Publications by authors named "Ales Svatos"

165 Publications

An Integrated-Omics/Chemistry Approach Unravels Enzymatic and Spontaneous Steps to Form Flavoalkaloidal Nudicaulin Pigments in Flowers of L.

Int J Mol Sci 2021 Apr 16;22(8). Epub 2021 Apr 16.

Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, D-07745 Jena, Germany.

Flower colour is an important trait for plants to attract pollinators and ensure their reproductive success. Among yellow flower pigments, the nudicaulins in L. (Iceland poppy) are unique due to their rarity and unparalleled flavoalkaloid structure. Nudicaulins are derived from pelargonidin glycoside and indole, products of the flavonoid and indole/tryptophan biosynthetic pathway, respectively. To gain insight into the molecular and chemical basis of nudicaulin biosynthesis, we combined transcriptome, differential gel electrophoresis (DIGE)-based proteome, and ultra-performance liquid chromatography-high resolution mass spectrometry (UPLC-HRMS)-based metabolome data of petals with chemical investigations. We identified candidate genes and proteins for all biosynthetic steps as well as some key metabolites across five stages of petal development. Candidate genes of amino acid biosynthesis showed a relatively stable expression throughout petal development, whereas most candidate genes of flavonoid biosynthesis showed increasing expression during development followed by downregulation in the final stage. Notably, gene candidates of indole-3-glycerol-phosphate lyase (IGL), sharing characteristic sequence motifs with known plant IGL genes, were co-expressed with flavonoid biosynthesis genes, and are probably providing free indole. The fusion of indole with pelargonidin glycosides was retraced synthetically and promoted by high precursor concentrations, an excess of indole, and a specific glycosylation pattern of pelargonidin. Thus, nudicaulin biosynthesis combines the enzymatic steps of two different pathways with a spontaneous fusion of indole and pelargonidin glycoside under precisely tuned reaction conditions.
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http://dx.doi.org/10.3390/ijms22084129DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8073789PMC
April 2021

Incipient genome erosion and metabolic streamlining for antibiotic production in a defensive symbiont.

Proc Natl Acad Sci U S A 2021 Apr;118(17)

Research Group Insect Symbiosis, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany;

Genome erosion is a frequently observed result of relaxed selection in insect nutritional symbionts, but it has rarely been studied in defensive mutualisms. Solitary beewolf wasps harbor an actinobacterial symbiont of the genus that provides protection to the developing offspring against pathogenic microorganisms. Here, we characterized the genomic architecture and functional gene content of this culturable symbiont using genomics, transcriptomics, and proteomics in combination with in vitro assays. Despite retaining a large linear chromosome (7.3 Mb), the wasp symbiont accumulated frameshift mutations in more than a third of its protein-coding genes, indicative of incipient genome erosion. Although many of the frameshifted genes were still expressed, the encoded proteins were not detected, indicating post-transcriptional regulation. Most pseudogenization events affected accessory genes, regulators, and transporters, but "" also experienced mutations in central metabolic pathways, resulting in auxotrophies for biotin, proline, and arginine that were confirmed experimentally in axenic culture. In contrast to the strong A+T bias in the genomes of most obligate symbionts, we observed a significant G+C enrichment in regions likely experiencing reduced selection. Differential expression analyses revealed that-compared to in vitro symbiont cultures-"" in beewolf antennae showed overexpression of genes for antibiotic biosynthesis, the uptake of host-provided nutrients and the metabolism of building blocks required for antibiotic production. Our results show unusual traits in the early stage of genome erosion in a defensive symbiont and suggest tight integration of host-symbiont metabolic pathways that effectively grants the host control over the antimicrobial activity of its bacterial partner.
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http://dx.doi.org/10.1073/pnas.2023047118DOI Listing
April 2021

Sexual deception of a beetle pollinator through floral mimicry.

Curr Biol 2021 Mar 19. Epub 2021 Mar 19.

Centre for Functional Biodiversity, School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Pietermaritzburg 3209, South Africa. Electronic address:

Sexual mimicry is a complex multimodal strategy used by some plants to lure insects to flowers for pollination. It is notable for being highly species-specific and is typically mediated by volatiles belonging to a restricted set of chemical compound classes. Well-documented cases involve exploitation of bees and wasps (Hymenoptera) and flies (Diptera). Although beetles (Coleoptera) are the largest insect order and are well known as pollinators of both early and modern plants, it has been unclear whether they are sexually deceived by plants during flower visits. Here we report the discovery of an unambiguous case of sexual deception of a beetle: male longhorn beetles (Chorothyse hessei, Cerambycidae) pollinate the elaborate insectiform flowers of a rare southern African orchid (Disa forficaria), while exhibiting copulatory behavior including biting the antennae-like petals, curving the abdomen into the hairy lip cleft, and ejaculating sperm. The beetles are strongly attracted by (16S,9Z)-16-ethyl hexadec-9-enolide, a novel macrolide that we isolated from the floral scent. Structure-activity studies confirmed that chirality and other aspects of the structural geometry of the macrolide are critical for the attraction of the male beetles. These results demonstrate a new biological function for plant macrolides and confirm that beetles can be exploited through sexual deception to serve as pollinators.
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http://dx.doi.org/10.1016/j.cub.2021.03.037DOI Listing
March 2021

Cobamide remodeling in the freshwater microalga Chlamydomonas reinhardtii.

FEMS Microbiol Lett 2020 Nov;367(20)

Research Group Anaerobic Microbiology, Institute of Microbiology, Friedrich Schiller University, Philosophenweg 12, D-07743 Jena, Germany.

