Publications by authors named "Paolina Garbeva"

51 Publications

Microbial volatile organic compounds in intra-kingdom and inter-kingdom interactions.

Nat Rev Microbiol 2021 Feb 1. Epub 2021 Feb 1.

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

Microorganisms produce and excrete a versatile array of metabolites with different physico-chemical properties and biological activities. However, the ability of microorganisms to release volatile compounds has only attracted research attention in the past decade. Recent research has revealed that microbial volatiles are chemically very diverse and have important roles in distant interactions and communication. Microbial volatiles can diffuse fast in both gas and water phases, and thus can mediate swift chemical interactions. As well as constitutively emitted volatiles, microorganisms can emit induced volatiles that are triggered by biological interactions or environmental cues. In this Review, we highlight recent discoveries concerning microbial volatile compounds and their roles in intra-kingdom microbial interactions and inter-kingdom interactions with plants and insects. Furthermore, we indicate the potential biotechnological applications of microbial volatiles and discuss challenges and perspectives in this emerging research field.
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http://dx.doi.org/10.1038/s41579-020-00508-1DOI Listing
February 2021

Intraspecific variation in multiple trait responses of Alexandrium ostenfeldii towards elevated pCO.

Harmful Algae 2021 01 15;101:101970. Epub 2021 Jan 15.

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

Dissolved oceanic CO concentrations are rising as result of increasing atmospheric partial pressure of CO (pCO), which has large consequences for phytoplankton. To test how higher CO availability affects different traits of the toxic dinoflagellate Alexandrium ostenfeldii, we exposed three strains of the same population to 400 and 1,000 µatm CO, and measured traits including growth rate, cell volume, elemental composition, C fractionation, toxin content, and volatile organic compounds (VOCs). Strains largely increased their growth rates and particulate organic carbon and nitrogen production with higher pCO and showed significant changes in their VOC profile. One strain showed a significant decrease in both PSP and cyclic imine content and thereby in cellular toxicity. Fractionation against C increased in response to elevated pCO, which may point towards enhanced CO acquisition and/or a downscaling of the carbon concentrating mechanisms. Besides consistent responses in some traits, other traits showed large variation in both direction and strength of responses towards elevated pCO. The observed intraspecific variation in phenotypic plasticity of important functional traits within the same population may help A. ostenfeldii to negate the effects of immediate environmental fluctuations and allow populations to adapt more quickly to changing environments.
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http://dx.doi.org/10.1016/j.hal.2020.101970DOI Listing
January 2021

A non-invasive soil-based setup to study tomato root volatiles released by healthy and infected roots.

Sci Rep 2020 07 29;10(1):12704. Epub 2020 Jul 29.

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

The role of root exudates in mediating plant-microbe interactions has been well documented. However, the function of volatile organic compounds (VOCs) emitted by plant roots has only recently begun to attract attention. This newly recognized relevance of belowground VOCs has so far mostly been tested using systems limited to a two-compartment Petri-dish design. Furthermore, many of the plant-microbe interaction studies have only investigated the effects of microbial VOCs on plant growth. Here, we go two steps further. First we investigated the volatile profile of healthy and pathogen (Fusarium oxysporum) infected tomato roots grown in soil. We then used a unique soil-based olfactometer-choice assay to compare the migration pattern of four beneficial bacteria (Bacillus spp.) towards the roots of the tomato plants. We demonstrate that the blend of root-emitted VOCs differs between healthy and diseased plants. Our results show that VOCs are involved in attracting bacteria to plant roots.
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http://dx.doi.org/10.1038/s41598-020-69468-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7391657PMC
July 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

Effects of plastic mulch film residues on wheat rhizosphere and soil properties.

J Hazard Mater 2020 04 17;387:121711. Epub 2019 Nov 17.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), 6700 AB Wageningen, the Netherlands.

Plastic residues could accumulate in soils as a consequence of using plastic mulching, which results in a serious environmental concern for agroecosystems. As an alternative, biodegradable plastic films stand as promising products to minimize plastic debris accumulation and reduce soil pollution. However, the effects of residues from traditional and biodegradable plastic films on the soil-plant system are not well studied. In this study, we used a controlled pot experiment to investigate the effects of macro- and micro- sized residues of low-density polyethylene and biodegradable plastic mulch films on the rhizosphere bacterial communities, rhizosphere volatile profiles and soil chemical properties. Interestingly, we identified significant effects of biodegradable plastic residues on the rhizosphere bacterial communities and on the blend of volatiles emitted in the rhizosphere. For example, in treatments with biodegradable plastics, bacteria genera like Bacillus and Variovorax were present in higher relative abundances and volatile compounds like dodecanal were exclusively produced in treatment with biodegradable microplastics. Furthermore, significant differences in soil pH, electrical conductivity and C:N ratio were observed across treatments. Our study provides evidence for both biotic and abiotic impacts of plastic residues on the soil-plant system, suggesting the urgent need for more research examining their environmental impacts on agroecosystems.
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http://dx.doi.org/10.1016/j.jhazmat.2019.121711DOI Listing
April 2020

The ecological role of bacterial seed endophytes associated with wild cabbage in the United Kingdom.

