Publications by authors named "Jos M Raaijmakers"

111 Publications

Designing a home for beneficial plant microbiomes.

Curr Opin Plant Biol 2021 Mar 5;62:102025. Epub 2021 Mar 5.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, Netherlands; Institute of Biology, Leiden University, Leiden, Netherlands.

The plant microbiome comprises a highly diverse community of saprotrophic, mutualistic, and pathogenic microbes that can affect plant growth and plant health. There is substantial interest to exploit beneficial members of plant microbiomes for new sustainable management strategies in crop production. However, poor survival and colonization of plant tissues by introduced microbial isolates as well as lack of expression of the plant growth-promoting or disease-suppressive traits at the right time and place are still major limitations for successful implementation of microbiomes in future agricultural practices and plant breeding programs. Similar to building a home for humans, we discuss different strategies of building a home for beneficial plant microbiomes, here referred to as the 'MicrobiHome'.
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http://dx.doi.org/10.1016/j.pbi.2021.102025DOI Listing
March 2021

Extracting the GEMs: Genotype, Environment, and Microbiome Interactions Shaping Host Phenotypes.

Front Microbiol 2020 12;11:574053. Epub 2021 Jan 12.

Department of Microbial Ecology, Netherlands Institute of Ecology, Wageningen, Netherlands.

One of the fundamental tenets of biology is that the phenotype of an organism () is determined by its genotype (), the environment (), and their interaction (). Quantitative phenotypes can then be modeled as = + + + , where is the biological variance. This simple and tractable model has long served as the basis for studies investigating the heritability of traits and decomposing the variability in fitness. The importance and contribution of microbe interactions to a given host phenotype is largely unclear, nor how this relates to the traditional GE model. Here we address this fundamental question and propose an expansion of the original model, referred to as GEM, which explicitly incorporates the contribution of the microbiome () to the host phenotype, while maintaining the simplicity and tractability of the original GE model. We show that by keeping host, environment, and microbiome as separate but interacting variables, the GEM model can capture the nuanced ecological interactions between these variables. Finally, we demonstrate with an experiment how the GEM model can be used to statistically disentangle the relative contributions of each component on specific host phenotypes.
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http://dx.doi.org/10.3389/fmicb.2020.574053DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7874016PMC
January 2021

Successive plant growth amplifies genotype-specific assembly of the tomato rhizosphere microbiome.

Sci Total Environ 2021 Jun 26;772:144825. Epub 2021 Jan 26.

Department of Microbial Ecology, Netherlands Institute of Ecology, Wageningen, the Netherlands; Institute of Biology, Leiden University, Leiden, the Netherlands.

Plant microbiome assembly is a spatial and dynamic process driven by root exudates and influenced by soil type, plant developmental stage and genotype. Genotype-dependent microbiome assembly has been reported for different crop plant species. Despite the effect of plant genetics on microbiome assembly, the magnitude of host control over its root microbiome is relatively small or, for many plant species, still largely unknown. Here we cultivated modern and wild tomato genotypes for four successive cycles and showed that divergence in microbiome assembly between the two genotypes was significantly amplified over time. Also, we show that the composition of the rhizosphere microbiome of modern and wild plants became more dissimilar from the initial bulk soil and from each other. Co-occurrence analyses further identified amplicon sequence variants (ASVs) associated with early and late successions of the tomato rhizosphere microbiome. Among the members of the Late Successional Rhizosphere microbiome, we observed an enrichment of ASVs belonging to the genera Acidovorax, Massilia and Rhizobium in the wild tomato rhizosphere, whereas the modern tomato rhizosphere was enriched for an ASV belonging to the genus Pseudomonas. Collectively, our approach allowed us to study the dynamics of rhizosphere microbiome over successional cultivation as well as to categorize rhizobacterial taxa for their ability to form transient or long-term associations with their host plants.
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http://dx.doi.org/10.1016/j.scitotenv.2020.144825DOI Listing
June 2021

Impact of root-associated strains of three Paraburkholderia species on primary and secondary metabolism of Brassica oleracea.

Sci Rep 2021 Feb 2;11(1):2781. Epub 2021 Feb 2.

Department of Microbial Ecology, Netherlands Institute of Ecology NIOO-KNAW, Wageningen, 6708 PB, The Netherlands.

Several root-colonizing bacterial species can simultaneously promote plant growth and induce systemic resistance. How these rhizobacteria modulate plant metabolism to accommodate the carbon and energy demand from these two competing processes is largely unknown. Here, we show that strains of three Paraburkholderia species, P. graminis PHS1 (Pbg), P. hospita mHSR1 (Pbh), and P. terricola mHS1 (Pbt), upon colonization of the roots of two Broccoli cultivars led to cultivar-dependent increases in biomass, changes in primary and secondary metabolism and induced resistance against the bacterial leaf pathogen Xanthomonas campestris. Strains that promoted growth led to greater accumulation of soluble sugars in the shoot and particularly fructose levels showed an increase of up to 280-fold relative to the non-treated control plants. Similarly, a number of secondary metabolites constituting chemical and structural defense, including flavonoids, hydroxycinnamates, stilbenoids, coumarins and lignins, showed greater accumulation while other resource-competing metabolite pathways were depleted. High soluble sugar generation, efficient sugar utilization, and suppression or remobilization of resource-competing metabolites potentially contributed to curb the tradeoff between the carbon and energy demanding processes induced by Paraburkholderia-Broccoli interaction. Collectively, our results provide a comprehensive and integrated view of the temporal changes in plant metabolome associated with rhizobacteria-mediated plant growth promotion and induced resistance.
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http://dx.doi.org/10.1038/s41598-021-82238-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7854645PMC
February 2021