Microalgae are not able to produce cobamides (Cbas, B12 vitamers) de novo. Hence, the production of catalytically active Cba-containing methionine synthase (MetH), which is present in selected representatives, is dependent on the availability of exogenous B12 vitamers. Preferences in the utilization of exogenous Cbas equipped with either adenine or 5,6-dimethylbenzimidazole as lower base have been reported for some microalgae. Here, we investigated the utilization of norcobamides (NorCbas) for growth by the Cba-dependent Chlamydomonas reinhardtii mutant strain (ΔmetE). The growth yields in the presence of NorCbas were lower in comparison to those achieved with Cbas. NorCbas lack a methyl group in the linker moiety of the nucleotide loop. C. reinhardtii was also tested for the remodeling of NorCbas (e.g. adeninyl-norcobamide) in the presence of different benzimidazoles. Extraction of the NorCbas from C. reinhardtii, their purification, and identification confirmed the exchange of the lower base of the vitamers. However, the linker moiety of the NorCbas nucleotide loop was not exchanged. This observation strongly indicates the presence of an alternative mode of Cba deconstruction in C. reinhardtii that differs from the amidohydrolase (CbiZ)-dependent pathway described in Cba-remodeling bacteria and archaea.
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http://dx.doi.org/10.1093/femsle/fnaa171DOI Listing
November 2020

Mate discrimination among subspecies through a conserved olfactory pathway.

Sci Adv 2020 Jun 17;6(25):eaba5279. Epub 2020 Jun 17.

Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, D-07745 Jena, Germany.

Communication mechanisms underlying the sexual isolation of species are poorly understood. Using four subspecies of as a model, we identify two behaviorally active, male-specific pheromones. One functions as a conserved male antiaphrodisiac in all subspecies and acts via gustation. The second induces female receptivity via olfaction exclusively in the two subspecies that produce it. Genetic analysis of the cognate receptor for the olfactory pheromone indicates an important role for this sensory pathway in promoting sexual isolation of subspecies, in combination with auditory signals. Unexpectedly, the peripheral sensory pathway detecting this pheromone is conserved molecularly, physiologically, and anatomically across subspecies. These observations imply that subspecies-specific behaviors arise from differential interpretation of the same peripheral cue, reminiscent of sexually conserved detection but dimorphic interpretation of male pheromones in . Our results reveal that, during incipient speciation, pheromone production, detection, and interpretation do not necessarily evolve in a coordinated manner.
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http://dx.doi.org/10.1126/sciadv.aba5279DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7360436PMC
June 2020

Canditate metabolites for ash dieback tolerance in Fraxinus excelsior.

J Exp Bot 2020 10;71(19):6074-6083

Forestry Development Department, Teagasc, Dublin, Ireland.

Ash dieback, a forest epidemic caused by the invasive fungus Hymenoscyphus fraxineus, threatens ash trees throughout Europe. Within Fraxinus excelsior populations, a small proportion of genotypes show a low susceptibility to the pathogen. We compared the metabolomes from a cohort of low-susceptibility ash genotypes with a cohort of high-susceptibility ash genotypes. This revealed two significantly different chemotypes. A total of 64 candidate metabolites associated with reduced or increased susceptibility in the chemical families secoiridoids, coumarins, flavonoids, phenylethanoids, and lignans. Increased levels of two coumarins, fraxetin and esculetin, were strongly associated with reduced susceptibility to ash dieback. Both coumarins inhibited the growth of H. fraxineus in vitro when supplied at physiological concentrations, thereby validating their role as markers for low susceptibility to ash dieback. Similarly, fungal growth inhibition was observed when the methanolic bark extract of low-susceptibility ash genotypes was supplied. Our findings indicate the presence of constitutive chemical defense barriers against ash dieback in ash.
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http://dx.doi.org/10.1093/jxb/eraa306DOI Listing
October 2020

Desaturase specificity is controlled by the physicochemical properties of a single amino acid residue in the substrate binding tunnel.

Comput Struct Biotechnol J 2020 14;18:1202-1209. Epub 2020 May 14.

Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Flemingovo n., 2, 166 10 Prague 6, Czech Republic.

Membrane fatty acyl desaturases (mFAD) are ubiquitous enzymes in eukaryotes. They introduce double bonds into fatty acids (FAs), producing structurally diverse unsaturated FAs which serve as membrane lipid components or precursors of signaling molecules. The mechanisms controlling enzymatic specificity and selectivity of desaturation are, however, poorly understood. We found that the physicochemical properties, particularly side chain volume, of a single amino acid (aa) residue in insect mFADs (Lepidoptera: and ) control the desaturation products. Molecular dynamics simulations of systems comprising wild-type or mutant mFADs with fatty acyl-CoA substrates revealed that the single aa substitution likely directs the outcome of the desaturation reaction by modulating the distance between substrate fatty acyl carbon atoms and active center metal ions. These findings, as well as our methodology combining mFAD mutational screening with molecular dynamics simulations, will facilitate prediction of desaturation products and facilitate engineering of mFADs for biotechnological applications.
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http://dx.doi.org/10.1016/j.csbj.2020.05.011DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7283083PMC
May 2020

The Anti-Inflammatory and Antimicrobial Potential of Selected Ethnomedicinal Plants from Sri Lanka.

Molecules 2020 Apr 20;25(8). Epub 2020 Apr 20.

Department of Pharmaceutical/Medicinal Chemistry, Institute of Pharmacy, Friedrich-Schiller-University Jena, 07743 Jena, Germany.

