular tools. Here, we developed PCR primers to quantify the ACC deaminase gene acdS and its mRNA in soil communities and assessed acdS microorganisms colonizing maize and other Poaceae species.

Results: Effective acdS primers suitable for soil microbial communities were obtained, enabling recovery of bona fida acdS genes and transcripts of diverse genetic backgrounds. High numbers of acdS genes and transcripts were evidenced in the rhizosphere of Poaceae, and numbers fluctuated according to plant genotype. Illumina sequencing revealed taxonomic specificities of acdS microorganisms according to plant host. The phylogenetic distance between Poaceae genotypes correlated with acdS transcript numbers, but not with acdS gene numbers or the genetic distance between acdS functional groups.

Conclusion: The development of acdS primers enabled the first direct analysis of ACC deaminase functional group in soil and showed that plant ability to interact with soil-inhabiting acdS microorganisms could also involve particular plant traits unrelated to the evolutionary history of Poaceae species.
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http://dx.doi.org/10.1186/s40168-018-0503-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6011333PMC
June 2018

Phylogenetic diversity and antagonistic traits of root and rhizosphere pseudomonads of bean from Iran for controlling Rhizoctonia solani.

Res Microbiol 2017 Oct 26;168(8):760-772. Epub 2017 Aug 26.

UMR Ecologie Microbienne, CNRS, INRA, VetAgro Sup, UCBL, Université de Lyon, 43 bd du 11 Novembre, F-69622 Villeurbanne, France. Electronic address:

Fluorescent pseudomonads from bean root and rhizosphere in Iran were investigated for biocontrol of the fungal pathogen Rhizoctonia solani. Phylogenetic analysis of concatenated 16S rRNA, gyrB and rpoD sequences for 33 Pseudomonas isolates showed that 15 belonged to four clusters within the 'P. fluorescens' group, i.e. one corresponding to P. thivervalensis, two others including P. moraviensis or P. baetica, and the last one without closely-related established species. The 18 other isolates belonged to five clusters within the 'P. putida' group, one including P. mosselii and P. entomophila, another including strains currently described as P. putida, and three without closely-related species described. Ten isolates were selected based on in vitro inhibition of R. solani. Cellulase activity was identified in three pseudomonads, chitinase activity in two pseudomonads, extracellular protease activity in nine pseudomonads and hydrogen cyanide production in two pseudomonads. Genes coding for production of phenazine, pyoluteorin, pyrrolnitrin and 2,4-diacetylphloroglucinol were not found, whereas the 1-aminocyclopropane-1-carboxylate deamination gene acdS was present in three pseudomonads. The antagonistic acdS strain VKh13 from the 'P. putida' group effectively protected soil-grown bean from R. solani AG 4-HGI. Results show that pseudomonads from uncharacterized taxa were readily obtained from Iranian soils and displayed biocontrol potential against R. solani.
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http://dx.doi.org/10.1016/j.resmic.2017.08.002DOI Listing
October 2017

Distribution of 2,4-Diacetylphloroglucinol Biosynthetic Genes among the spp. Reveals Unexpected Polyphyletism.

Front Microbiol 2017 30;8:1218. Epub 2017 Jun 30.

Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Université de Lyon, Université Claude Bernard Lyon1, VetAgro Sup, UMR Ecologie MicrobienneVilleurbanne, France.

Fluorescent pseudomonads protecting plant roots from phytopathogens by producing 2,4-diacetylphloroglucinol (DAPG) are considered to form a monophyletic lineage comprised of DAPG strains in the "" and "" subgroups of the "" group. However, DAPG production ability has not been investigated for many species of these two subgroups, and whether or not the DAPG are truly monophyletic remained to be verified. Thus, the distribution of the DAPG biosynthetic operon ( genes) in the spp. was investigated in sequenced genomes and type strains. Results showed that the DAPG include species of the "" group, i.e., , and , as expected, as well as in which it had not been documented. Surprisingly, they also include bacteria outside the " group, as exemplified by sp. OT69, and even two Betaproteobacteria genera. The operon-based phylogenetic tree was substantially congruent with the one inferred from concatenated housekeeping genes , and . Contrariwise to current supposition, ancestral character reconstructions favored multiple independent acquisitions rather that one ancestral event followed by vertical inheritance. Indeed, based on synteny analyses, these acquisitions appeared to vary according to the subgroup and even the phylogenetic groups within the subgroups. In conclusion, our study shows that the populations form a polyphyletic group and suggests that DAPG biosynthesis might not be restricted to this genus. This is important to consider when assessing the ecological significance of bacterial populations in rhizosphere ecosystems.
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http://dx.doi.org/10.3389/fmicb.2017.01218DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5491608PMC
June 2017

Let the Core Microbiota Be Functional.