Discovery of Thanafactin A, a Linear, Proline-Containing Octalipopeptide from sp. SH-C52, Motivated by Genome Mining.

J Nat Prod 2021 01 31;84(1):101-109. Epub 2020 Dec 31.

Pharmaceutical Institute, Department of Pharmaceutical Biology, University of Tübingen, 72076 Tübingen, Germany.

Genome mining of the bacterial strains sp. SH-C52 and DSM 11579 showed that both strains contained a highly similar gene cluster encoding an octamodular nonribosomal peptide synthetase (NRPS) system which was not associated with a known secondary metabolite. Insertional mutagenesis of an NRPS component followed by comparative profiling led to the discovery of the corresponding novel linear octalipopeptide thanafactin A, which was subsequently isolated and its structure determined by two-dimensional NMR and further spectroscopic and chromatographic methods. In bioassays, thanafactin A exhibited weak protease inhibitory activity and was found to modulate swarming motility in a strain-specific manner.
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http://dx.doi.org/10.1021/acs.jnatprod.0c01174DOI Listing
January 2021

Restoring degraded microbiome function with self-assembled communities.

FEMS Microbiol Ecol 2020 Nov;96(12)

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PB, Wageningen, The Netherlands.

The natural microbial functions of many soils are severely degraded. Current state-of-the-art technology to restore these functions is through the isolation, screening, formulation and application of microbial inoculants and synthetic consortia. These approaches have inconsistent success, in part due to the incompatibility between the biofertilizer, crop, climate, existing soil microbiome and physicochemical characteristics of the soils. Here, we review the current state of the art in biofertilization and identify two key deficiencies in current strategies: the difficulty in designing complex multispecies biofertilizers and the bottleneck in scaling the production of complex multispecies biofertilizers. To address the challenge of producing scalable, multispecies biofertilizers, we propose to merge ecological theory with bioprocess engineering to produce 'self-assembled communities' enriched for particular functional guilds and adapted to a target soil and host plant. Using the nitrogen problem as an anchor, we review relevant ecology (microbial, plant and environmental), as well as reactor design strategies and operational parameters for the production of functionally enriched self-assembled communities. The use of self-assembled communities for biofertilization addresses two major hurdles in microbiome engineering: the importance of enriching microbes indigenous to (and targeted for) a specific environment and the recognized potential benefits of microbial consortia over isolates (e.g. functional redundancy). The proposed community enrichment model could also be instrumental for other microbial functions such as phosphorus solubilization, plant growth promotion or disease suppression.
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http://dx.doi.org/10.1093/femsec/fiaa225DOI Listing
November 2020

Towards meaningful scales in ecosystem microbiome research.

Environ Microbiol 2021 Jan 21;23(1):1-4. Epub 2020 Oct 21.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.

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http://dx.doi.org/10.1111/1462-2920.15276DOI Listing
January 2021

Volatiles from soil-borne fungi affect directional growth of roots.

Plant Cell Environ 2021 01 30;44(1):339-345. Epub 2020 Sep 30.

Department of Microbial Ecology, Netherlands Institute of Ecology, Wageningen, The Netherlands.

Volatiles play major roles in mediating ecological interactions between soil (micro)organisms and plants. It is well-established that microbial volatiles can increase root biomass and lateral root formation. To date, however, it is unknown whether microbial volatiles can affect directional root growth. Here, we present a novel method to study belowground volatile-mediated interactions. As proof-of-concept, we designed a root Y-tube olfactometer, and tested the effects of volatiles from four different soil-borne fungi on directional growth of Brassica rapa roots in soil. Subsequently, we compared the fungal volatile organic compounds (VOCs) previously profiled with Gas Chromatography-Mass Spectrometry (GC-MS). Using our newly designed setup, we show that directional root growth in soil is differentially affected by fungal volatiles. Roots grew more frequently toward volatiles from the root pathogen Rhizoctonia solani, whereas volatiles from the other three saprophytic fungi did not impact directional root growth. GC-MS profiling showed that six VOCs were exclusively emitted by R. solani. These findings verify that this novel method is suitable to unravel the intriguing chemical cross-talk between roots and soil-borne fungi and its impact on root growth.
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http://dx.doi.org/10.1111/pce.13890DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7821104PMC
January 2021

Draft Genome Sequence of Lipopeptide-Producing Strain Pseudomonas fluorescens DSM 11579 and Comparative Genomics with sp. Strain SH-C52, a Closely Related Lipopeptide-Producing Strain.