Traditional folk medicine in Sri Lanka is mostly based on plants and plant-derived products, however, many of these medicinal plant species are scientifically unexplored. Here, we evaluated the anti-inflammatory and antimicrobial potency of 28 different extracts prepared from seven popular medicinal plant species employed in Sri Lanka. The extracts were subjected to cell-based and cell-free assays of 5-lipoxygenase (5-LO), microsomal prostaglandin E synthase (mPGES)-1, and nitric oxide (NO) scavenging activity. Moreover, antibacterial and disinfectant activities were assessed. Characterization of secondary metabolites was achieved by gas chromatography coupled to mass spectrometric (GC-MS) analysis. -Hexane- and dichloromethane-based extracts of efficiently suppressed 5-LO activity in human neutrophils (IC = 0.92 and 1.39 µg/mL), and potently inhibited isolated human 5-LO (IC = 0.15 and 0.16 µg/mL) and mPGES-1 (IC = 0.29 and 0.49 µg/mL). Lipophilic extracts of displayed potent inhibition of mPGES-1 only. A methanolic extract of caused significant NO scavenging activity. The lipophilic extracts of exhibited prominent antibacterial and disinfectant activities, and GC-MS analysis revealed the presence of fatty acids, sesquiterpenes and other types of secondary metabolites. Together, our results suggest the prospective utilization of as disinfective agent with potent anti-inflammatory properties.
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http://dx.doi.org/10.3390/molecules25081894DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7221831PMC
April 2020

Response of the wood-decay fungus Schizophyllum commune to co-occurring microorganisms.

PLoS One 2020 23;15(4):e0232145. Epub 2020 Apr 23.

Institute of Microbiology, Friedrich Schiller University, Jena, Germany.

Microorganisms are constantly interacting in a given environment by a constant exchange of signaling molecules. In timber, wood-decay fungi will come into contact with other fungi and bacteria. In naturally bleached wood, dark, pigmented lines arising from confrontation of two fungi often hint at such interactions. The metabolites (and pigment) exchange was investigated using the lignicolous basidiomycete Schizophyllum commune, and co-occurring fungi and bacteria inoculated directly on sterilized wood, or on media. In interactions with competitive wood degrading fungi, yeasts or bacteria, different competition strategies and communication types were observed, and stress reactions, as well as competitor-induced enzymes or pigments were analyzed. Melanin, indole, flavonoids and carotenoids were shown to be induced in S. commune interactions. The induced genes included multi-copper oxidases lcc1, lcc2, mco1, mco2, mco3 and mco4, possibly involved in both pigment production and lignin degradation typical for wood bleaching by wood-decay fungi.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0232145PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7179906PMC
July 2020

Author Correction: The oomycete Lagenisma coscinodisci hijacks host alkaloid synthesis during infection of a marine diatom.

Nat Commun 2020 Mar 31;11(1):1698. Epub 2020 Mar 31.

Research Group Plankton Community Interaction, Max Planck Institute for Chemical Ecology, Jena, Germany.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41467-020-15527-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7109102PMC
March 2020

Editorial: Single Plant Cell Metabolomics.

Front Plant Sci 2020 2;11:161. Epub 2020 Mar 2.

Department of Chemistry & Biochemistry, University of Oklahoma, Norman, OK, United States.

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http://dx.doi.org/10.3389/fpls.2020.00161DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7061530PMC
March 2020

Identification to species level of live single microalgal cells from plankton samples with matrix-free laser/desorption ionization mass spectrometry.

Metabolomics 2020 02 24;16(3):28. Epub 2020 Feb 24.

Max Planck Institute for Chemical Ecology, Max Planck Fellow Group On Plankton Community Interaction, Hans-Knöll-Str. 8, 07745, Jena, Germany.

Introduction: Marine planktonic communities are complex microbial consortia often dominated by microscopic algae. The taxonomic identification of individual phytoplankton cells usually relies on their morphology and demands expert knowledge. Recently, a live single-cell mass spectrometry (LSC-MS) pipeline was developed to generate metabolic profiles of microalgae.

Objective: Taxonomic identification of diverse microalgal single cells from collection strains and plankton samples based on the metabolic fingerprints analyzed with matrix-free laser desorption/ionization high-resolution mass spectrometry.

Methods: Matrix-free atmospheric pressure laser-desorption ionization mass spectrometry was performed to acquire single-cell mass spectra from collection strains and prior identified environmental isolates. The computational identification of microalgal species was performed by spectral pattern matching (SPM). Three similarity scores and a bootstrap-derived confidence score were evaluated in terms of their classification performance. The effects of high and low-mass resolutions on the classification success were evaluated.

Results: Several hundred single-cell mass spectra from nine genera and nine species of marine microalgae were obtained. SPM enabled the identification of single cells at the genus and species level with high accuracies. The receiver operating characteristic (ROC) curves indicated a good performance of the similarity measures but were outperformed by the bootstrap-derived confidence scores.

Conclusion: This is the first study to solve taxonomic identification of microalgae based on the metabolic fingerprints of the individual cell using an SPM approach.
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http://dx.doi.org/10.1007/s11306-020-1646-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7036359PMC
February 2020

The oomycete Lagenisma coscinodisci hijacks host alkaloid synthesis during infection of a marine diatom.

Nat Commun 2019 10 30;10(1):4938. Epub 2019 Oct 30.

Research Group Plankton Community Interaction, Max Planck Institute for Chemical Ecology, Jena, Germany.