Trends Plant Sci 2017 07 23;22(7):583-595. Epub 2017 May 23.

UMR Ecologie Microbienne, CNRS, INRA, VetAgro Sup, UCBL, Université de Lyon, 69622 Villeurbanne, France.

The microbial community that is systematically associated with a given host plant is called the core microbiota. The definition of the core microbiota was so far based on its taxonomic composition, but we argue that it should also be based on its functions. This so-called functional core microbiota encompasses microbial vehicles carrying replicators (genes) with essential functions for holobiont (i.e., plant plus microbiota) fitness. It builds up from enhanced horizontal transfers of replicators as well as from ecological enrichment of their vehicles. The transmission pathways of this functional core microbiota vary over plant generations according to environmental constraints and its added value for holobiont fitness.
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http://dx.doi.org/10.1016/j.tplants.2017.04.008DOI Listing
July 2017

Fluorescent Pseudomonas Strains with only Few Plant-Beneficial Properties Are Favored in the Maize Rhizosphere.

Front Plant Sci 2016 25;7:1212. Epub 2016 Aug 25.

Université de LyonLyon, France; Université Lyon 1Villeurbanne, France; CNRS, UMR5557, Ecologie MicrobienneVilleurbanne, France; INRA, UMR1418Villeurbanne, France.

Plant Growth-Promoting Rhizobacteria (PGPR) enhance plant health and growth using a variety of traits. Effective PGPR strains typically exhibit multiple plant-beneficial properties, but whether they are better adapted to the rhizosphere than PGPR strains with fewer plant-beneficial properties is unknown. Here, we tested the hypothesis that strains with higher numbers of plant-beneficial properties would be preferentially selected by plant roots. To this end, the co-occurrence of 18 properties involved in enhanced plant nutrition, plant hormone modulation, or pathogen inhibition was analyzed by molecular and biochemical methods in a collection of maize rhizosphere and bulk soil isolates of fluorescent Pseudomonas. Twelve plant-beneficial properties were found among the 698 isolates. Contrarily to expectation, maize preferentially selected pseudomonads with low numbers of plant-beneficial properties (up to five). This selection was not due to the predominance of strains with specific assortments of these properties, or with specific taxonomic status. Therefore, the occurrence of only few plant-beneficial properties appeared favorable for root colonization by pseudomonads.
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http://dx.doi.org/10.3389/fpls.2016.01212DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4996994PMC
September 2016

Is plant evolutionary history impacting recruitment of diazotrophs and nifH expression in the rhizosphere?

Sci Rep 2016 Feb 23;6:21690. Epub 2016 Feb 23.

Université de Lyon, F-69622, Lyon, France.

Plant evolutionary history influences the taxonomic composition of the root-associated bacterial community, but whether it can also modulate its functioning is unknown. Here, we tested the hypothesis that crop diversification is a significant factor determining the ecology of the functional group of nitrogen-fixing bacteria the rhizosphere of Poaceae. A greenhouse experiment was carried out using a range of Poaceae, i.e. four Zea mays varieties (from two genetic groups) and teosinte (representing maize's ancestor), sorghum (from the same Panicoideae subfamily), and wheat (from neighboring Pooideae subfamily), as well as the dicot tomato as external reference. Diazotroph rhizosphere community was characterized at 21 days in terms of size (quantitative PCR of nifH genes), composition (T-RFLP and partial sequencing of nifH alleles) and functioning (quantitative RT-PCR, T-RFLP and partial sequencing of nifH transcripts). Plant species and varieties had a significant effect on diazotroph community size and the number of nifH transcripts per root system. Contrarily to expectations, however, there was no relation between Poaceae evolutionary history and the size, diversity or expression of the rhizosphere diazotroph community. These results suggest a constant selection of this functional group through evolution for optimization of nitrogen fixation in the rhizosphere.
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http://dx.doi.org/10.1038/srep21690DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4763242PMC
February 2016

Analysis of genes contributing to plant-beneficial functions in Plant Growth-Promoting Rhizobacteria and related Proteobacteria.

Sci Rep 2014 Sep 2;4:6261. Epub 2014 Sep 2.

1] Université de Lyon, F-69622, Lyon, France [2] Université Lyon 1, Villeurbanne, France [3] CNRS, UMR5557, Ecologie Microbienne, Villeurbanne, France.