Microbiol Resour Announc 2020 May 21;9(21). Epub 2020 May 21.

Department of Pharmaceutical Biology, Pharmaceutical Institute, University of Tübingen, Tübingen, Germany

DSM 11579 is known to be a producer of the lipopeptides brabantamide and thanamycin. Its draft genome gives insight into the complete secondary metabolite production capacity of the strain and builds the basis for a comparative study with sp. strain SH-C52, a lipopeptide-producing strain involved in natural disease-suppressive soils.
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http://dx.doi.org/10.1128/MRA.00304-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7242667PMC
May 2020

DiSCount: computer vision for automated quantification of seed germination.

Plant Methods 2020 1;16:60. Epub 2020 May 1.

1Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), PO BOX 50, 6708 PB Wageningen, The Netherlands.

Background: Plant parasitic weeds belonging to the genus are a major threat for food production in Sub-Saharan Africa and Southeast Asia. The parasite's life cycle starts with the induction of seed germination by host plant-derived signals, followed by parasite attachment, infection, outgrowth, flowering, reproduction, seed set and dispersal. Given the small seed size of the parasite (< 200 μm), quantification of the impact of new control measures that interfere with seed germination relies on manual, labour-intensive counting of seed batches under the microscope. Hence, there is a need for high-throughput assays that allow for large-scale screening of compounds or microorganisms that adversely affect seed germination.

Results: Here, we introduce DiSCount (gital triga er): a computer vision tool for automated quantification of total and germinated seed numbers in standard glass fibre filter assays. We developed the software using a machine learning approach trained with a dataset of 98 manually annotated images. Then, we validated and tested the model against a total dataset of 188 manually counted images. The results showed that DiSCount has an average error of 3.38 percentage points per image compared to the manually counted dataset. Most importantly, DiSCount achieves a 100 to 3000-fold speed increase in image analysis when compared to manual analysis, with an inference time of approximately 3 s per image on a single CPU and 0.1 s on a GPU.

Conclusions: DiSCount is accurate and efficient in quantifying total and germinated seeds in a standardized germination assay. This automated computer vision tool enables for high-throughput, large-scale screening of chemical compound libraries and biological control agents of this devastating parasitic weed. The complete software and manual are hosted at https://gitlab.com/lodewijk-track32/discount_paper and the archived version is available at Zenodo with the DOI 10.5281/zenodo.3627138. The dataset used for testing is available at Zenodo with the DOI 10.5281/zenodo.3403956.
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http://dx.doi.org/10.1186/s13007-020-00602-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7195706PMC
May 2020

Multitrophic interactions in the rhizosphere microbiome of wheat: from bacteria and fungi to protists.

FEMS Microbiol Ecol 2020 04;96(4)

Laboratory of Environmental Microbiology, Embrapa Environment, Rodovia SP 340 km 125.5, 13918-110, Jaguariúna SP, Brazil.

Plants modulate the soil microbiota by root exudation assembling a complex rhizosphere microbiome with organisms spanning different trophic levels. Here, we assessed the diversity of bacterial, fungal and cercozoan communities in landraces and modern varieties of wheat. The dominant taxa within each group were the bacterial phyla Proteobacteria, Actinobacteria and Acidobacteria; the fungi phyla Ascomycota, Chytridiomycota and Basidiomycota; and the Cercozoa classes Sarcomonadea, Thecofilosea and Imbricatea. We showed that microbial networks of the wheat landraces formed a more intricate network topology than that of modern wheat cultivars, suggesting that breeding selection resulted in a reduced ability to recruit specific microbes in the rhizosphere. The high connectedness of certain cercozoan taxa to bacteria and fungi indicated trophic network hierarchies where certain predators gain predominance over others. Positive correlations between protists and bacteria in landraces were preserved as a subset in cultivars as was the case for the Sarcomonadea class with Actinobacteria. The correlations between the microbiome structure and plant genotype observed in our results suggest the importance of top-down control by organisms of higher trophic levels as a key factor for understanding the drivers of microbiome community assembly in the rhizosphere.
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http://dx.doi.org/10.1093/femsec/fiaa032DOI Listing
April 2020

Microbial and volatile profiling of soils suppressive to of wheat.

Proc Biol Sci 2020 02 19;287(1921):20192527. Epub 2020 Feb 19.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.