Microbiologyopen 2020 01 13;9(1):e00954. Epub 2019 Nov 13.

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

Endophytic bacteria are known for their ability in promoting plant growth and defense against biotic and abiotic stress. However, very little is known about the microbial endophytes living in the spermosphere. Here, we isolated bacteria from the seeds of five different populations of wild cabbage (Brassica oleracea L) that grow within 15 km of each other along the Dorset coast in the UK. The seeds of each plant population contained a unique microbiome. Sequencing of the 16S rRNA genes revealed that these bacteria belong to three different phyla (Actinobacteria, Firmicutes, and Proteobacteria). Isolated endophytic bacteria were grown in monocultures or mixtures and the effects of bacterial volatile organic compounds (VOCs) on the growth and development on B. oleracea and on resistance against a insect herbivore was evaluated. Our results reveal that the VOCs emitted by the endophytic bacteria had a profound effect on plant development but only a minor effect on resistance against an herbivore of B. oleracea. Plants exposed to bacterial VOCs showed faster seed germination and seedling development. Furthermore, seed endophytic bacteria exhibited activity via volatiles against the plant pathogen F. culmorum. Hence, our results illustrate the ecological importance of the bacterial seed microbiome for host plant health and development.
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http://dx.doi.org/10.1002/mbo3.954DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6957406PMC
January 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

Airborne medicine: bacterial volatiles and their influence on plant health.

New Phytol 2020 04 27;226(1):32-43. Epub 2019 Nov 27.

Department of Biology, University of Fribourg, Chemin du musée 10, CH-1700, Fribourg, Switzerland.

Like most other eukaryotes, plants do not live alone but in close association with a diverse microflora. These plant-associated microbes contribute to plant health in many different ways, ranging from modulation of hormonal pathways to direct antibiosis of plant pathogens. Over the last 15 yr, the importance of volatile organic compounds as mediators of mutualistic interactions between plant-associated bacteria and their hosts has become evident. This review summarizes current knowledge concerning bacterial volatile-mediated plant protection against abiotic and biotic stresses. It then discusses the translational potential of such metabolites or of their emitters for sustainable crop protection, the possible ways to harness this potential, and the major challenges still preventing us from doing so. Finally, the review concludes with highlighting the most pressing scientific gaps that need to be filled in order to enable a better understanding of: the molecular mechanisms underlying the biosynthesis of bacterial volatiles; the complex regulation of bacterial volatile emission in natural communities; the perception of bacterial volatiles by plants; and the modes of actions of bacterial volatiles on their host.
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http://dx.doi.org/10.1111/nph.16282DOI Listing
April 2020

Volatile-mediated antagonism of soil bacterial communities against fungi.

Environ Microbiol 2020 03 4;22(3):1025-1035. Epub 2019 Nov 4.

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

Competition is a major type of interaction between fungi and bacteria in soil and is also an important factor in suppression of plant diseases caused by soil-borne fungal pathogens. There is increasing attention for the possible role of volatiles in competitive interactions between bacteria and fungi. However, knowledge on the actual role of bacterial volatiles in interactions with fungi within soil microbial communities is lacking. Here, we examined colonization of sterile agricultural soils by fungi and bacteria from non-sterile soil inoculums during exposure to volatiles emitted by soil-derived bacterial communities. We found that colonization of soil by fungi was negatively affected by exposure to volatiles emitted by bacterial communities whereas that of bacteria was barely changed. Furthermore, there were strong effects of bacterial community volatiles on the assembly of fungal soil colonizers. Identification of volatile composition produced by bacterial communities revealed several compounds with known fungistatic activity. Our results are the first to reveal a collective volatile-mediated antagonism of soil bacteria against fungi. Given the better exploration abilities of filamentous fungi in unsaturated soils, this may be an important strategy for bacteria to defend occupied nutrient patches against invading fungi. Another implication of our research is that bacterial volatiles in soil atmospheres can have a major contribution to soil fungistasis.
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http://dx.doi.org/10.1111/1462-2920.14808DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7064993PMC
March 2020

Phylogenomic analyses and distribution of terpene synthases among .