The positive effects of root-colonizing bacteria cooperating with plants lead to improved growth and/or health of their eukaryotic hosts. Some of these Plant Growth-Promoting Rhizobacteria (PGPR) display several plant-beneficial properties, suggesting that the accumulation of the corresponding genes could have been selected in these bacteria. Here, this issue was targeted using 23 genes contributing directly or indirectly to established PGPR effects, based on genome sequence analysis of 304 contrasted Alpha- Beta- and Gammaproteobacteria. Most of the 23 genes studied were also found in non-PGPR Proteobacteria and none of them were common to all 25 PGPR genomes studied. However, ancestral character reconstruction indicated that gene transfers -predominantly ancient- resulted in characteristic gene combinations according to taxonomic subgroups of PGPR strains. This suggests that the PGPR-plant cooperation could have established separately in various taxa, yielding PGPR strains that use different gene assortments. The number of genes contributing to plant-beneficial functions increased along the continuum -animal pathogens, phytopathogens, saprophytes, endophytes/symbionts, PGPR- indicating that the accumulation of these genes (and possibly of different plant-beneficial traits) might be an intrinsic PGPR feature. This work uncovered preferential associations occurring between certain genes contributing to phytobeneficial traits and provides new insights into the emergence of PGPR bacteria.
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http://dx.doi.org/10.1038/srep06261DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4151105PMC
September 2014

Evaluation of rhizobacterial indicators of tobacco black root rot suppressiveness in farmers' fields.

Environ Microbiol Rep 2014 Aug 8;6(4):346-53. Epub 2014 Jan 8.

Université de Lyon, F-69622, Lyon, France; Université Lyon 1, Villeurbanne, France; CNRS, Ecologie Microbienne, UMR5557, Villeurbanne, France; Biology Centre of the Academy of Sciences of the Czech Republic, Institute of Soil Biology, České Budějovice, Czech Republic.

Very few soil quality indicators include disease-suppressiveness criteria. We assessed whether 64 16S rRNA microarray probes whose signals correlated with tobacco black root rot suppressiveness in greenhouse analysis could also discriminate suppressive from conducive soils under field conditions. Rhizobacterial communities of tobacco and wheat sampled in 2 years from four farmers' fields of contrasted suppressiveness status were compared. The 64 previously identified indicator probes correctly classified 72% of 29 field samples, with nine probes for Azospirillum, Gluconacetobacter, Sphingomonadaceae, Planctomycetes, Mycoplasma, Lactobacillus crispatus and Thermodesulforhabdus providing the best prediction. The whole probe set (1033 probes) revealed strong effects of plant, field location and year on rhizobacterial community composition, and a smaller (7% variance) but significant effect of soil suppressiveness status. Seventeen additional probes correlating with suppressiveness status in the field (noticeably for Agrobacterium, Methylobacterium, Ochrobactrum) were selected, and combined with the nine others, they improved correct sample classification from 72% to 79% (100% tobacco and 63% wheat samples). Pseudomonas probes were not informative in the field, even those targeting biocontrol pseudomonads producing 2,4-diacetylphloroglucinol, nor was quantitative polymerase chain reaction for 2,4-diacetylphloroglucinol-synthesis gene phlD. This study shows that a subset of 16S rRNA probes targeting diverse rhizobacteria can be useful as suppressiveness indicators under field conditions.
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http://dx.doi.org/10.1111/1758-2229.12131DOI Listing
August 2014

Frequent, independent transfers of a catabolic gene from bacteria to contrasted filamentous eukaryotes.

Proc Biol Sci 2014 Aug;281(1789):20140848

Université de Lyon, Lyon 69622, France Université Lyon 1, Villeurbanne, France CNRS, UMR5557, Ecologie Microbienne, Villeurbanne, France

Even genetically distant prokaryotes can exchange genes between them, and these horizontal gene transfer events play a central role in adaptation and evolution. While this was long thought to be restricted to prokaryotes, certain eukaryotes have acquired genes of bacterial origin. However, gene acquisitions in eukaryotes are thought to be much less important in magnitude than in prokaryotes. Here, we describe the complex evolutionary history of a bacterial catabolic gene that has been transferred repeatedly from different bacterial phyla to stramenopiles and fungi. Indeed, phylogenomic analysis pointed to multiple acquisitions of the gene in these filamentous eukaryotes-as many as 15 different events for 65 microeukaryotes. Furthermore, once transferred, this gene acquired introns and was found expressed in mRNA databases for most recipients. Our results show that effective inter-domain transfers and subsequent adaptation of a prokaryotic gene in eukaryotic cells can happen at an unprecedented magnitude.
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http://dx.doi.org/10.1098/rspb.2014.0848DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4100511PMC
August 2014

Prevalence of type III secretion system in effective biocontrol pseudomonads.

Res Microbiol 2014 May 12;165(4):300-4. Epub 2014 Apr 12.

