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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

Two Types of Threonine-Tagged Lipopeptides Synergize in Host Colonization by Pathogenic Burkholderia Species.

Abstract (Expand)

Bacterial infections of agriculturally important mushrooms and plants pose a major threat to human food sources worldwide. However, structures of chemical mediators required by the pathogen for host … colonization and infection remain elusive in most cases. Here, we report two types of threonine-tagged lipopeptides conserved among mushroom and rice pathogenic Burkholderia species that facilitate bacterial infection of hosts. Genome mining, metabolic profiling of infected mushrooms, and heterologous expression of orphan gene clusters allowed the discovery of these unprecedented metabolites in the mushroom pathogen Burkholderia gladioli (haereogladin, burriogladin) and the plant pathogen Burkholderia glumae (haereoglumin and burrioglumin). Through targeted gene deletions, the molecular basis of lipopeptide biosynthesis by nonribosomal peptide synthetases was revealed. Surprisingly, both types of lipopeptides feature unusual threonine tags, which yield longer peptide backbones than one would expect based on the canonical colinearity of the NRPS assembly lines. Both peptides play an indirect role in host infection as biosurfactants that enable host colonization by mediating swarming and biofilm formation abilities. Moreover, MALDI imaging mass spectrometry was applied to investigate the biological role of the lipopeptides. Our results shed light on conserved mechanisms that mushroom and plant pathogenic bacteria utilize for host infection and expand current knowledge on bacterial virulence factors that may represent a new starting point for the targeted development of crop protection measures in the future.

Authors: T. Thongkongkaew, W. Ding, E. Bratovanov, E. Oueis, M. A. Garci A-Altares, N. Zaburannyi, K. Harmrolfs, Y. Zhang, K. Scherlach, R. Muller, C. Hertweck

Date Published: 18th May 2018

Publication Type: Journal

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