Beilstein J Org Chem 2019 29;15:1181-1193. Epub 2019 May 29.

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

Terpene synthases are widely distributed among microorganisms and have been mainly studied in members of the genus . However, little is known about the distribution and evolution of the genes for terpene synthases. Here, we performed whole-genome based phylogenetic analysis of species, and compared the distribution of terpene synthase genes among them. Overall, our study revealed that ten major types of terpene synthases are present within the genus , namely those for geosmin, 2-methylisoborneol, -isozizaene, 7--α-eudesmol, -cubenol, caryolan-1-ol, cyclooctat-9-en-7-ol, isoafricanol, pentalenene and α-amorphene. The species divide in three phylogenetic groups based on their whole genomes for which the distribution of the ten terpene synthases was analysed. Geosmin synthases were the most widely distributed and were found to be evolutionary positively selected. Other terpene synthases were found to be specific for one of the three clades or a subclade within the genus . A phylogenetic analysis of the most widely distributed classes of terpene synthases in comparison to the phylogenomic analysis of this genus is discussed.
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http://dx.doi.org/10.3762/bjoc.15.115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6604706PMC
May 2019

Microbe-driven chemical ecology: past, present and future.

ISME J 2019 11 9;13(11):2656-2663. Epub 2019 Jul 9.

Netherlands Institute of Ecology, Wageningen, 6708 PB, The Netherlands.

In recent years, research in the field of Microbial Ecology has revealed the tremendous diversity and complexity of microbial communities across different ecosystems. Microbes play a major role in ecosystem functioning and contribute to the health and fitness of higher organisms. Scientists are now facing many technological and methodological challenges in analyzing these complex natural microbial communities. The advances in analytical and omics techniques have shown that microbial communities are largely shaped by chemical interaction networks mediated by specialized (water-soluble and volatile) metabolites. However, studies concerning microbial chemical interactions need to consider biotic and abiotic factors on multidimensional levels, which require the development of new tools and approaches mimicking natural microbial habitats. In this review, we describe environmental factors affecting the production and transport of specialized metabolites. We evaluate their ecological functions and discuss approaches to address future challenges in microbial chemical ecology (MCE). We aim to emphasize that future developments in the field of MCE will need to include holistic studies involving organisms at all levels and to consider mechanisms underlying the interactions between viruses, micro-, and macro-organisms in their natural environments.
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http://dx.doi.org/10.1038/s41396-019-0469-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6794290PMC
November 2019

Pathogen suppression by microbial volatile organic compounds in soils.

FEMS Microbiol Ecol 2019 08;95(8)

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

There is increasing evidence that microbial volatile organic compounds (mVOCs) play an important role in interactions between microbes in soils. In this minireview, we zoom in on the possible role of mVOCs in the suppression of plant-pathogenic soil fungi. In particular, we have screened the literature to see what the actual evidence is that mVOCs in soil atmospheres can contribute to pathogen suppression. Furthermore, we discuss biotic and abiotic factors that influence the production of suppressive mVOCs in soils. Since microbes producing mVOCs in soils are part of microbial communities, community ecological aspects such as diversity and assembly play an important role in the composition of produced mVOC blends. These aspects have not received much attention so far. In addition, the fluctuating abiotic conditions in soils, such as changing moisture contents, influence mVOC production and activity. The biotic and abiotic complexity of the soil environment hampers the extrapolation of the production and suppressing activity of mVOCs by microbial isolates on artificial growth media. Yet, several pathogen suppressive mVOCs produced by pure cultures do also occur in soil atmospheres. Therefore, an integration of lab and field studies on the production of mVOCs is needed to understand and predict the composition and dynamics of mVOCs in soil atmospheres. This knowledge, together with the knowledge of the chemistry and physical behaviour of mVOCs in soils, forms the basis for the development of sustainable management strategies to enhance the natural control of soil-borne pathogens with mVOCs. Possibilities for the mVOC-based control of soil-borne pathogens are discussed.
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http://dx.doi.org/10.1093/femsec/fiz105DOI Listing
August 2019

Root traits and belowground herbivores relate to plant-soil feedback variation among congeners.

Nat Commun 2019 04 5;10(1):1564. Epub 2019 Apr 5.

Laboratory of Nematology, Wageningen University, PO Box 8123, Droevendaalsesteeg, 16700 ES, Wageningen, The Netherlands.