Department of Sustainable Agro-Ecosystems and Bioresources, IASMA Research and Innovation Centre, Fondazione Edmund Mach (FEM), I-38010 S. Michele all'Adige, Italy; Research Group Environmental Genomics and Systems Biology, Institute of Natural Resource Sciences, Zurich University for Applied Sciences (ZHAW), Campus Grüental, P.O. Box, CH-8820 Wädenswil, Switzerland. Electronic address:

Functional type III secretion system (T3SS) genes are needed for effective biocontrol of Pythium damping-off of cucumber by Pseudomonas fluorescens KD, but whether biocontrol Pseudomonas strains with T3SS genes display overall a higher plant-protecting activity is unknown. The assessment of 198 biocontrol fluorescent pseudomonads originating from 60 soils worldwide indicated that 32% harbour the ATPase-encoding T3SS gene hrcN, which was most often found in tomato isolates. The hrcN(+) biocontrol strains (and especially those also producing 2,4-diacetylphloroglucinol and displaying 1-aminocyclopropane-1-carboxylate deaminase activity) displayed higher plant-protecting ability in comparison with hrcN(-) biocontrol strains, both in the Pythium/cucumber and Fusarium/cucumber pathosystems.
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http://dx.doi.org/10.1016/j.resmic.2014.03.008DOI Listing
May 2014

Rhizosphere ecology and phytoprotection in soils naturally suppressive to Thielaviopsis black root rot of tobacco.

Environ Microbiol 2014 Jul 17;16(7):1949-60. Epub 2014 Apr 17.

Université de Lyon, F-69622, Lyon, France; Université Lyon 1, Villeurbanne, France; CNRS, UMR5557, Ecologie Microbienne, Villeurbanne, France.

Soil suppressiveness to disease is an intriguing emerging property in agroecosystems, with important implications because it enables significant protection of susceptible plants from soil-borne pathogens. Unlike many soils where disease suppressiveness requires crop monoculture to establish, certain soils are naturally suppressive to disease, and this type of specific disease suppressiveness is maintained despite crop rotation. Soils naturally suppressive to Thielaviopsis basicola-mediated black root rot of tobacco and other crops occur in Morens region (Switzerland) and have been studied for over 30 years. In Morens, vermiculite-rich suppressive soils formed on morainic deposits while illite-rich conducive soils developed on sandstone, but suppressiveness is of microbial origin. Antagonistic pseudomonads play a role in black root rot suppressiveness, including Pseudomonas protegens (formerly P. fluorescens) CHA0, a major model strain for research. However, other types of rhizobacterial taxa may differ in prevalence between suppressive and conducive soils, suggesting that the microbial basis of black root rot suppressiveness could be far more complex than solely a Pseudomonas property. This first review on black root rot suppressive soils covers early findings on these soils, the significance of recent results, and compares them with other types of suppressive soils in terms of rhizosphere ecology and plant protection mechanisms.
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http://dx.doi.org/10.1111/1462-2920.12459DOI Listing
July 2014

Root microbiome relates to plant host evolution in maize and other Poaceae.

Environ Microbiol 2014 Sep 7;16(9):2804-14. Epub 2014 Apr 7.

Université de Lyon, F-69622, Lyon, France; Université Lyon 1, Villeurbanne, France; CNRS, UMR5557, Ecologie Microbienne, Villeurbanne, France.

Prokaryote-eukaryote interactions are primordial, but host selection of its bacterial community remains poorly understood. Because eukaryote evolution affects numerous traits shaping the ecology of their microbiome, we can expect that many evolutionary changes in the former will have the potential to impact on the composition of the latter. Consequently, the more phylogenetically distant the eukaryotic hosts, the more distinct their associated bacterial communities should be. We tested this with plants, by comparing the bacterial communities associated with maize genotypes or other Poaceae. 16S rRNA taxonomic microarray analysis showed that the genetic distance between rhizobacterial communities correlated significantly with the phylogenetic distance (derived from chloroplastic sequences) between Poaceae genotypes. This correlation was also significant when considering specific bacterial populations from all main bacterial divisions, instead of the whole rhizobacterial community. These results indicate that eukaryotic host's evolutionary history can be a significant factor shaping directly the assembly and composition of its associated bacterial compartment.
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http://dx.doi.org/10.1111/1462-2920.12442DOI Listing
September 2014

Cell culturability of Pseudomonas protegens CHA0 depends on soil pH.

FEMS Microbiol Ecol 2014 Feb 14;87(2):441-50. Epub 2013 Nov 14.

Plant Pathology, Institute of Integrative Biology, Swiss Federal Institute of Technology, Zürich, Switzerland; Agroscope Changins-Wädenswil research station ACW, Nyon, Switzerland.