Flagellated oomycetes frequently infect unicellular algae, thus limiting their proliferation. Here we show that the marine oomycete Lagenisma coscinodisci rewires the metabolome of the bloom-forming diatom Coscinodiscus granii, thereby promoting infection success. The algal alkaloids β-carboline and 4-carboxy-2,3,4,9-tetrahydro-1H-β-carboline are induced during infection. Single-cell profiling with AP-MALDI-MS and confocal laser scanning microscopy reveals that algal carbolines accumulate in the reproductive form of the parasite. The compounds arrest the algal cell division, increase the infection rate and induce plasmolysis in the host. Our results indicate that the oomycete manipulates the host metabolome to support its own multiplication.
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http://dx.doi.org/10.1038/s41467-019-12908-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6821873PMC
October 2019

Applications of MicroArrays for Mass Spectrometry (MAMS) in Single-Cell Metabolomics.

Methods Mol Biol 2020 ;2064:73-88

Research Group Mass Spectrometry, Max Planck Institute for Chemical Ecology, Jena, Germany.

The metabolic network is the endpoint in the flow of information that begins with the "gene" and ends with "phenotype" (observable function) of the cell. Previously, due to the variety of metabolites analyzed inside cells, the metabolomic measurements were performed with samples including multiple cells. Unfortunately, this sampling process may mask important metabolic phenomena, such as cell-to-cell heterogeneity. For these studies, we must use analytical techniques that can robustly deliver reproducible results with single-cell sensitivity. In this chapter, we summarize laser-based methods for single-cell analysis and a novel approach of MicroArrays for Mass Spectrometry (or MAMS) is described in full detail. This particular type of microarrays was tailored for the study of cells grown in liquid medium using multiple-analytical read-outs, such as optical and laser desorption/ionization (LDI) or MALDI mass spectrometry.
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http://dx.doi.org/10.1007/978-1-4939-9831-9_6DOI Listing
December 2020

Azadirachtin-A from Impacts Multiple Biological Targets in Cotton Bollworm .

ACS Omega 2019 May 31;4(5):9531-9541. Epub 2019 May 31.

Plant Molecular Biology Unit, Division of Biochemical Sciences and Division of Organic Chemistry, CSIR-National Chemical Laboratory, Dr. Homi Bhabha Road, Pune 411008, Maharashtra, India.

Azadirachtin-A (AzaA) from the Indian neem tree () has insecticidal properties; however, its molecular mechanism remains elusive. The "targeted and nontargeted proteomic profiling", metabolomics, matrix-assisted laser desorption/ionization time of flight (MALDI-TOF) imaging, gene expression, and in silico analysis provided clues about its action on . Fourth instar larvae fed on AzaA-based diet (AzaD) suffered from significant mortality, growth retardation, reduced larval mass, complications in molting, and prolonged development. Furthermore, death of AzaD-fed larvae was observed with various phenotypes like bursting, blackening, and half-molting. Liquid chromatography-mass spectrometry (LC-MS) data showed limited catabolic processing of ingested AzaA and dramatic alternations of primary metabolism in . MALDI-TOF imaging indicated the presence of AzaA in midgut of . In the gut, out of 79 proteins identified, 34 were upregulated, which were related to digestion, immunity, energy production, and apoptosis mechanism. On the other hand, 45 proteins were downregulated, including those from carbohydrate metabolism, lipid metabolism, and energy transfer. In the hemolymph, 21 upregulated proteins were reported to be involved in immunity, RNA processing, and mRNA-directed protein synthesis, while 7 downregulated proteins were implicated in energy transfer, hydrolysis, lipid metabolism, defense mechanisms, and amino acid storage-related functions. Subsequently, six target proteins were identified using labeled AzaA that interacted with whole insect proteins. In silico analysis suggests that AzaA could be efficiently accommodated in the hydrophobic pocket of juvenile hormone esterase and showed strong interaction with active site residues, indicating plausible targets of AzaA in . Quantitative polymerase chain reaction analysis suggested differential gene expression patterns and partly corroborated the proteomic results. Overall, data suggest that AzaA generally targets more than one protein in and hence could be a potent biopesticide.
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http://dx.doi.org/10.1021/acsomega.8b03479DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6648242PMC
May 2019

Plant-Based Natural Product Chemistry for Integrated Pest Management of Drosophila suzukii.

J Chem Ecol 2019 Jul 1;45(7):626-637. Epub 2019 Jul 1.

Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, D-07745, Jena, Germany.

Since the first reports of damage by Drosophila suzukii, the spotted-wing Drosophila (SWD), over a decade ago in Europe, widespread efforts have been made to understand both the ecology and the evolution of this insect pest, especially due to its phylogenetic proximity to one of the original model organisms, D. melanogaster. In addition, researchers have sought to find economically viable solutions for the monitoring and management of this agricultural pest, which has now swept across much of Europe, North America and Asia. In a new direction of study, we present an investigation of plant-based chemistry, where we search for natural compounds that are structurally similar to known olfactory cues from parasitoid wasps that in turn are well-described ovipositional avoidance cues for many Drosophila species. Here we test 11 plant species across two plant genera, Nepeta and Actinidia, and while we find iridoid compounds in both, only those odorants from Actinidia are noted to be detected by the insect antenna, and in addition, found to be behaviorally active. Moreover, the Actinidia extracts resulted in oviposition avoidance when they were added to fruit samples in the laboratory. Thus we propose the possible efficacy of these plants or their extracted chemistry as a novel means for establishing a cost-effective integrated pest management strategy towards the control of this pest fly.
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http://dx.doi.org/10.1007/s10886-019-01085-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6661260PMC
July 2019

Untargeted Metabolomics Approach Reveals Differences in Host Plant Chemistry Before and After Infestation With Different Pea Aphid Host Races.