Plant-soil feedbacks contribute to vegetation dynamics by species-specific interactions between plants and soil biota. Variation in plant-soil feedbacks can be predicted by root traits, successional position, and plant nativeness. However, it is unknown whether closely related plant species develop more similar plant-soil feedbacks than more distantly related species. Where previous comparisons included plant species from distant phylogenetic positions, we studied plant-soil feedbacks of congeneric species. Using eight intra-continentally range-expanding and native Geranium species, we tested relations between phylogenetic distances, chemical and structural root traits, root microbiomes, and plant-soil feedbacks. We show that root chemistry and specific root length better predict bacterial and fungal community composition than phylogenetic distance. Negative plant-soil feedback strength correlates with root-feeding nematode numbers, whereas microbiome dissimilarity, nativeness, or phylogeny does not predict plant-soil feedbacks. We conclude that root microbiome variation among congeners is best explained by root traits, and that root-feeding nematode abundances predict plant-soil feedbacks.
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http://dx.doi.org/10.1038/s41467-019-09615-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6450911PMC
April 2019

Biological activities associated with the volatile compound 2,5-bis(1-methylethyl)-pyrazine.

FEMS Microbiol Lett 2019 02;366(3)

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), PO BOX 50, 6700 AB Wageningen, the Netherlands.

Pyrazines are 1,4-diazabenzene-based volatile organic compounds and known for their broad-spectrum antimicrobial activity. In the present study, we assessed the antimicrobial activity of 2,5-bis(1-methylethyl)-pyrazine, produced by Paenibacillus sp. AD87 during co-culture with Burkholderia sp. AD24. In addition, we were using transcriptional reporter assays in E. coli and mammalian cells to decipher the possible mode of action. Bacterial and mammalian luciferase reporter strains were deployed to elucidate antimicrobial and toxicological effects of 2,5-bis(1-methylethyl)-pyrazine. At high levels of exposure, 2,5-bis(1-methylethyl)-pyrazine exerted strong DNA damage response. At lower concentrations, cell-wall damage response was observed. The activity was corroborated by a general toxicity reporter assay in E. coli ΔampD, defective in peptidoglycan turnover. The maximum E. coli cell-wall stress activity was measured at a concentration close to the onset of the mammalian cytotoxicity, while other adverse outcome pathways, such as the activation of aryl hydrocarbon and estrogenic receptor, the p53 tumour suppressor and the oxidative stress-related Nrf2 transcription factor, were induced at elevated concentrations compared to the response of mammalian cells. Because of its broad-spectrum antimicrobial activity at lower concentrations and the relatively low mammalian toxicity, 2,5-bis(1-methylethyl)-pyrazine is a potential bio-based fumigant with possible applications in food industry, agriculture or logistics.
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http://dx.doi.org/10.1093/femsle/fnz023DOI Listing
February 2019

Macro- and micro- plastics in soil-plant system: Effects of plastic mulch film residues on wheat (Triticum aestivum) growth.

Sci Total Environ 2018 Dec 20;645:1048-1056. Epub 2018 Jul 20.

Soil Physics and Land Management Group, Wageningen University & Research, Droevendaalsesteeg 4, 6708PB Wageningen, the Netherlands.

Plastic residues have become a serious environmental problem in the regions with intensive use of plastic mulching. Even though plastic mulch is widely used, the effects of macro- and micro- plastic residues on the soil-plant system and the agroecosystem are largely unknown. In this study, low density polyethylene and one type of starch-based biodegradable plastic mulch film were selected and used as examples of macro- and micro- sized plastic residues. A pot experiment was performed in a climate chamber to determine what effect mixing 1% concentration of residues of these plastics with sandy soil would have on wheat growth in the presence and absence of earthworms. The results showed that macro- and micro- plastic residues affected both above-ground and below-ground parts of the wheat plant during both vegetative and reproductive growth. The type of plastic mulch films used had a strong effect on wheat growth with the biodegradable plastic mulch showing stronger negative effects as compared to polyethylene. The presence of earthworms had an overall positive effect on the wheat growth and chiefly alleviated the impairments made by plastic residues.
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http://dx.doi.org/10.1016/j.scitotenv.2018.07.229DOI Listing
December 2018

LAESI mass spectrometry imaging as a tool to differentiate the root metabolome of native and range-expanding plant species.

Planta 2018 Dec 23;248(6):1515-1523. Epub 2018 Aug 23.

