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Published year: 20216
Bacterial endosymbionts protect beneficial soil fungus from nematode attack.

Abstract (Expand)

Fungi of the genus Mortierella occur ubiquitously in soils where they play pivotal roles in carbon cycling, xenobiont degradation, and promoting plant growth. These important fungi are, however, … threatened by micropredators such as fungivorous nematodes, and yet little is known about their protective tactics. We report that Mortierella verticillata NRRL 6337 harbors a bacterial endosymbiont that efficiently shields its host from nematode attacks with anthelmintic metabolites. Microscopic investigation and 16S ribosomal DNA analysis revealed that a previously overlooked bacterial symbiont belonging to the genus Mycoavidus dwells in M. verticillata hyphae. Metabolic profiling of the wild-type fungus and a symbiont-free strain obtained by antibiotic treatment as well as genome analyses revealed that highly cytotoxic macrolactones (CJ-12,950 and CJ-13,357, syn necroxime C and D), initially thought to be metabolites of the soil-inhabiting fungus, are actually biosynthesized by the endosymbiont. According to comparative genomics, the symbiont belongs to a new species (Candidatus Mycoavidus necroximicus) with 12% of its 2.2 Mb genome dedicated to natural product biosynthesis, including the modular polyketide-nonribosomal peptide synthetase for necroxime assembly. Using Caenorhabditis elegans and the fungivorous nematode Aphelenchus avenae as test strains, we show that necroximes exert highly potent anthelmintic activities. Effective host protection was demonstrated in cocultures of nematodes with symbiotic and chemically complemented aposymbiotic fungal strains. Image analysis and mathematical quantification of nematode movement enabled evaluation of the potency. Our work describes a relevant role for endofungal bacteria in protecting fungi against mycophagous nematodes.

Authors: H. Buttner, S. P. Niehs, K. Vandelannoote, Z. Cseresnyes, B. Dose, I. Richter, R. Gerst, M. T. Figge, T. P. Stinear, S. J. Pidot, C. Hertweck

Date Published: 14th Sep 2021

Publication Type: Journal

Multimodal Molecular Imaging and Identification of Bacterial Toxins Causing Mushroom Soft Rot and Cavity Disease

Abstract (Expand)

Soft rot disease of edible mushrooms leads to rapid degeneration of fungal tissue and thus severely affects farming productivity worldwide. The bacterial mushroom pathogen Burkholderia gladioli pv. … agaricicola has been identified as the cause. Yet, little is known about the molecular basis, the spatial distribution and the biological role of antifungal agents and toxins involved in this infectious disease. We combine genome mining, metabolic profiling, MALDI-Imaging and UV Raman spectroscopy, to detect, identify and visualize a complex of chemical mediators and toxins produced by the pathogen during the infection process, including toxoflavin, caryoynencin, and sinapigladioside. Furthermore, targeted gene knockouts and in vitro assays link antifungal agents to prevalent symptoms of soft rot, mushroom browning, and impaired mycelium growth. Comparisons of related pathogenic, mutualistic and environmental Burkholderia spp. indicate that the arsenal of antifungal agents may have paved the way for ancestral bacteria to colonize niches where frequent, antagonistic interactions with fungi occur. Our findings not only demonstrate the power of label-free, in vivo detection of polyyne virulence factors by Raman imaging, but may also inspire new approaches to disease control.

Authors: Benjamin Dose, Tawatchai Thongkongkaew, David Zopf, Hak Joong Kim, Evgeni V. Bratovanov, María García-Altares Pérez, Kirstin Scherlach, Jana Krabbe, Claudia Ross, Ron Hermenau, Sarah P. Niehs, Anja Silge, Julian Hniopek, Michael Schmitt, Jürgen Popp, Christian Hertweck

Date Published: 7th Jul 2021

Publication Type: Journal

Mining and unearthing hidden biosynthetic potential.