Pseudomonas inoculants may lose colony-forming ability in soil, but soil properties involved are poorly documented. Here, we tested the hypothesis that soil acidity could reduce persistence and cell culturability of Pseudomonas protegens CHA0. At 1 week in vitro, strain CHA0 was found as culturable cells at pH 7, whereas most cells at pH 4 and all cells at pH 3 were noncultured. In 21 natural soils of contrasted pH, cell culturability loss of P. protegens CHA0 took place in all six very acidic soils (pH < 5.0) and in three of five acidic soils (5.0 < pH < 6.5), whereas it was negligible in the neutral and alkaline soils at 2 weeks and 2 months. No correlation was found between total cell counts of P. protegens CHA0 and soil composition data, whereas colony counts of the strain correlated with soil pH. Maintenance of cell culturability in soils coincided with a reduction in inoculant cell size. Some of the noncultured CHA0 cells were nutrient responsive in Kogure's viability test, both in vitro and in soil. Thus, this shows for the first time that the sole intrinsic soil composition factor triggering cell culturability loss in P. protegens CHA0 is soil acidity.
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http://dx.doi.org/10.1111/1574-6941.12234DOI Listing
February 2014

Plant growth-promoting rhizobacteria and root system functioning.

Front Plant Sci 2013 Sep 17;4:356. Epub 2013 Sep 17.

Université de Lyon Lyon, France ; Université Claude Bernard Lyon 1 Villeurbanne, France ; Centre National de la Recherche Scientifique, UMR 5557, Ecologie Microbienne, Université Lyon 1 Villeurbanne, France.

The rhizosphere supports the development and activity of a huge and diversified microbial community, including microorganisms capable to promote plant growth. Among the latter, plant growth-promoting rhizobacteria (PGPR) colonize roots of monocots and dicots, and enhance plant growth by direct and indirect mechanisms. Modification of root system architecture by PGPR implicates the production of phytohormones and other signals that lead, mostly, to enhanced lateral root branching and development of root hairs. PGPR also modify root functioning, improve plant nutrition and influence the physiology of the whole plant. Recent results provided first clues as to how PGPR signals could trigger these plant responses. Whether local and/or systemic, the plant molecular pathways involved remain often unknown. From an ecological point of view, it emerged that PGPR form coherent functional groups, whose rhizosphere ecology is influenced by a myriad of abiotic and biotic factors in natural and agricultural soils, and these factors can in turn modulate PGPR effects on roots. In this paper, we address novel knowledge and gaps on PGPR modes of action and signals, and highlight recent progress on the links between plant morphological and physiological effects induced by PGPR. We also show the importance of taking into account the size, diversity, and gene expression patterns of PGPR assemblages in the rhizosphere to better understand their impact on plant growth and functioning. Integrating mechanistic and ecological knowledge on PGPR populations in soil will be a prerequisite to develop novel management strategies for sustainable agriculture.
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http://dx.doi.org/10.3389/fpls.2013.00356DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3775148PMC
September 2013

Effect of clay mineralogy on iron bioavailability and rhizosphere transcription of 2,4-diacetylphloroglucinol biosynthetic genes in biocontrol Pseudomonas protegens.

Mol Plant Microbe Interact 2013 May;26(5):566-74

Universite de Lyon, Lyon, France.

Pseudomonas strains producing 2,4-diacetylphloroglucinol (DAPG) can protect plants from soilborne phytopathogens and are considered the primary reason for suppressiveness of morainic Swiss soils to Thielaviopsis basicola-mediated black root-rot disease of tobacco, even though they also occur nearby in conducive sandstone soils. The underlying molecular mechanisms accounting for this discrepancy are not understood. In this study, we assessed the hypothesis that the presence of iron-rich vermiculite clay (dominant in suppressive soils) instead of illite (dominant in neighboring conducive soils) translates into higher levels of iron bioavailability and transcription of Pseudomonas DAPG synthetic genes in the tobacco rhizosphere. Rhizosphere monitoring of reporter gene systems pvd-inaZ and phlA-gfp in Pseudomonas protegens indicated that the level of iron bioavailability and the number of cells expressing phl genes (DAPG synthesis), respectively, were higher in vermiculitic than in illitic artificial soils. This was in accordance with the effect of iron on phlA-gfp expression in vitro and, indeed, iron addition to the illitic soil increased the number of cells expressing phlA-gfp. Similar findings were made in the presence of the pathogen T. basicola. Altogether, results substantiate the hypothesis that iron-releasing minerals may confer disease suppressiveness by modulating iron bioavailability in the rhizosphere and expression of biocontrol-relevant genes in antagonistic P. protegens.
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http://dx.doi.org/10.1094/MPMI-11-12-0274-RDOI Listing
May 2013

Unexpected phytostimulatory behavior for Escherichia coli and Agrobacterium tumefaciens model strains.

Mol Plant Microbe Interact 2013 May;26(5):495-502

Universite de Lyon, Lyon, France.