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

Main Conclusion: LAESI-MSI, an innovative high-throughput technique holds a unique potential for untargeted detection, profiling and spatial localization of metabolites from intact plant samples without need for extraction or extensive sample preparation. Our understanding of chemical diversity in biological samples has greatly improved through recent advances in mass spectrometry (MS). MS-based-imaging (MSI) techniques have further enhanced this by providing spatial information on the distribution of metabolites and their relative abundance. This study aims to employ laser-ablation electrospray ionization (LAESI) MSI as a tool to profile and compare the root metabolome of two pairs of native and range-expanding plant species. It has been proposed that successful range-expanding plant species, like introduced exotic invaders, have a novel, or a more diverse secondary chemistry. Although some tests have been made using aboveground plant materials, tests using root materials are rare. We tested the hypothesis that range-expanding plants possess more diverse root chemistries than native plant species. To examine the root chemistry of the selected plant species, LAESI-MSI was performed in positive ion mode and data were acquired in a mass range of m/z 50-1200 with a spatial resolution of 100 µm. The acquired data were analyzed using in-house scripts, and differences in the spatial profiles were studied for discriminatory mass features. The results revealed clear differences in the metabolite profiles amongst and within both pairs of congeneric plant species, in the form of distinct metabolic fingerprints. The use of ambient conditions and the fact that no sample preparation was required, established LAESI-MSI as an ideal technique for untargeted metabolomics and for direct correlation of the acquired data to the underlying metabolomic complexity present in intact plant samples.
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http://dx.doi.org/10.1007/s00425-018-2989-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6244666PMC
December 2018

Growth promotion and inhibition induced by interactions of groundwater bacteria.

FEMS Microbiol Ecol 2018 11;94(11)

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

Microorganisms can produce a plethora of secondary metabolites, some acting as signaling compounds and others as suppressing agents. As yet, the potential of groundwater microbes to produce antimicrobial compounds to increase their competitiveness against other bacteria has not been examined. In this study, we developed an AlamarBlue® based high-throughput screening method that allowed for a fast and highly standardized evaluation of both growth-inhibiting and -promoting metabolites. With this technique, 149 screened bacterial isolates were grown in monocultures and in 1402 co-cultures. Co-cultivation did not increase the frequency of growth inhibition against the two tested model organisms (Staphylococcus aureus 533R4 and Escherichia coli WA321) compared to monocultures. Mainly co-cultivation of Proteobacteria induced growth inhibition of both model organisms. Only slightly increased growth promotion of S. aureus 533R4 was observed. Growth-promoting effects on E. coli WA321 were observed by supernatants from co-cultures between Bacteroidetes and Firmicutes. With the standardized screening for both growth-inhibiting and -promoting effects, this method will enable further studies to elaborate and better understand complex inter-specific interactions and networks in aquatic communities as well as in other environments.
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http://dx.doi.org/10.1093/femsec/fiy164DOI Listing
November 2018

Deciphering the genome and secondary metabolome of the plant pathogen Fusarium culmorum.

FEMS Microbiol Ecol 2018 06;94(6)

Department of Microbial Ecology, Netherlands Institute of Ecology, Droevendaalsesteeg 10,6708 PB Wageningen, the Netherlands.

Fusarium culmorum is one of the most important fungal plant pathogens that causes diseases on a wide diversity of cereal and non-cereal crops. We report herein for the first time the genome sequence of F. culmorum strain PV and its associated secondary metabolome that plays a role in the interaction with other microorganisms and contributes to its pathogenicity on plants. The genome revealed the presence of two terpene synthases, trichodiene and longiborneol synthase, which generate an array of volatile terpenes. Furthermore, we identified two gene clusters, deoxynivalenol and zearalenone, which encode for the production of mycotoxins. Linking the production of mycotoxins with in vitro bioassays, we found high virulence of F. culmorum PV on maize, barley and wheat. By using ultra-performance liquid chromatography-mass spectrometry, we confirmed several compounds important for the behaviour and lifestyle of F. culmorum. This research sets the basis for future studies in microbe-plant interactions.
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http://dx.doi.org/10.1093/femsec/fiy078DOI 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

Calling from distance: attraction of soil bacteria by plant root volatiles.

ISME J 2018 05 22;12(5):1252-1262. Epub 2018 Jan 22.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), 6700 AB, Wageningen, The Netherlands.