Front Plant Sci 2019 28;10:188. Epub 2019 Feb 28.

Department of Biochemistry, Max-Planck Institute for Chemical Ecology, Jena, Germany.

The pea aphid (), a phloem-sucking insect, has undergone a rapid radiation together with the domestication and anthropogenic range expansion of several of its legume host plants. This insect species is a complex of at least 15 genetically different host races that can all develop on the universal host plant . However, each host race is specialized on a particular plant species, such as , , or , which makes it an attractive model insect to study ecological speciation. Previous work revealed that pea aphid host plants produce a specific phytohormone profile depending on the host plant - host race combination. Native aphid races induce lower defense hormone levels in their host plant than non-native pea aphid races. Whether these changes in hormone levels also lead to changes in other metabolites is still unknown. We used a mass spectrometry-based untargeted metabolomic approach to identify plant chemical compounds that vary among different host plant-host race combinations and might therefore, be involved in pea aphid host race specialization. We found significant differences among the metabolic fingerprints of the four legume species studied prior to aphid infestation, which correlated with aphid performance. After infestation, the metabolic profiles of and plants infested with their respective native aphid host race were consistently different from profiles after infestation with non-native host races and from uninfested control plants. The metabolic profiles of plants infested with their native aphid host race were also different from plants infested with non-native host races, but not different from uninfested control plants. The compounds responsible for these differences were putatively identified as flavonoids, saponins, non-proteinogenic amino acids and peptides among others. As members of these compound classes are known for their activity against insects and aphids in particular, they may be responsible for the differential performance of host races on native vs. non-native host plants. We conclude that the untargeted metabolomic approach is suitable to identify candidate compounds involved in the specificity of pea aphid - host plant interactions.
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http://dx.doi.org/10.3389/fpls.2019.00188DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6403166PMC
February 2019

Live Single-Cell Metabolomics With Matrix-Free Laser/Desorption Ionization Mass Spectrometry to Address Microalgal Physiology.

Front Plant Sci 2019 18;10:172. Epub 2019 Feb 18.

Max Planck Fellow Group on Plankton Community Interaction, Max Planck Institute for Chemical Ecology, Jena, Germany.

Unicellular phototrophic algae can form massive blooms with up to millions of individual cells per milliliter in freshwater and marine ecosystems. Despite the temporal dominance of bloom formers many algal species can co-exist and compete for nutrients and space, creating a complex and diverse community. While microscopy and single cell genomics can address the taxonomic inventory, the cellular metabolome has yet to be thoroughly explored to determine the physiological status of microalgae. This might, however, provide a key to understand the observed species diversity in the homogeneous environment. Here, we introduce an effective, rapid and versatile method to analyze living single cells from aqueous substrata with laser-desorption/ionization mass spectrometry (LDI-MS) using a simple and inexpensive matrix-free support. The cells deposited on a cultivation-medium wetted support are analyzed with minimal disturbance as they remain in their natural viable state until their disruption during LDI-MS. Metabolites desorbed from single cells are analyzed on High-Resolution Mass Spectrometry (HR-MS) using the Orbitrap FT-MS technology to fingerprint cellular chemistry. This live single-cell mass spectrometry (LSC-MS) allows assessing the physiological status and strain-specifics of different microalgae, including marine diatoms and freshwater chlorophytes, at the single-cell level. We further report a reliable and robust data treatment pipeline to perform multivariate statistics on the replicated LSC-MS data. Comparing single cell MS spectra from natural phytoplankton samples and from laboratory strains allows the identification and discrimination of inter and intra-specific metabolic variability and thereby has promising applications in addressing highly complex phytoplankton communities. Notably, the herein described matrix-free live-single-cell LDI-HR-MS approach enables monitoring dynamics of the plankton and might explain why key-players survive, thrive, avoid selective feeding or pathogenic virus and bacteria, while others are overcome and die.
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http://dx.doi.org/10.3389/fpls.2019.00172DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6387974PMC
February 2019

Enzymatic Bioweathering and Metal Mobilization From Black Slate by the Basidiomycete .

Front Microbiol 2018 24;9:2545. Epub 2018 Oct 24.

Microbial Communication, Institute of Microbiology, Friedrich Schiller University, Jena, Germany.

is a filamentous basidiomycete causing white-rot in many wood species with the help of a broad range of enzymes including multicopper oxidases such as laccases and laccase-like oxidases. Since these enzymes exhibit a broad substrate range, their ability to oxidatively degrade black slate was investigated. Both haploid monokaryotic, and mated dikaryotic strains were able to grow on black slate rich in organic carbon as sole carbon source. On defined media, only the monokaryon showed growth promotion by addition of slate. At the same time, metals were released from the slate and, after reaching a threshold concentration, inhibited further growth of the fungus. The proteome during decomposition of the black slate showed induction of proteins potentially involved in rock degradation and stress resistance, and the gene for laccase-like oxidase was up-regulated. Specifically in the dikaryon, the laccase gene was induced, while as well as , and expression levels remained similar. Spectrophotometric analysis revealed that both life forms were able to degrade the rock and produce smaller particles.
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http://dx.doi.org/10.3389/fmicb.2018.02545DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6207625PMC
October 2018

Plant Defensive β-Glucosidases Resist Digestion and Sustain Activity in the Gut of a Lepidopteran Herbivore.

Front Plant Sci 2018 8;9:1389. Epub 2018 Oct 8.

Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.