In disease-suppressive soils, microbiota protect plants from root infections. Bacterial members of this microbiota have been shown to produce specific molecules that mediate this phenotype. To date, however, studies have focused on individual suppressive soils and the degree of natural variability of soil suppressiveness remains unclear. Here, we screened a large collection of field soils for suppressiveness to using wheat () as a model host plant. A high variation of disease suppressiveness was observed, with 14% showing a clear suppressive phenotype. The microbiological basis of suppressiveness to was confirmed by gamma sterilization and soil transplantation. Amplicon sequencing revealed diverse bacterial taxonomic compositions and no specific taxa were found exclusively enriched in all suppressive soils. Nonetheless, co-occurrence network analysis revealed that two suppressive soils shared an overrepresented bacterial guild dominated by various Acidobacteria. In addition, our study revealed that volatile emission may contribute to suppression, but not for all suppressive soils. Our study raises new questions regarding the possible mechanistic variability of disease-suppressive phenotypes across physico-chemically different soils. Accordingly, we anticipate that larger-scale soil profiling, along with functional studies, will enable a deeper understanding of disease-suppressive microbiomes.
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http://dx.doi.org/10.1098/rspb.2019.2527DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7062018PMC
February 2020

Production of ammonia as a low-cost and long-distance antibiotic strategy by Streptomyces species.

ISME J 2020 02 7;14(2):569-583. Epub 2019 Nov 7.

Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE, Leiden, The Netherlands.

Soil-inhabiting streptomycetes are nature's medicine makers, producing over half of all known antibiotics and many other bioactive natural products. However, these bacteria also produce many volatiles, molecules that disperse through the soil matrix and may impact other (micro)organisms from a distance. Here, we show that soil- and surface-grown streptomycetes have the ability to kill bacteria over long distances via air-borne antibiosis. Our research shows that streptomycetes do so by producing surprisingly high amounts of the low-cost volatile ammonia, dispersing over long distances to inhibit the growth of Gram-positive and Gram-negative bacteria. Glycine is required as precursor to produce ammonia, and inactivation of the glycine cleavage system nullified ammonia biosynthesis and concomitantly air-borne antibiosis. Reduced expression of the porin master regulator OmpR and its cognate kinase EnvZ is used as a resistance strategy by E. coli cells to survive ammonia-mediated antibiosis. Finally, ammonia was shown to enhance the activity of canonical antibiotics, suggesting that streptomycetes adopt a low-cost strategy to sensitize competitors for antibiosis from a distance.
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http://dx.doi.org/10.1038/s41396-019-0537-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6976574PMC
February 2020

Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome.

Science 2019 11;366(6465):606-612

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PB Wageningen, Netherlands.

Microorganisms living inside plants can promote plant growth and health, but their genomic and functional diversity remain largely elusive. Here, metagenomics and network inference show that fungal infection of plant roots enriched for Chitinophagaceae and Flavobacteriaceae in the root endosphere and for chitinase genes and various unknown biosynthetic gene clusters encoding the production of nonribosomal peptide synthetases (NRPSs) and polyketide synthases (PKSs). After strain-level genome reconstruction, a consortium of and was designed that consistently suppressed fungal root disease. Site-directed mutagenesis then revealed that a previously unidentified NRPS-PKS gene cluster from was essential for disease suppression by the endophytic consortium. Our results highlight that endophytic root microbiomes harbor a wealth of as yet unknown functional traits that, in concert, can protect the plant inside out.
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http://dx.doi.org/10.1126/science.aaw9285DOI Listing
November 2019

Harnessing the microbiome to control plant parasitic weeds.

Curr Opin Microbiol 2019 06 23;49:26-33. Epub 2019 Oct 23.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands; Department of Plant Science, The Pennsylvania State University, University Park, PA, USA; Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, USA.

Microbiomes can significantly expand the genomic potential of plants, contributing to nutrient acquisition, plant growth promotion and tolerance to (a)biotic stresses. Among biotic stressors, root parasitic weeds (RPWs), mainly of the genera Orobanche, Phelipanche and Striga, are major yield-limiting factors of a wide range of staple crops, particularly in developing countries. Here, we provide a conceptual synthesis of putative mechanisms by which soil and plant microbiomes could be harnessed to control RPWs. These mechanisms are partitioned in direct and indirect modes of action and discussed in the context of past and present studies on microbe-mediated suppression of RPWs. Specific emphasis is given to the large but yet unexplored potential of root-associated microorganisms to interfere with the chemical signalling cascade between the host plant and the RPWs. We further provide concepts and ideas for future research directions and prospective designs of novel control strategies.
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http://dx.doi.org/10.1016/j.mib.2019.09.006DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6906922PMC
June 2019

Resistance Breeding of Common Bean Shapes the Physiology of the Rhizosphere Microbiome.

Front Microbiol 2019 1;10:2252. Epub 2019 Oct 1.

Cell and Molecular Biology Laboratory, Center for Nuclear Energy in Agriculture CENA, University of São Paulo, Piracicaba, Brazil.

The taxonomically diverse rhizosphere microbiome contributes to plant nutrition, growth and health, including protection against soil-borne pathogens. We previously showed that breeding for -resistance in common bean changed the rhizosphere microbiome composition and functioning. Here, we assessed the impact of -resistance breeding in common bean on microbiome physiology. Combined with metatranscriptome data, community-level physiological profiling by Biolog EcoPlate analyses revealed that the rhizosphere microbiome of the -resistant accession was distinctly different from that of the -susceptible accession, with higher consumption of amino acids and amines, higher metabolism of xylanase and sialidase, and higher expression of genes associated with nitrogen, phosphorus and iron metabolism. The resistome analysis indicates higher expression of soxR, which is involved in protecting bacteria against oxidative stress induced by a pathogen invasion. These results further support our hypothesis that breeding for resistance has unintentionally shaped the assembly and activity of the rhizobacterial community toward a higher abundance of specific rhizosphere competent bacterial taxa that can provide complementary protection against fungal root infections.
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http://dx.doi.org/10.3389/fmicb.2019.02252DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6779718PMC
October 2019

Deciphering rhizosphere microbiome assembly of wild and modern common bean (Phaseolus vulgaris) in native and agricultural soils from Colombia.