Plants release a wide set of secondary metabolites including volatile organic compounds (VOCs). Many of those compounds are considered to function as defense against herbivory, pests, and pathogens. However, little knowledge exists about the role of belowground plant VOCs for attracting beneficial soil microorganisms. We developed an olfactometer system to test the attraction of soil bacteria by VOCs emitted by Carex arenaria roots. Moreover, we tested whether infection of C. arenaria with the fungal pathogen Fusarium culmorum modifies the VOCs profile and bacterial attraction. The results revealed that migration of distant bacteria in soil towards roots can be stimulated by plant VOCs. Upon fungal infection, the blend of root VOCs changed and specific bacteria with antifungal properties were attracted. Tests with various pure VOCs indicated that those compounds can diffuse over long distance but with different diffusion abilities. Overall, this work highlights the importance of plant VOCs in belowground long-distance plant-microbe interactions.
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http://dx.doi.org/10.1038/s41396-017-0035-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5931972PMC
May 2018

The effect of isabelin, a sesquiterpene lactone from Ambrosia artemisiifolia on soil microorganisms and human pathogens.

FEMS Microbiol Lett 2018 02;365(4)

Netherlands Institute of Ecology (NIOO-KNAW), Department of Microbial Ecology, PO BOX 50, 6700 AB Wageningen, The Netherlands.

Ambrosia artemisiifolia L. (common ragweed) is an invasive weed, which is well known for the strong allergenic effect of its pollen as well as for its invasiveness and impact in crop fields (e.g. causing yield losses). This species produces a broad range of sesquiterpenoids. In recent years, new bioactive molecules have been discovered in this plant, e.g. isabelin, a sesquiterpene dilactone. The bioactivity of isabelin has been already demonstrated on allergy-related receptors and its inhibitory effect on seeds of various plant species. Isabelin was tested for potential antimicrobial effects by using a selection of soil-borne bacteria and fungi and three human pathogens as model organisms. For the majority of microorganisms tested, no antimicrobial activity of isabelin was observed. However, isabelin revealed strong antimicrobial activity against the Gram-positive soil bacterium Paenibacillus sp. and against the Gram-positive, multidrug-resistant Staphylococcus aureus. The observed inhibitory activity of isabelin can enlighten the importance to study similar compounds for their effect on human pathogens and on soil and rhizosphere microorganisms.
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http://dx.doi.org/10.1093/femsle/fny001DOI Listing
February 2018

Microbial Volatiles: Small Molecules with an Important Role in Intra- and Inter-Kingdom Interactions.

Front Microbiol 2017 12;8:2484. Epub 2017 Dec 12.

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

During the last decades, research on the function of volatile organic compounds focused primarily on the interactions between plants and insects. However, microorganisms can also release a plethora of volatiles and it appears that microbial volatile organic compounds (mVOCs) can play an important role in intra- and inter-kingdom interactions. So far, most studies are focused on aboveground volatile-mediated interactions and much less information is available about the function of volatiles belowground. This minireview summarizes the current knowledge on the biological functions of mVOCs with the focus on mVOCs-mediated interactions belowground. We pinpointed mVOCs involved in microbe-microbe and microbe-plant interactions, and highlighted the ecological importance of microbial terpenes as a largely underexplored group of mVOCs. We indicated challenges in studying belowground mVOCs-mediated interactions and opportunities for further studies and practical applications.
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http://dx.doi.org/10.3389/fmicb.2017.02484DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5733050PMC
December 2017

Decay of low-density polyethylene by bacteria extracted from earthworm's guts: A potential for soil restoration.

Sci Total Environ 2018 May 27;624:753-757. Epub 2017 Dec 27.

Netherlands Institute of Ecology (NIOO-KNAW), Department of Microbial Ecology, 6700 AB Wageningen, The Netherlands.

Low-density polyethylene (LDPE) is the most abundant source of microplastic pollution worldwide. A recent study found that LDPE decay was increased and the size of the plastic was decreased after passing through the gut of the earthworm Lumbricus terrestris (Oligochaeta). Here, we investigated the involvement of earthworm gut bacteria in the microplastic decay. The bacteria isolated from the earthworm's gut were Gram-positive, belonging to phylum Actinobacteria and Firmicutes. These bacteria were used in a short-term microcosm experiment performed with gamma-sterilized soil with or without LDPE microplastics (MP). We observed that the LDPE-MP particle size was significantly reduced in the presence of bacteria. In addition, the volatile profiles of the treatments were compared and clear differences were detected. Several volatile compounds such as octadecane, eicosane, docosane and tricosane were measured only in the treatments containing both bacteria and LDPE-MP, indicating that these long-chain alkanes are byproducts of bacterial LDPE-MP decay.
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http://dx.doi.org/10.1016/j.scitotenv.2017.12.144DOI Listing
May 2018

Belowground Plant-Herbivore Interactions Vary among Climate-Driven Range-Expanding Plant Species with Different Degrees of Novel Chemistry.

