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9 Publications visible to you, out of a total of 9
The Termite Fungal Cultivar Termitomyces Combines Diverse Enzymes and Oxidative Reactions for Plant Biomass Conversion.

Abstract (Expand)

Macrotermitine termites have domesticated fungi in the genus Termitomyces as their primary food source using predigested plant biomass. To access the full nutritional value of lignin-enriched plant … biomass, the termite-fungus symbiosis requires the depolymerization of this complex phenolic polymer. While most previous work suggests that lignocellulose degradation is accomplished predominantly by the fungal cultivar, our current understanding of the underlying biomolecular mechanisms remains rudimentary. Here, we provide conclusive omics and activity-based evidence that Termitomyces employs not only a broad array of carbohydrate-active enzymes (CAZymes) but also a restricted set of oxidizing enzymes (manganese peroxidase, dye decolorization peroxidase, an unspecific peroxygenase, laccases, and aryl-alcohol oxidases) and Fenton chemistry for biomass degradation. We propose for the first time that Termitomyces induces hydroquinone-mediated Fenton chemistry (Fe(2+) + H2O2 + H(+) --> Fe(3+) + (*)OH + H2O) using a herein newly described 2-methoxy-1,4-dihydroxybenzene (2-MH2Q, compound 19)-based electron shuttle system to complement the enzymatic degradation pathways. This study provides a comprehensive depiction of how efficient biomass degradation by means of this ancient insect's agricultural symbiosis is accomplished. IMPORTANCE Fungus-growing termites have optimized the decomposition of recalcitrant plant biomass to access valuable nutrients by engaging in a tripartite symbiosis with complementary contributions from a fungal mutualist and a codiversified gut microbiome. This complex symbiotic interplay makes them one of the most successful and important decomposers for carbon cycling in Old World ecosystems. To date, most research has focused on the enzymatic contributions of microbial partners to carbohydrate decomposition. Here, we provide genomic, transcriptomic, and enzymatic evidence that Termitomyces also employs redox mechanisms, including diverse ligninolytic enzymes and a Fenton chemistry-based hydroquinone-catalyzed lignin degradation mechanism, to break down lignin-rich plant material. Insights into these efficient decomposition mechanisms reveal new sources of efficient ligninolytic agents applicable for energy generation from renewable sources.

Authors: F. Schalk, C. Gostincar, N. B. Kreuzenbeck, B. H. Conlon, E. Sommerwerk, P. Rabe, I. Burkhardt, T. Kruger, O. Kniemeyer, A. A. Brakhage, N. Gunde-Cimerman, Z. W. de Beer, J. S. Dickschat, M. Poulsen, C. Beemelmanns

Date Published: 15th Jun 2021

Publication Type: Journal

GNPS-guided discovery of xylacremolide C and D, evaluation of their putative biosynthetic origin and bioactivity studies of xylacremolide A and B.

Abstract (Expand)

Targeted HRMS(2)-GNPS-based metabolomic analysis of Pseudoxylaria sp. X187, a fungal antagonist of the fungus-growing termite symbiosis, resulted in the identification of two lipopeptidic congeners of … xylacremolides, named xylacremolide C and D, which are built from d-phenylalanine, l-proline and an acetyl-CoA starter unit elongated by four malonyl-CoA derived ketide units. The putative xya gene cluster was identified from a draft genome generated by Illumina and PacBio sequencing and RNAseq studies. Biological activities of xylacremolide A and B were evaluated and revealed weak histone deacetylase inhibitory (HDACi) and antifungal activities, as well as moderate protease inhibition activity across a panel of nine human, viral and bacterial proteases.

Authors: F. Schalk, J. Fricke, S. Um, B. H. Conlon, H. Maus, N. Jager, T. Heinzel, T. Schirmeister, M. Poulsen, C. Beemelmanns

Date Published: 24th May 2021

Publication Type: Journal

Polyhalogenation of Isoflavonoids by the Termite-Associated Actinomadura sp. RB99.