Microbiome 2019 08 14;7(1):114. Epub 2019 Aug 14.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), P.O. Box 50, Wageningen, 6708 PB, The Netherlands.

Background: Modern crop varieties are typically cultivated in agriculturally well-managed soils far from the centers of origin of their wild relatives. How this habitat expansion impacted plant microbiome assembly is not well understood.

Results: Here, we investigated if the transition from a native to an agricultural soil affected rhizobacterial community assembly of wild and modern common bean (Phaseolus vulgaris) and if this led to a depletion of rhizobacterial diversity. The impact of the bean genotype on rhizobacterial assembly was more prominent in the agricultural soil than in the native soil. Although only 113 operational taxonomic units (OTUs) out of a total of 15,925 were shared by all eight bean accessions grown in native and agricultural soils, this core microbiome represented a large fraction (25.9%) of all sequence reads. More OTUs were exclusively found in the rhizosphere of common bean in the agricultural soil as compared to the native soil and in the rhizosphere of modern bean accessions as compared to wild accessions. Co-occurrence analyses further showed a reduction in complexity of the interactions in the bean rhizosphere microbiome in the agricultural soil as compared to the native soil.

Conclusions: Collectively, these results suggest that habitat expansion of common bean from its native soil environment to an agricultural context had an unexpected overall positive effect on rhizobacterial diversity and led to a stronger bean genotype-dependent effect on rhizosphere microbiome assembly.
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http://dx.doi.org/10.1186/s40168-019-0727-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6694607PMC
August 2019

Volatiles of pathogenic and non-pathogenic soil-borne fungi affect plant development and resistance to insects.

Oecologia 2019 Jul 15;190(3):589-604. Epub 2019 Jun 15.

Laboratory of Entomology, Wageningen University and Research, Wageningen, The Netherlands.

Plants are ubiquitously exposed to a wide diversity of (micro)organisms, including mutualists and antagonists. Prior to direct contact, plants can perceive microbial organic and inorganic volatile compounds (hereafter: volatiles) from a distance that, in turn, may affect plant development and resistance. To date, however, the specificity of plant responses to volatiles emitted by pathogenic and non-pathogenic fungi and the ecological consequences of such responses remain largely elusive. We investigated whether Arabidopsis thaliana plants can differentiate between volatiles of pathogenic and non-pathogenic soil-borne fungi. We profiled volatile organic compounds (VOCs) and measured CO emission of 11 fungi. We assessed the main effects of fungal volatiles on plant development and insect resistance. Despite distinct differences in VOC profiles between the pathogenic and non-pathogenic fungi, plants did not discriminate, based on plant phenotypic responses, between pathogenic and non-pathogenic fungi. Overall, plant growth was promoted and flowering was accelerated upon exposure to fungal volatiles, irrespectively of fungal CO emission levels. In addition, plants became significantly more susceptible to a generalist insect leaf-chewing herbivore upon exposure to the volatiles of some of the fungi, demonstrating that a prior fungal volatile exposure can negatively affect plant resistance. These data indicate that plant development and resistance can be modulated in response to exposure to fungal volatiles.
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http://dx.doi.org/10.1007/s00442-019-04433-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6647456PMC
July 2019

Ecology and Evolution of Plant Microbiomes.

Annu Rev Microbiol 2019 09 15;73:69-88. Epub 2019 May 15.

Department of Microbial Ecology, Netherlands Institute of Ecology, 6708 PB Wageningen, The Netherlands; email:

Microorganisms colonizing plant surfaces and internal tissues provide a number of life-support functions for their host. Despite increasing recognition of the vast functional capabilities of the plant microbiome, our understanding of the ecology and evolution of the taxonomically hyperdiverse microbial communities is limited. Here, we review current knowledge of plant genotypic and phenotypic traits as well as allogenic and autogenic factors that shape microbiome composition and functions. We give specific emphasis to the impact of plant domestication on microbiome assembly and how insights into microbiomes of wild plant relatives and native habitats can contribute to reinstate or enrich for microorganisms with beneficial effects on plant growth, development, and health. Finally, we introduce new concepts and perspectives in plant microbiome research, in particular how community ecology theory can provide a mechanistic framework to unravel the interplay of distinct ecological processes-i.e., selection, dispersal, drift, diversification-that structure the plant microbiome.
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http://dx.doi.org/10.1146/annurev-micro-090817-062524DOI Listing
September 2019

Priming of Plant Growth Promotion by Volatiles of Root-Associated Microbacterium spp.