Front Plant Sci 2017 25;8:1861. Epub 2017 Oct 25.

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

An increasing number of studies report plant range expansions to higher latitudes and altitudes in response to global warming. However, consequences for interactions with other species in the novel ranges are poorly understood. Here, we examine how range-expanding plant species interact with root-feeding nematodes from the new range. Root-feeding nematodes are ubiquitous belowground herbivores that may impact the structure and composition of natural vegetation. Because of their ecological novelty, we hypothesized that range-expanding plant species will be less suitable hosts for root-feeding nematodes than native congeneric plant species. In greenhouse and lab trials we compared nematode preference and performance of two root-feeding nematode species between range-expanding plant species and their congeneric natives. In order to understand differences in nematode preferences, we compared root volatile profiles of all range-expanders and congeneric natives. Nematode preferences and performances differed substantially among the pairs of range-expanders and natives. The range-expander that had the most unique volatile profile compared to its related native was unattractive and a poor host for nematodes. Other range-expanding plant species that differed less in root chemistry from native congeners, also differed less in nematode attraction and performance. We conclude that the three climate-driven range-expanding plant species studied varied considerably in their chemical novelty compared to their congeneric natives, and therefore affected native root-feeding nematodes in species-specific ways. Our data suggest that through variation in chemical novelty, range-expanding plant species may vary in their impacts on belowground herbivores in the new range.
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http://dx.doi.org/10.3389/fpls.2017.01861DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5660973PMC
October 2017

Exploring bacterial interspecific interactions for discovery of novel antimicrobial compounds.

Microb Biotechnol 2017 07 29;10(4):910-925. Epub 2017 May 29.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), PO BOX 50, 6700 AB, Wageningen, The Netherlands.

Recent studies indicated that the production of secondary metabolites by soil bacteria can be triggered by interspecific interactions. However, little is known to date about interspecific interactions between Gram-positive and Gram-negative bacteria. In this study, we aimed to understand how the interspecific interaction between the Gram-positive Paenibacillus sp. AD87 and the Gram-negative Burkholderia sp. AD24 affects the fitness, gene expression and the production of soluble and volatile secondary metabolites of both bacteria. To obtain better insight into this interaction, transcriptome and metabolome analyses were performed. Our results revealed that the interaction between the two bacteria affected their fitness, gene expression and the production of secondary metabolites. During interaction, the growth of Paenibacillus was not affected, whereas the growth of Burkholderia was inhibited at 48 and 72 h. Transcriptome analysis revealed that the interaction between Burkholderia and Paenibacillus caused significant transcriptional changes in both bacteria as compared to the monocultures. The metabolomic analysis revealed that the interaction increased the production of specific volatile and soluble antimicrobial compounds such as 2,5-bis(1-methylethyl)-pyrazine and an unknown Pederin-like compound. The pyrazine volatile compound produced by Paenibacillus was subjected to bioassays and showed strong inhibitory activity against Burkholderia and a range of plant and human pathogens. Moreover, strong additive antimicrobial effects were observed when soluble extracts from the interacting bacteria were combined with the pure 2,5-bis(1-methylethyl)-pyrazine. The results obtained in this study highlight the importance to explore bacterial interspecific interactions to discover novel secondary metabolites and to perform simultaneously metabolomics of both, soluble and volatile compounds.
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http://dx.doi.org/10.1111/1751-7915.12735DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5481530PMC
July 2017

Fungal volatile compounds induce production of the secondary metabolite Sodorifen in Serratia plymuthica PRI-2C.

Sci Rep 2017 04 13;7(1):862. Epub 2017 Apr 13.

Netherlands Institute of Ecology (NIOO-KNAW), Department of Microbial Ecology, 6700 AB, Wageningen, The Netherlands.

The ability of bacteria and fungi to communicate with each other is a remarkable aspect of the microbial world. It is recognized that volatile organic compounds (VOCs) act as communication signals, however the molecular responses by bacteria to fungal VOCs remain unknown. Here we perform transcriptomics and proteomics analyses of Serratia plymuthica PRI-2C exposed to VOCs emitted by the fungal pathogen Fusarium culmorum. We find that the bacterium responds to fungal VOCs with changes in gene and protein expression related to motility, signal transduction, energy metabolism, cell envelope biogenesis, and secondary metabolite production. Metabolomic analysis of the bacterium exposed to the fungal VOCs, gene cluster comparison, and heterologous co-expression of a terpene synthase and a methyltransferase revealed the production of the unusual terpene sodorifen in response to fungal VOCs. These results strongly suggest that VOCs are not only a metabolic waste but important compounds in the long-distance communication between fungi and bacteria.
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http://dx.doi.org/10.1038/s41598-017-00893-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5429845PMC
April 2017

The antimicrobial volatile power of the rhizospheric isolate Pseudomonas donghuensis P482.