Abstract (Expand)

Genetically encoded small molecules (secondary metabolites) play eminent roles in ecological interactions, as pathogenicity factors and as drug leads. Yet, these chemical mediators often evade detection, … and the discovery of novel entities is hampered by low production and high rediscovery rates. These limitations may be addressed by genome mining for biosynthetic gene clusters, thereby unveiling cryptic metabolic potential. The development of sophisticated data mining methods and genetic and analytical tools has enabled the discovery of an impressive array of previously overlooked natural products. This review shows the newest developments in the field, highlighting compound discovery from unconventional sources and microbiomes.

Authors: K. Scherlach, C. Hertweck

Date Published: 23rd Jun 2021

Publication Type: Journal

Biosynthesis of Sinapigladioside, an Antifungal Isothiocyanate from Burkholderia Symbionts.

Abstract (Expand)

Sinapigladioside is a rare isothiocyanate-bearing natural product from beetle-associated bacteria ( Burkholderia gladioli ) that may protect the beetle offspring against entomopathogenic fungi. The … biosynthetic origin of sinapigladioside has been elusive, and little is known about bacterial isothiocyanate biosynthesis in general. On the basis of stable-isotope labeling, bioinformatics, and mutagenesis we identified the sinapigladioside biosynthesis gene cluster in the symbiont and found that an isonitrile synthase plays a key role in the biosynthetic pathway. Genome mining and network analyses indicate that related gene clusters are distributed across various bacterial phyla including producers of both nitriles and isothiocyanates. Our findings support a model for bacterial isothiocyanate biosynthesis by sulfur transfer onto isonitrile precursors.

Authors: B. Dose, S. P. Niehs, K. Scherlach, S. Shahda, L. V. Florez, M. Kaltenpoth, C. Hertweck

Date Published: 19th Mar 2021

Publication Type: Journal

Iron Coordination Properties of Gramibactin as Model for the New Class of Diazeniumdiolate Based Siderophores.

Abstract (Expand)

Gramibactin (GBT) is an archetype for the new class of diazeniumdiolate siderophores, produced by Paraburkholderia graminis, a cereal-associated rhizosphere bacterium, for which a detailed solution … thermodynamic study exploring the iron coordination properties is reported. The acid-base behavior of gramibactin as well as its complexing ability toward Fe(3+) was studied over a wide range of pH values (2</=pH</=11). For the latter the ligand-competition method employing EDTA was used. Only two species are formed: [Fe(GBT)](-) (pH 2 to 9) and [Fe(GBT)(OH)2 ](3-) (pH>/=9). The formation of [Fe(GBT)](-) and its occurrence in real systems was confirmed by LC-HRESIMS analysis of the bacteria culture broth extract. The sequestering ability of gramibactin was also evaluated in terms of the parameters pFe and pL0.5 . Gramibactin exhibits a higher sequestering ability toward Fe(3+) than EDTA and of the same order of magnitude as hydroxamate-type microbial siderophores, but smaller than most of the catecholate-type siderophores and much higher than the most known phytosiderophores.

Authors: S. Gama, R. Hermenau, M. Frontauria, D. Milea, S. Sammartano, C. Hertweck, W. Plass

Date Published: 5th Feb 2021

Publication Type: Journal

N-Heterocyclization in Gliotoxin Biosynthesis is Catalyzed by a Distinct Cytochrome P450 Monooxygenase.

Abstract (Expand)

Gliotoxin and related epidithiodiketopiperazines (ETP) from diverse fungi feature highly functionalized hydroindole scaffolds with an array of medicinally and ecologically relevant activities. Mutation … analysis, heterologous reconstitution, and biotransformation experiments revealed that a cytochrome P450 monooxygenase (GliF) from the human-pathogenic fungus Aspergillus fumigatus plays a key role in the formation of the complex heterocycle. In vitro assays using a biosynthetic precursor from a blocked mutant showed that GliF is specific to ETPs and catalyzes an unprecedented heterocyclization reaction that cannot be emulated with current synthetic methods. In silico analyses indicate that this rare biotransformation takes place in related ETP biosynthetic pathways.

Authors: D. H. Scharf, P. Chankhamjon, K. Scherlach, J. Dworschak, T. Heinekamp, M. Roth, A. A. Brakhage, C. Hertweck

Date Published: 15th Jan 2021

Publication Type: Journal

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