Appl Environ Microbiol 2018 11 30;84(22). Epub 2018 Oct 30.

Department of Microbial Ecology, Netherlands Institute of Ecology, Wageningen, The Netherlands

Volatile compounds produced by plant-associated microorganisms represent a diverse resource to promote plant growth and health. Here, we investigated the effect of volatiles from root-associated species on plant growth and development. Volatiles of eight strains induced significant increases in shoot and root biomass of but differed in their effects on root architecture. strain EC8 also enhanced root and shoot biomass of lettuce and tomato. Biomass increases were also observed for plants exposed only briefly to volatiles from EC8 prior to transplantation of the seedlings to soil. These results indicate that volatiles from EC8 can prime plants for growth promotion without direct and prolonged contact. We further showed that the induction of plant growth promotion is tissue specific; that is, exposure of roots to volatiles from EC8 led to an increase in plant biomass, whereas shoot exposure resulted in no or less growth promotion. Gas chromatography-quadrupole time of flight mass spectometry (GC-QTOF-MS) analysis revealed that EC8 produces a wide array of sulfur-containing compounds, as well as ketones. Bioassays with synthetic sulfur volatile compounds revealed that the plant growth response to dimethyl trisulfide was concentration-dependent, with a significant increase in shoot weight at 1 μM and negative effects on plant biomass at concentrations higher than 1 mM. Genome-wide transcriptome analysis of volatile-exposed seedlings showed upregulation of genes involved in assimilation and transport of sulfate and nitrate. Collectively, these results show that root-associated primes plants, via the roots, for growth promotion, most likely via modulation of sulfur and nitrogen metabolism. In the past decade, various studies have described the effects of microbial volatiles on other (micro)organisms , but their broad-spectrum activity and the mechanisms underlying volatile-mediated plant growth promotion have not been addressed in detail. Here, we revealed that volatiles from root-associated bacteria of the genus can enhance the growth of different plant species and can prime plants for growth promotion without direct and prolonged contact between the bacterium and the plant. Collectively, these results provide new opportunities for sustainable agriculture and horticulture by exposing roots of plants only briefly to a specific blend of microbial volatile compounds prior to transplantation of the seedlings to the greenhouse or field. This strategy has no need for large-scale introduction or root colonization and survival of the microbial inoculant.
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http://dx.doi.org/10.1128/AEM.01865-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6210106PMC
November 2018

The wild side of plant microbiomes.

Microbiome 2018 08 16;6(1):143. Epub 2018 Aug 16.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), P.O. Box 50, 6708 PB, Wageningen, The Netherlands.

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http://dx.doi.org/10.1186/s40168-018-0519-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6097318PMC
August 2018

Microbial Extracellular Polymeric Substances: Ecological Function and Impact on Soil Aggregation.

Front Microbiol 2018 23;9:1636. Epub 2018 Jul 23.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, Netherlands.

A wide range of microorganisms produce extracellular polymeric substances (EPS), highly hydrated polymers that are mainly composed of polysaccharides, proteins, and DNA. EPS are fundamental for microbial life and provide an ideal environment for chemical reactions, nutrient entrapment, and protection against environmental stresses such as salinity and drought. Microbial EPS can enhance the aggregation of soil particles and benefit plants by maintaining the moisture of the environment and trapping nutrients. In addition, EPS have unique characteristics, such as biocompatibility, gelling, and thickening capabilities, with industrial applications. However, despite decades of research on the industrial potential of EPS, only a few polymers are widely used in different areas, especially in agriculture. This review provides an overview of current knowledge on the ecological functions of microbial EPSs and their application in agricultural soils to improve soil particle aggregation, an important factor for soil structure, health, and fertility.
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http://dx.doi.org/10.3389/fmicb.2018.01636DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6064872PMC
July 2018

Breeding for soil-borne pathogen resistance impacts active rhizosphere microbiome of common bean.

ISME J 2018 12 17;12(12):3038-3042. Epub 2018 Jul 17.

Cell and Molecular Biology Laboratory, Center for Nuclear Energy in Agriculture CENA, University of Sao Paulo USP, Piracicaba, SP, 13416-000, Brazil.

Over the past century, plant breeding programs have substantially improved plant growth and health, but have not yet considered the potential effects on the plant microbiome. Here, we conducted metatranscriptome analysis to determine if and how breeding for resistance of common bean against the root pathogen Fusarium oxysporum (Fox) affected gene expression in the rhizobacterial community. Our data revealed that the microbiome of the Fox-resistant cultivar presented a significantly higher expression of genes associated with nutrient metabolism, motility, chemotaxis, and the biosynthesis of the antifungal compounds phenazine and colicin V. Network analysis further revealed a more complex community for Fox-resistant cultivar and indicated Paenibacillus as a keystone genus in the rhizosphere microbiome. We suggest that resistance breeding in common bean has unintentionally co-selected for plant traits that strengthen the rhizosphere microbiome network structure and enrich for specific beneficial bacterial genera that express antifungal traits involved in plant protection against infections by root pathogens.
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http://dx.doi.org/10.1038/s41396-018-0234-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6246553PMC
December 2018

Involvement of Burkholderiaceae and sulfurous volatiles in disease-suppressive soils.