PLoS One 2017 30;12(3):e0174362. Epub 2017 Mar 30.

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

Soil and rhizosphere bacteria produce an array of secondary metabolites including a wide range of volatile organic compounds (VOCs). These compounds play an important role in the long-distance interactions and communication between (micro)organisms. Furthermore, bacterial VOCs are involved in plant pathogens inhibition and induction of soil fungistasis and suppressivenes. In the present study, we analysed the volatile blend emitted by the rhizospheric isolate Pseudomonas donghuensis P482 and evaluated the volatile effect on the plant pathogenic fungi and bacteria as well as one oomycete. Moreover, we investigated the role of the GacS/GacA system on VOCs production in P. donghuensis P482. The results obtained demonstrated that VOCs emitted by P. donghuensis P482 have strong antifungal and antioomycete, but not antibacterial activity. The production of certain volatiles such as dimethyl sulfide, S-methyl thioacetate, methyl thiocyanate, dimethyl trisulfide, 1-undecan and HCN is depended on the GacS/GacA two-component regulatory system. Apparently, these compounds play an important role in the pathogens suppression as the gacA mutant entirely lost the ability to inhibit via volatiles the growth of tested plant pathogens.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0174362PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5373542PMC
August 2017

Editorial: Smelly Fumes: Volatile-Mediated Communication between Bacteria and Other Organisms.

Front Microbiol 2016 20;7:2031. Epub 2016 Dec 20.

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

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http://dx.doi.org/10.3389/fmicb.2016.02031DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5168464PMC
December 2016

The Ecological Role of Volatile and Soluble Secondary Metabolites Produced by Soil Bacteria.

Trends Microbiol 2017 04 27;25(4):280-292. Epub 2016 Dec 27.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), PO Box 50, 6700 AB, Wageningen, The Netherlands. Electronic address:

The rich diversity of secondary metabolites produced by soil bacteria has been appreciated for over a century, and advances in chemical analysis and genome sequencing continue to greatly advance our understanding of this biochemical complexity. However, we are just at the beginning of understanding the physicochemical properties of bacterial metabolites, the factors that govern their production and ecological roles. Interspecific interactions and competitor sensing are among the main biotic factors affecting the production of bacterial secondary metabolites. Many soil bacteria produce both volatile and soluble compounds. In contrast to soluble compounds, volatile organic compounds can diffuse easily through air- and gas-filled pores in the soil and likely play an important role in long-distance microbial interactions. In this review we provide an overview of the most important soluble and volatile classes of secondary metabolites produced by soil bacteria, their ecological roles, and their possible synergistic effects.
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http://dx.doi.org/10.1016/j.tim.2016.12.002DOI Listing
April 2017

Validation of the AlamarBlue® Assay as a Fast Screening Method to Determine the Antimicrobial Activity of Botanical Extracts.

PLoS One 2016 29;11(12):e0169090. Epub 2016 Dec 29.

Instituto de Biología Molecular y Celular (IBMC), Universidad Miguel Hernández (UMH), Avenida de la Universidad s/n, E-03202 Elche, Alicante, Spain.

Plant compounds are a potential source of new antimicrobial molecules against a variety of infections. Plant extracts suppose complex phytochemical libraries that may be used for the first stages of the screening process for antimicrobials. However, their large variability and complexity require fast and inexpensive methods that allow a rapid and adequate screening for antimicrobial activity against a variety of bacteria and fungi. In this study, a multi-well plate assay using the AlamarBlue® fluorescent dye was applied to screen for antimicrobial activity of several botanical extracts and the data were correlated with microbial colony forming units (CFU). This correlation was performed for three pathogenic model microorganisms: Escherichia coli (Gram negative bacteria), Staphylococcus aureus (Gram positive bacteria) and for the yeast-like fungi Candida albicans. A total of ten plant extracts from different Mediterranean plants, including several Cistus and Hibiscus species, were successfully tested. HPLC-DAD-ESI-MS/MS analysis was utilized for the characterization of the extracts in order to establish structure-activity correlations. The results show that extracts enriched in ellagitannins and flavonols are promising antibacterial agents against both Gram positive and Gram negative bacteria. In contrast, phenolic acids, anthocyanidins and flavonols may be related to the observed antifungal activity.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0169090PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5199036PMC
July 2017