Plant-beneficial effects of bacteria are often underestimated, especially for well-studied strains associated with pathogenicity or originating from other environments. We assessed the impact of seed inoculation with the emblematic bacterial models Agrobacterium tumefaciens C58 (plasmid-cured) or Escherichia coli K-12 on maize seedlings in nonsterile soil. Compared with the noninoculated control, root biomass (with A. tumefaciens or E. coli) and shoot biomass (with A. tumefaciens) were enhanced at 10 days for 'PR37Y15' but not 'DK315', as found with the phytostimulator Azospirillum brasilense UAP-154 (positive control). In roots as well as in shoots, Agrobacterium tumefaciens and E. coli triggered similar (in PR37Y15) or different (in DK315) changes in the high-performance liquid chromatography profiles of secondary metabolites (especially benzoxazinoids), distinct from those of Azospirillum brasilense UAP-154. Genome sequence analysis revealed homologs of nitrite reductase genes nirK and nirBD and siderophore synthesis genes for Agrobacterium tumefaciens, as well as homologs of nitrite reductase genes nirBD and phosphatase genes phoA and appA in E. coli, whose contribution to phytostimulation will require experimental assessment. In conclusion, the two emblematic bacterial models had a systemic impact on maize secondary metabolism and resulted in unexpected phytostimulation of seedlings in the Azospirillum sp.-responsive cultivar.
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http://dx.doi.org/10.1094/MPMI-12-12-0298-RDOI Listing
May 2013

Comparison of prominent Azospirillum strains in Azospirillum-Pseudomonas-Glomus consortia for promotion of maize growth.

Appl Microbiol Biotechnol 2013 May 18;97(10):4639-49. Epub 2012 Jul 18.

Université de Lyon, 69622 Lyon, France.

Azospirillum are prominent plant growth-promoting rhizobacteria (PGPR) extensively used as phytostimulatory crop inoculants, but only few studies are dealing with Azospirillum-containing mixed inocula involving more than two microorganisms. We compared here three prominent Azospirillum strains as part of three-component consortia including also the PGPR Pseudomonas fluorescens F113 and a mycorrhizal inoculant mix composed of three Glomus strains. Inoculant colonization of maize was assessed by quantitative PCR, transcription of auxin synthesis gene ipdC (involved in phytostimulation) in Azospirillum by RT-PCR, and effects on maize by secondary metabolic profiling and shoot biomass measurements. Results showed that phytostimulation by all the three-component consortia was comparable, despite contrasted survival of the Azospirillum strains and different secondary metabolic responses of maize to inoculation. Unexpectedly, the presence of Azospirillum in the inoculum resulted in lower phytostimulation in comparison with the Pseudomonas-Glomus two-component consortium, but this effect was transient. Azospirillum's ipdC gene was transcribed in all treatments, especially with three-component consortia, but not with all plants and samplings. Inoculation had no negative impact on the prevalence of mycorrhizal taxa in roots. In conclusion, this study brought new insights in the functioning of microbial consortia and showed that Azospirillum-Pseudomonas-Glomus three-component inoculants may be useful in environmental biotechnology for maize growth promotion.
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http://dx.doi.org/10.1007/s00253-012-4249-zDOI Listing
May 2013

Evolutionary history of synthesis pathway genes for phloroglucinol and cyanide antimicrobials in plant-associated fluorescent pseudomonads.

Mol Phylogenet Evol 2012 Jun 8;63(3):877-90. Epub 2012 Mar 8.

Plant Pathology, Institute of Integrative Biology, ETH-Zürich, CH-8092 Zürich, Switzerland.

Plant-beneficial fluorescent Pseudomonas spp. play important ecological roles. Here, their evolutionary history was investigated by a multilocus approach targeting genes involved in synthesis of secondary antimicrobial metabolites implicated in biocontrol of phytopathogens. Some of these genes were proposed to be ancestral, and this was investigated using a worldwide collection of 30 plant-colonizing fluorescent pseudomonads, based on phylogenetic analysis of 14 loci involved in production of 2,4-diacetylphloroglucinol (phlACBDE, phlF, intergenic locus phlA/phlF), hydrogen cyanide (hcnABC, anr) or global regulation of secondary metabolism (gacA, gacS, rsmZ). The 10 housekeeping loci rrs, dsbA, gyrB, rpoD, fdxA, recA, rpoB, rpsL, rpsG, and fusA served as controls. Each strain was readily distinguished from the others when considering allelic combinations for these 14 biocontrol-relevant loci. Topology comparisons based on Shimodaira-Hasegawa tests showed extensive incongruence when comparing single-locus phylogenetic trees with one another, but less when comparing (after sequence concatenation) trees inferred for genes involved in 2,4-diacetylphloroglucinol synthesis, hydrogen cyanide synthesis, or secondary metabolism global regulation with trees for housekeeping genes. The 14 loci displayed linkage disequilibrium, as housekeeping loci did, and all 12 protein-coding loci were subjected to purifying selection except for one positively-selected site in HcnA. Overall, the evolutionary history of Pseudomonas genes involved in synthesis of secondary antimicrobial metabolites important for biocontrol functions is in fact similar to that of housekeeping genes, and results suggest that they are ancestral in pseudomonads producing hydrogen cyanide and 2,4-diacetylphloroglucinol.
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http://dx.doi.org/10.1016/j.ympev.2012.02.030DOI Listing
June 2012