ISME J 2018 09 13;12(9):2307-2321. Epub 2018 Jun 13.

Department of Microbial Ecology, The Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.

Disease-suppressive soils are ecosystems in which plants suffer less from root infections due to the activities of specific microbial consortia. The characteristics of soils suppressive to specific fungal root pathogens are comparable to those of adaptive immunity in animals, as reported by Raaijmakers and Mazzola (Science 352:1392-3, 2016), but the mechanisms and microbial species involved in the soil suppressiveness are largely unknown. Previous taxonomic and metatranscriptome analyses of a soil suppressive to the fungal root pathogen Rhizoctonia solani revealed that members of the Burkholderiaceae family were more abundant and more active in suppressive than in non-suppressive soils. Here, isolation, phylogeny, and soil bioassays revealed a significant disease-suppressive activity for representative isolates of Burkholderia pyrrocinia, Paraburkholderia caledonica, P. graminis, P. hospita, and P. terricola. In vitro antifungal activity was only observed for P. graminis. Comparative genomics and metabolite profiling further showed that the antifungal activity of P. graminis PHS1 was associated with the production of sulfurous volatile compounds encoded by genes not found in the other four genera. Site-directed mutagenesis of two of these genes, encoding a dimethyl sulfoxide reductase and a cysteine desulfurase, resulted in a loss of antifungal activity both in vitro and in situ. These results indicate that specific members of the Burkholderiaceae family contribute to soil suppressiveness via the production of sulfurous volatile compounds.
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http://dx.doi.org/10.1038/s41396-018-0186-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6092406PMC
September 2018

Modulation of plant chemistry by beneficial root microbiota.

Nat Prod Rep 2018 05 3;35(5):398-409. Epub 2018 May 3.

Netherlands Institute of Ecology NIOO-KNAW, Department of Microbial Ecology, Wageningen, 6708 PB, Netherlands.

Covering: 1981-2017Plants are colonized by an astounding number of microorganisms that can reach cell densities much greater than the number of plant cells. Various plant-associated microorganisms can have profound beneficial effects on plant growth, development, physiology and tolerance to (a)biotic stress. In return, plants release metabolites into their direct surroundings, thereby feeding the microbial community and influencing their composition, gene expression and the production of secondary metabolites. Similarly, microbes living on and in plant tissue may induce known and yet unknown biosynthetic pathways in plants leading to diverse alterations in the plant metabolome. Here, we provide an overview of the impact of beneficial microbiota on plant chemistry, with an emphasis on bacteria living on or inside root tissues. We will also provide new perspectives on deciphering the yet untapped potential of microbe-mediated alteration of plant chemistry as an alternative platform to discover new pathways, genes and enzymes involved the biosynthesis of high value natural plant products.
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http://dx.doi.org/10.1039/c7np00057jDOI Listing
May 2018

Comparative Microbiome Analysis of a Fusarium Wilt Suppressive Soil and a Fusarium Wilt Conducive Soil From the Châteaurenard Region.

Front Microbiol 2018 4;9:568. Epub 2018 Apr 4.

Agroécologie, AgroSup Dijon, Institut National de la Recherche Agronomique, Université Bourgogne Franche-Comté, Dijon, France.

Disease-suppressive soils are soils in which specific soil-borne plant pathogens cause only limited disease although the pathogen and susceptible host plants are both present. Suppressiveness is in most cases of microbial origin. We conducted a comparative metabarcoding analysis of the taxonomic diversity of fungal and bacterial communities from suppressive and non-suppressive (conducive) soils as regards Fusarium wilts sampled from the Châteaurenard region (France). Bioassays based on Fusarium wilt of flax confirmed that disease incidence was significantly lower in the suppressive soil than in the conducive soil. Furthermore, we succeeded in partly transferring Fusarium wilt-suppressiveness to the conducive soil by mixing 10% (w/w) of the suppressive soil into the conducive soil. Fungal diversity differed significantly between the suppressive and conducive soils. Among dominant fungal operational taxonomic units (OTUs) affiliated to known genera, 17 OTUs were detected exclusively in the suppressive soil. These OTUs were assigned to the , and genera. Additionally, the relative abundance of specific members of the bacterial community was significantly higher in the suppressive and mixed soils than in the conducive soil. OTUs found more abundant in Fusarium wilt-suppressive soils were affiliated to the bacterial genera , and . Several of the fungal and bacterial genera detected exclusively or more abundantly in the Fusarium wilt-suppressive soil included genera known for their activity against . Overall, this study supports the potential role of known fungal and bacterial genera in Fusarium wilt suppressive soils from Châteaurenard and pinpoints new bacterial and fungal genera for their putative role in Fusarium wilt suppressiveness.
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http://dx.doi.org/10.3389/fmicb.2018.00568DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5893819PMC
April 2018

Embracing Community Ecology in Plant Microbiome Research.