Two-component activated chemical defenses are a major part of many plants' strategies to disrupt herbivory. The activation step is often the β-glucosidase-catalyzed removal of a glucose moiety from a pro-toxin, leading to an unstable and toxic aglycone. While some β-glucosidases have been well studied, several aspects of their roles , such as their precise sites of enzymatic activity during and after ingestion, and the importance of particular isoforms in plant defense are still not fully understood. Here, plant defensive β-glucosidases from maize, white mustard and almonds were shown to resist digestion by larvae of the generalist lepidopteran , and the majority of the ingested activities toward both general and plant pro-toxic substrates was recovered in the frass. Among other proteins potentially involved in defense, we identified specific plant β-glucosidases and a maize β-glucosidase aggregating factor in frass from plant-fed insects using proteomic methods. We therefore found that, while larvae efficiently degraded bulk food protein during digestion, β-glucosidases were among a small number of plant defensive proteins that resist insect digestive proteolysis. These enzymes remain intact in the gut lumen and frass and can therefore further catalyze the activation of plant defenses after ingestion, especially in pH-neutral regions of the digestive system. As most of the ingested enzymatic activity persists in the frass, and only particular β-glucosidases were detected via proteomic analyses, our data support the involvement of specific isoforms (maize ZmGlu1 and MA1 myrosinase) in defense .
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http://dx.doi.org/10.3389/fpls.2018.01389DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6186830PMC
October 2018

Metabolomic and transcriptomic data on major metabolic/biosynthetic pathways in workers and soldiers of the termite (Isoptera: Rhinotermitidae) and chemical synthesis of intermediates of defensive ()-nitropentadec-1-ene biosynthesis.

Data Brief 2018 Jun 2;18:1614-1627. Epub 2018 May 2.

The Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Flemingovo n. 2, 166 10 Prague, Czech Republic.

Production of nitro compounds has only seldom been recorded in arthropods. The aliphatic nitroalkene ()-nitropentadec-1-ene (), identified in soldiers of the termite genus , was the first case documented in insects in early seventies. Yet, the biosynthetic origin of has long remained unknown. We previously proposed that N arises through the condensation of amino acids glycine and/or l-serine with tetradecanoic acid along a biosynthetic pathway analogous to the formation of sphingolipids. Here, we provide a metabolomics and transcriptomic data of the termite workers and soldiers. Data are related to biosynthesis in soldiers. Original metabolomics data were deposited in MetaboLights metabolomics database and are become publicly available after publishing the original article. Additionally, chemical synthesis of biosynthetic intermediates of in nonlabeled and stable labeled forms are reported. Data extend our poor knowledge of arthropod metabolome and transcriptome and would be useful for comparative study in termites or other arthropods. The data were used for de-replication of biosynthesis and published separately (Jirošová et al., 2017) [1].
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http://dx.doi.org/10.1016/j.dib.2018.04.052DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5997979PMC
June 2018

The Olfactory Logic behind Fruit Odor Preferences in Larval and Adult Drosophila.

Cell Rep 2018 05;23(8):2524-2531

Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Hans-Knoell-Strasse 8, 07745 Jena, Germany. Electronic address:

Despite the comprehensive knowledge on odor coding, our understanding of the relationship between sensory input and behavioral output in Drosophila remains weak. Here, we measure the behavioral responses generated by larval and adult flies in response to 34 fruit odors and find that larval preference for fruit odors differs from that of adult flies. Next, we provide a functional analysis of the full repertoire of the peripheral olfactory system using the same comprehensive stimulus spectrum. We find that 90% and 53% of larval and adult olfactory receptors tested here, respectively, are involved in evaluating these fruit odors. Finally, we find that the total amount of olfactory neuronal activity correlates strongly positively with behavioral output in larvae and correlates weakly negatively in adult flies. Our results suggest that larval and adult flies have evolved different mechanisms for detection and computation of fruit odors, mechanisms likely mirroring the different lifestyles of both developmental stages.
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http://dx.doi.org/10.1016/j.celrep.2018.04.085DOI Listing
May 2018

Lipophilic extracts of Leucas zeylanica, a multi-purpose medicinal plant in the tropics, inhibit key enzymes involved in inflammation and gout.

J Ethnopharmacol 2018 Oct 1;224:474-481. Epub 2018 May 1.

Institute of Pharmacy, Friedrich-Schiller-University Jena, Philosophenweg 14, D-07743 Jena, Germany. Electronic address:

Ethnopharmacological Relevance: Leucas zeylanica (L.) W.T. Aiton is a popular, multi-purpose medicinal plant in Sri Lanka but the pharmacological potential and the chemical profile have not been systematically investigated to understand and rationalize the reported ethnobotanical significance.

Aim Of The Study: The present study was undertaken to scientifically validate the traditional usage of this plant for the treatment of inflammatory conditions, gout and microbial infections. Inhibition of 5-lipoxygenase (5-LO), microsomal prostaglandin E synthase (mPGES)-1 and xanthine oxidase (XO) by different extracts of L. zeylanica was investigated to determine the anti-inflammatory and anti-gout activity, respectively. The antibacterial and antifungal activities were also studied and the relevant constituents in the bioactive extracts were tentatively identified.

Materials And Methods: Cell-free and/or cell-based assays were employed in order to investigate the effects of the extracts against the activity of human 5-LO, mPGES-1 and XO as well as to assess antioxidant properties. The antibacterial activity of the extracts was determined by the broth micro-dilution method against Gram positive and Gram negative bacteria including methicillin-resistant Staphylococcus aureus while the agar dilution method was employed to determine the anti-Candida activity. Gas chromatography coupled to mass spectrometric (GC-MS) analysis enabled the characterization of secondary metabolites in the extracts.