Is diversification history of maize influencing selection of soil bacteria by roots?

Mol Ecol 2012 Jan 29;21(1):195-206. Epub 2011 Nov 29.

Université de Lyon, F-69622, Lyon, France.

A wide range of plant lines has been propagated by farmers during crop selection and dissemination, but consequences of this crop diversification on plant-microbe interactions have been neglected. Our hypothesis was that crop evolutionary history shaped the way the resulting lines interact with soil bacteria in their rhizospheres. Here, the significance of maize diversification as a factor influencing selection of soil bacteria by seedling roots was assessed by comparing rhizobacterial community composition of inbred lines representing the five main genetic groups of maize, cultivated in a same European soil. Rhizobacterial community composition of 21-day-old seedlings was analysed using a 16S rRNA taxonomic microarray targeting 19 bacterial phyla. Rhizobacterial community composition of inbred lines depended on the maize genetic group. Differences were largely due to the prevalence of certain Betaproteobacteria and especially Burkholderia, as confirmed by quantitative PCR and cloning/sequencing. However, these differences in bacterial root colonization did not correlate with plant microsatellite genetic distances between maize genetic groups or individual lines. Therefore, the genetic structure of maize that arose during crop diversification (resulting in five main groups), but not the extent of maize diversification itself (as determined by maize genetic distances), was a significant factor shaping rhizobacterial community composition of seedlings.
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http://dx.doi.org/10.1111/j.1365-294X.2011.05359.xDOI Listing
January 2012

Actinobacterial community dominated by a distinct clade in acidic soil of a waterlogged deciduous forest.

FEMS Microbiol Ecol 2011 Nov 9;78(2):386-94. Epub 2011 Aug 9.

Crop Research Institute, Prague, Czech Republic.

Members of the Actinobacteria are among the most important litter decomposers in soil. The site of a waterlogged deciduous forest with acidic soil was explored for actinobacteria because seasonality of litter inputs, temperature, and precipitation provided contrasting environmental conditions, particularly variation of organic matter quantity and quality. We hypothesized that these factors, which are known to influence decomposition, were also likely to affect actinobacterial community composition. The relationship between the actinobacterial community, soil moisture and organic matter content was assessed in two soil horizons in the summer and winter seasons using a 16S rRNA taxonomic microarray and cloning-sequencing of 16S rRNA genes. Both approaches showed that the community differed significantly between horizons and seasons, paralleling the changes in soil moisture and organic matter content. The microarray analysis further indicated that the actinobacterial community of the upper horizon was characterized by high incidence of the genus Mycobacterium. In both horizons and seasons, the actinobacterial clone libraries were dominated (by 80%) by sequences of a separate clade sharing an ancestral node with Streptosporangineae. This relatedness is supported also by some common adaptations, for example, to soil acidity and periodic oxygen deprivation or dryness.
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http://dx.doi.org/10.1111/j.1574-6941.2011.01173.xDOI Listing
November 2011

Development of bacterial community during spontaneous succession on spoil heaps after brown coal mining.

FEMS Microbiol Ecol 2011 Oct 21;78(1):59-69. Epub 2011 Jul 21.

Laboratory of Environmental Microbiology, Institute of Microbiology of the ASCR, Praha, Czech Republic.

Changes in the abundance of bacteria and fungi and in the composition of bacterial communities during primary succession were investigated in a brown coal mine deposit area near Sokolov, the Czech Republic, using phospholipid fatty acids analysis, microarray and 16S rRNA gene sequencing. The study considered a chronosequence of sites undergoing spontaneous succession: 6-, 12-, 21- and 45-year-old and a 21-year-old site revegetated with Alnus glutinosa. During succession, organic carbon and the total nitrogen content increased while the pH and the C/N ratio decreased. Microbial biomass and bacterial diversity increased until 21 years and decreased later; bacteria dominated over fungi in the initial and late phases of succession. Bacterial community composition of the 6-year-old site with no vegetation cover largely differed from the older sites, especially by a higher content of Gammaproteobacteria, Cyanobacteria and some Alphaproteobacteria. Bacteria belonging to the genera Acidithiobacillus, Thiobacillus and related taxa, the CO(2) and N(2) fixers, dominated the community at this site. In the later phases, bacterial community development seemed to reflect more the changes in soil nutrient content and pH than vegetation with a decrease of Actinobacteria and an increase of Acidobacteria. The site revegetated with A. glutinosa resembled the 45-year-old primary succession site and exhibited an even lower pH and C/N ratio, indicating that recultivation is able to accelerate soil development.
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http://dx.doi.org/10.1111/j.1574-6941.2011.01164.xDOI Listing
October 2011