Trends Plant Sci 2018 06 11;23(6):467-469. Epub 2018 Apr 11.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), 6708 PB Wageningen, The Netherlands.

Community assembly is mediated by selection, dispersal, drift, and speciation. Environmental selection is mostly used to date to explain patterns in plant microbiome assembly, whereas the influence of the other processes remains largely elusive. Recent studies highlight that adopting community ecology concepts provides a mechanistic framework for plant microbiome research.
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http://dx.doi.org/10.1016/j.tplants.2018.03.013DOI Listing
June 2018

Healthy scents: microbial volatiles as new frontier in antibiotic research?

Curr Opin Microbiol 2018 10 12;45:84-91. Epub 2018 Mar 12.

Netherlands Institute of Ecology, Droevendaalsesteeg 10, 6708 PB Wageningen, The Netherlands. Electronic address:

Microorganisms represent a large and still resourceful pool for the discovery of novel compounds to combat antibiotic resistance in human and animal pathogens. The ability of microorganisms to produce structurally diverse volatile compounds has been known for decades, yet their biological functions and antimicrobial activities have only recently attracted attention. Various studies revealed that microbial volatiles can act as infochemicals in long-distance cross-kingdom communication as well as antimicrobials in competition and predation. Here, we review recent insights into the natural functions and modes of action of microbial volatiles and discuss their potential as a new class of antimicrobials and modulators of antibiotic resistance.
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http://dx.doi.org/10.1016/j.mib.2018.02.011DOI Listing
October 2018

Lost in diversity: the interactions between soil-borne fungi, biodiversity and plant productivity.

New Phytol 2018 04 22;218(2):542-553. Epub 2018 Feb 22.

School of Biological Sciences, University of Essex, Wivenhoe Park, Colchester, CO4 3SQ, UK.

There is consensus that plant species richness enhances plant productivity within natural grasslands, but the underlying drivers remain debated. Recently, differential accumulation of soil-borne fungal pathogens across the plant diversity gradient has been proposed as a cause of this pattern. However, the below-ground environment has generally been treated as a 'black box' in biodiversity experiments, leaving these fungi unidentified. Using next generation sequencing and pathogenicity assays, we analysed the community composition of root-associated fungi from a biodiversity experiment to examine if evidence exists for host specificity and negative density dependence in the interplay between soil-borne fungi, plant diversity and productivity. Plant species were colonised by distinct (pathogenic) fungal communities and isolated fungal species showed negative, species-specific effects on plant growth. Moreover, 57% of the pathogenic fungal operational taxonomic units (OTUs) recorded in plant monocultures were not detected in eight plant species plots, suggesting a loss of pathogenic OTUs with plant diversity. Our work provides strong evidence for host specificity and negative density-dependent effects of root-associated fungi on plant species in grasslands. Our work substantiates the hypothesis that fungal root pathogens are an important driver of biodiversity-ecosystem functioning relationships.
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http://dx.doi.org/10.1111/nph.15036DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5887887PMC
April 2018

Secondary Metabolism and Interspecific Competition Affect Accumulation of Spontaneous Mutants in the GacS-GacA Regulatory System in .

mBio 2018 01 16;9(1). Epub 2018 Jan 16.

Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, USA

Secondary metabolites are synthesized by many microorganisms and provide a fitness benefit in the presence of competitors and predators. Secondary metabolism also can be costly, as it shunts energy and intermediates from primary metabolism. In spp., secondary metabolism is controlled by the GacS-GacA global regulatory system. Intriguingly, spontaneous mutations in or (Gac mutants) are commonly observed in laboratory cultures. Here we investigated the role of secondary metabolism in the accumulation of Gac mutants in strain Pf-5. Our results showed that secondary metabolism, specifically biosynthesis of the antimicrobial compound pyoluteorin, contributes significantly to the accumulation of Gac mutants. Pyoluteorin biosynthesis, which poses a metabolic burden on the producer cells, but not pyoluteorin itself, leads to the accumulation of the spontaneous mutants. Interspecific competition also influenced the accumulation of the Gac mutants: a reduced proportion of Gac mutants accumulated when Pf-5 was cocultured with than in pure cultures of strain Pf-5. Overall, our study associated a fitness trade-off with secondary metabolism, with metabolic costs versus competitive benefits of production influencing the evolution of , assessed by the accumulation of Gac mutants. Many microorganisms produce antibiotics, which contribute to ecologic fitness in natural environments where microbes constantly compete for resources with other organisms. However, biosynthesis of antibiotics is costly due to the metabolic burdens of the antibiotic-producing microorganism. Our results provide an example of the fitness trade-off associated with antibiotic production. Under noncompetitive conditions, antibiotic biosynthesis led to accumulation of spontaneous mutants lacking a master regulator of antibiotic production. However, relatively few of these spontaneous mutants accumulated when a competitor was present. Results from this work provide information on the evolution of antibiotic biosynthesis and provide a framework for their discovery and regulation.
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http://dx.doi.org/10.1128/mBio.01845-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5770548PMC
January 2018