Results: The dichloromethane extract of L. zeylanica efficiently inhibited 5-LO activity in stimulated human neutrophils (IC = 5.5 µg/mL) and isolated human 5-LO and mPGES-1 (IC = 2.2 and 0.4 µg/mL). Potent inhibition of XO was observed by the same extract (IC = 47.5 μg/mL), which is the first report of XO-inhibitory activity of a Sri Lankan medicinal plant. Interestingly, significant radical scavenging activity was not observed by this extract. Only the n-hexane extract exhibited antibacterial activity against Staphylococcus aureus and Staphylococcus saprophyticus with a MIC of 250 µg/mL while the anti-Candida activity was moderate. GC-MS analysis revealed the presence of phytosterols, fatty acids, sesquiterpenes, diterpenes and several other types of secondary metabolites.

Conclusions: Potent inhibition of 5-LO, mPGES-1 and XO rationalizes the ethnopharmacological use of L. zeylanica as anti-inflammatory and anti-gout remedy. Interestingly, the antimicrobial activities were not prominent, despite its wide utility as an antimicrobial medication.
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http://dx.doi.org/10.1016/j.jep.2018.04.042DOI Listing
October 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

Evolutionary stability of antibiotic protection in a defensive symbiosis.

Proc Natl Acad Sci U S A 2018 Feb 14;115(9):E2020-E2029. Epub 2018 Feb 14.

Insect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany;

The increasing resistance of human pathogens severely limits the efficacy of antibiotics in medicine, yet many animals, including solitary beewolf wasps, successfully engage in defensive alliances with antibiotic-producing bacteria for millions of years. Here, we report on the in situ production of 49 derivatives belonging to three antibiotic compound classes (45 piericidin derivatives, 3 streptochlorin derivatives, and nigericin) by the symbionts of 25 beewolf host species and subspecies, spanning 68 million years of evolution. Despite a high degree of qualitative stability in the antibiotic mixture, we found consistent quantitative differences between species and across geographic localities, presumably reflecting adaptations to combat local pathogen communities. Antimicrobial bioassays with the three main components and in silico predictions based on the structure and specificity in polyketide synthase domains of the piericidin biosynthesis gene cluster yield insights into the mechanistic basis and ecoevolutionary implications of producing a complex mixture of antimicrobial compounds in a natural setting.
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http://dx.doi.org/10.1073/pnas.1719797115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5834716PMC
February 2018

Selective Utilization of Benzimidazolyl-Norcobamides as Cofactors by the Tetrachloroethene Reductive Dehalogenase of Sulfurospirillum multivorans.

J Bacteriol 2018 04 26;200(8). Epub 2018 Mar 26.

Department of Applied and Ecological Microbiology, Institute of Microbiology, Friedrich Schiller University, Jena, Germany

The organohalide-respiring bacterium produces a unique cobamide, namely, norpseudo-B, which serves as cofactor of the tetrachloroethene (PCE) reductive dehalogenase (PceA). As previously reported, a replacement of the adeninyl moiety, the lower base of the cofactor, by exogenously applied 5,6-dimethylbenzimidazole led to inactive PceA. To explore the general effect of benzimidazoles on the PCE metabolism, the susceptibility of the organism for guided biosynthesis of various singly substituted benzimidazolyl-norcobamides was investigated, and their use as cofactor by PceA was analyzed. Exogenously applied 5-methylbenzimidazole (5-MeBza), 5-hydroxybenzimidazole (5-OHBza), and 5-methoxybenzimidazole (5-OMeBza) were found to be efficiently incorporated as lower bases into norcobamides (NCbas). Structural analysis of the NCbas by nuclear magnetic resonance spectroscopy uncovered a regioselectivity in the utilization of these precursors for NCba biosynthesis. When 5-MeBza was added, a mixture of 5-MeBza-norcobamide and 6-MeBza-norcobamide was formed, and the PceA enzyme activity was affected. In the presence of 5-OHBza, almost exclusively 6-OHBza-norcobamide was produced, while in the presence of 5-OMeBza, predominantly 5-OMeBza-norcobamide was detected. Both NCbas were incorporated into PceA, and no negative effect on the PceA activity was observed. In crystal structures of PceA, both NCbas were bound in the base-off mode with the 6-OHBza and 5-OMeBza lower bases accommodated by the same solvent-exposed hydrophilic pocket that harbors the adenine as the lower base of authentic norpseudo-B In this study, a selective production of different norcobamide isomers containing singly substituted benzimidazoles as lower bases is shown, and unique structural insights into their utilization as cofactors by a cobamide-containing enzyme are provided. Guided biosynthesis of norcobamides containing singly substituted benzimidazoles as lower bases by the organohalide-respiring epsilonproteobacterium is reported. An unprecedented specificity in the formation of norcobamide isomers containing hydroxylated or methoxylated benzimidazoles was observed that implicated a strict regioselectivity of the norcobamide biosynthesis in the organism. In contrast to 5,6-dimethylbenzimidazolyl-norcobamide, the incorporation of singly substituted benzimidazolyl-norcobamides as a cofactor into the tetrachloroethene reductive dehalogenase was not impaired. The enzyme was found to be functional with different isomers and not limited to the use of adeninyl-norcobamide. Structural analysis of the enzyme equipped with either adeninyl- or benzimidazolyl-norcobamide cofactors visualized for the first time structurally different cobamides bound in base-off conformation to the cofactor-binding site of a cobamide-containing enzyme.
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http://dx.doi.org/10.1128/JB.00584-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5869469PMC
April 2018

A Poly(A) Ribonuclease Controls the Cellotriose-Based Interaction between and Its Host Arabidopsis.