Pseudomonas protegens sp. nov., widespread plant-protecting bacteria producing the biocontrol compounds 2,4-diacetylphloroglucinol and pyoluteorin.

Syst Appl Microbiol 2011 May 9;34(3):180-8. Epub 2011 Mar 9.

Plant Pathology Group, Institute of Integrative Biology, Swiss Federal Institute of Technology (ETH), CH-8092 Zürich, Switzerland.

Fluorescent Pseudomonas strains producing the antimicrobial secondary metabolite 2,4-diacetylphloroglucinol (Phl) play a prominent role in the biocontrol of plant diseases. A subset of Phl-producing fluorescent Pseudomonas strains, which can additionally synthesize the antimicrobial compound pyoluteorin (Plt), appears to cluster separately from other fluorescent Pseudomonas spp. based on 16S rRNA gene analysis and shares at most 98.4% 16S rRNA gene sequence identity with any other Pseudomonas species. In this study, a polyphasic approach based on molecular and phenotypic methods was used to clarify the taxonomy of representative Phl(+) Plt(+) strains isolated from tobacco, cotton or wheat on different continents. Phl(+) Plt(+) strains clustered separately from their nearest phylogenetic neighbors (i.e. species from the 'P. syringae', 'P. fluorescens' and 'P. chlororaphis' species complexes) based on rpoB, rpoD or gyrB phylogenies. DNA-DNA hybridization experiments clarified that Phl(+) Plt(+) strains formed a tight genomospecies that was distinct from P. syringae, P. fluorescens, or P. chlororaphis type strains. Within Phl(+) strains, the Phl(+) Plt(+) strains were differentiated from other biocontrol fluorescent Pseudomonas strains that produced Phl but not Plt, based on phenotypic and molecular data. Discriminative phenotypic characters were also identified by numerical taxonomic analysis and siderotyping. Altogether, this polyphasic approach supported the conclusion that Phl(+) Plt(+) fluorescent Pseudomonas strains belonged to a novel species for which the name Pseudomonas protegens is proposed, with CHA0(T) (=CFBP 6595(T), =DSM 19095(T)) as the type strain.
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http://dx.doi.org/10.1016/j.syapm.2010.10.005DOI Listing
May 2011

The role of the antimicrobial compound 2,4-diacetylphloroglucinol in the impact of biocontrol Pseudomonas fluorescens F113 on Azospirillum brasilense phytostimulators.

Microbiology (Reading) 2011 Jun 27;157(Pt 6):1694-1705. Epub 2011 Jan 27.

CNRS, UMR5557, Ecologie Microbienne, Villeurbanne, France.

Pseudomonads producing the antimicrobial metabolite 2,4-diacetylphloroglucinol (Phl) can control soil-borne phytopathogens, but their impact on other plant-beneficial bacteria remains poorly documented. Here, the effects of synthetic Phl and Phl(+) Pseudomonas fluorescens F113 on Azospirillum brasilense phytostimulators were investigated. Most A. brasilense strains were moderately sensitive to Phl. In vitro, Phl induced accumulation of carotenoids and poly-β-hydroxybutyrate-like granules, cytoplasmic membrane damage and growth inhibition in A. brasilense Cd. Experiments with P. fluorescens F113 and a Phl(-) mutant indicated that Phl production ability contributed to in vitro growth inhibition of A. brasilense Cd and Sp245. Under gnotobiotic conditions, each of the three strains, P. fluorescens F113 and A. brasilense Cd and Sp245, stimulated wheat growth. Co-inoculation of A. brasilense Sp245 and Pseudomonas resulted in the same level of phytostimulation as in single inoculations, whereas it abolished phytostimulation when A. brasilense Cd was used. Pseudomonas Phl production ability resulted in lower Azospirillum cell numbers per root system (based on colony counts) and restricted microscale root colonization of neighbouring Azospirillum cells (based on confocal microscopy), regardless of the A. brasilense strain used. Therefore, this work establishes that Phl(+) pseudomonads have the potential to interfere with A. brasilense phytostimulators on roots and with their plant growth promotion capacity.
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http://dx.doi.org/10.1099/mic.0.043943-0DOI Listing
June 2011