Plant Physiol 2018 03 25;176(3):2496-2514. Epub 2018 Jan 25.

Department of Plant Physiology, Matthias Schleiden Institute of Genetics, Bioinformatics, and Molecular Botany, Friedrich-Schiller-University, D-07743 Jena, Germany

, an endophytic root-colonizing fungus, efficiently promotes plant growth and induces resistance to abiotic stress and biotic diseases. fungal cell wall extract induces cytoplasmic calcium elevation in host plant roots. Here, we show that cellotriose (CT) is an elicitor-active cell wall moiety released by into the medium. CT induces a mild defense-like response, including the production of reactive oxygen species, changes in membrane potential, and the expression of genes involved in growth regulation and root development. CT-based cytoplasmic calcium elevation in Arabidopsis () roots does not require the BAK1 coreceptor or the putative Ca channels TPC1, GLR3.3, GLR2.4, and GLR2.5 and operates synergistically with the elicitor chitin. We identified an ethyl methanesulfonate-induced mutant () impaired in the response to CT and various other cellooligomers ( = 2-7), but not to chitooligomers ( = 4-8), in roots. The mutant contains a single nucleotide exchange in the gene encoding a poly(A) ribonuclease (AtPARN; At1g55870) that degrades the poly(A) tails of specific mRNAs. The wild-type cDNA, expressed under the control of a 35S promoter, complements the mutant phenotype. Our identification of cellotriose as a novel chemical mediator casts light on the complex -plant mutualistic relationship.
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http://dx.doi.org/10.1104/pp.17.01423DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5841714PMC
March 2018

Exodermis and endodermis are the sites of xanthone biosynthesis in Hypericum perforatum roots.

New Phytol 2018 02 6;217(3):1099-1112. Epub 2017 Dec 6.

Institute of Pharmaceutical Biology, Technische Universität Braunschweig, Mendelssohnstraße 1, 38106, Braunschweig, Germany.

Xanthones are specialized metabolites with antimicrobial properties, which accumulate in roots of Hypericum perforatum. This medicinal plant provides widely taken remedies for depressive episodes and skin disorders. Owing to the array of pharmacological activities, xanthone derivatives attract attention for drug design. Little is known about the sites of biosynthesis and accumulation of xanthones in roots. Xanthone biosynthesis is localized at the transcript, protein, and product levels using in situ mRNA hybridization, indirect immunofluorescence detection, and high lateral and mass resolution mass spectrometry imaging (AP-SMALDI-FT-Orbitrap MSI), respectively. The carbon skeleton of xanthones is formed by benzophenone synthase (BPS), for which a cDNA was cloned from root cultures of H. perforatum var. angustifolium. Both the BPS protein and the BPS transcripts are localized to the exodermis and the endodermis of roots. The xanthone compounds as the BPS products are detected in the same tissues. The exodermis and the endodermis, which are the outermost and innermost cell layers of the root cortex, respectively, are not only highly specialized barriers for controlling the passage of water and solutes but also preformed lines of defence against soilborne pathogens and predators.
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http://dx.doi.org/10.1111/nph.14929DOI Listing
February 2018

Secondary ion mass spectrometry imaging and multivariate data analysis reveal co-aggregation patterns of Populus trichocarpa leaf surface compounds on a micrometer scale.

Plant J 2018 Jan 8;93(1):193-206. Epub 2017 Dec 8.

Research Group Mass Spectrometry, Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, 07745, Jena, Germany.

Spatially resolved analysis of a multitude of compound classes has become feasible with the rapid advancement in mass spectrometry imaging strategies. In this study, we present a protocol that combines high lateral resolution time-of-flight secondary ion mass spectrometry (TOF-SIMS) imaging with a multivariate data analysis (MVA) approach to probe the complex leaf surface chemistry of Populus trichocarpa. Here, epicuticular waxes (EWs) found on the adaxial leaf surface of P. trichocarpa were blotted on silicon wafers and imaged using TOF-SIMS at 10 μm and 1 μm lateral resolution. Intense M and M molecular ions were clearly visible, which made it possible to resolve the individual compound classes present in EWs. Series of long-chain aliphatic saturated alcohols (C -C ), hydrocarbons (C -C ) and wax esters (WEs; C -C ) were clearly observed. These data correlated with the Li-chelation matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) analysis, which yielded mostly molecular adduct ions of the analyzed compounds. Subsequently, MVA was used to interrogate the TOF-SIMS dataset for identifying hidden patterns on the leaf's surface based on its chemical profile. After the application of principal component analysis (PCA), a small number of principal components (PCs) were found to be sufficient to explain maximum variance in the data. To further confirm the contributions from pure components, a five-factor multivariate curve resolution (MCR) model was applied. Two distinct patterns of small islets, here termed 'crystals', were apparent from the resulting score plots. Based on PCA and MCR results, the crystals were found to be formed by C or C alcohols. Other less obvious patterns observed in the PCs revealed that the adaxial leaf surface is coated with a relatively homogenous layer of alcohols, hydrocarbons and WEs. The ultra-high-resolution TOF-SIMS imaging combined with the MVA approach helped to highlight the diverse patterns underlying the leaf's surface. Currently, the methods available to analyze the surface chemistry of waxes in conjunction with the spatial information related to the distribution of compounds are limited. This study uses tools that may provide important biological insights into the composition of the wax layer, how this layer is repaired after mechanical damage or insect feeding, and which transport mechanisms are involved in deploying wax constituents to specific regions on the leaf surface.
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http://dx.doi.org/10.1111/tpj.13763DOI Listing
January 2018

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