Abstract (Expand)

Based on high-resolution tandem mass spectrometry (HR-MS(2)) and global natural products social molecular networking (GNPS), we found that plant-derived daidzein and genistein derivatives are polyhalogenated … by termite-associated Actinomadura species RB99. MS-guided purification from extracts of bacteria grown under optimized conditions led to the isolation of eight polychlorinated isoflavones, including six unreported derivatives, and seven novel polybrominated derivatives, two of which showed antimicrobial activity.

Authors: S. Rak Lee, F. Schalk, J. W. Schwitalla, R. Benndorf, J. Vollmers, A. K. Kaster, Z. W. de Beer, M. Park, M. J. Ahn, W. H. Jung, C. Beemelmanns, K. H. Kim

Date Published: 23rd Oct 2020

Publication Type: Journal

Targeted Discovery of Tetrapeptides and Cyclic Polyketide-Peptide Hybrids from a Fungal Antagonist of Farming Termites.

Abstract (Expand)

Herein, we report the targeted isolation and characterization of four linear nonribosomally synthesized tetrapeptides (pseudoxylaramide A-D) and two cyclic nonribosomal peptide synthetase-polyketide … synthase-derived natural products (xylacremolide A and B) from the termite-associated stowaway fungus Pseudoxylaria sp. X187. The fungal strain was prioritized for further metabolic analysis based on its taxonomical position and morphological and bioassay data. Metabolic data were dereplicated based on high-resolution tandem mass spectrometry data and global molecular networking analysis. The structure of all six new natural products was elucidated based on a combination of 1D and 2D NMR analysis, Marfey's analysis and X-ray crystallography.

Authors: F. Schalk, S. Um, H. Guo, N. B. Kreuzenbeck, H. Gorls, Z. W. de Beer, C. Beemelmanns

Date Published: 15th Oct 2020

Publication Type: Journal

Streptomyces smaragdinus sp. nov., isolated from the gut of the fungus growing-termite Macrotermes natalensis.

Abstract (Expand)

The taxonomic position of a novel aerobic, Gram-positive actinobacteria, designated strain RB5(T), was determined using a polyphasic approach. The strain, isolated from the gut of the fungus-farming … termite Macrotermes natalensis, showed morphological, physiological and chemotaxonomic properties typical of the genus Streptomyces. Based on 16S rRNA gene sequence analysis, the closest phylogenetic neighbour of RB5(T) was Streptomyces polyrhachis DSM 42102(T) (98.87 %). DNA-DNA hybridization experiments between strain RB5(T) and S. polyrhachis DSM 42102(T) resulted in a value of 27.4 % (26.8 %). The cell wall of strain RB5(T) contained ll-diaminopimelic acid as the diagnostic amino acid. Mycolic acids and diagnostic sugars in whole-cell hydrolysates were not detected. The strain produced the following major phospholipids: diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylinositol, phosphatidylinositol-mannoside and phosphatidylserine. The menaquinone profile showed hexa- and octahydrogenated menaquinones containing nine isoprene units [MK-9(H6) and MK-9(H8)]. The strain exhibited a fatty acid profile containing the following major fatty acids: 12-methyltridecanoic acid (iso-C14 : 0) 12-methyltetradecanoic acid (anteiso-C15 : 0), 13-methyltetradecanoic acid (iso-C15 : 0) and 14-methylpentadecanoic acid (iso-C16 : 0). Here, we propose a novel species of the genus Streptomyces - Streptomyces smaragdinus with the type strain RB5(T) (=VKM Ac-2839(T)=NRRL B65539(T)).

Authors: J. W. Schwitalla, R. Benndorf, K. Martin, J. Vollmers, A. K. Kaster, Z. W. de Beer, M. Poulsen, C. Beemelmanns

Date Published: 25th Sep 2020

Publication Type: Journal

Nocardia macrotermitis sp. nov. and Nocardia aurantia sp. nov., isolated from the gut of the fungus-growing termite Macrotermes natalensis.

Abstract (Expand)

The taxonomic positions of two novel aerobic, Gram-stain-positive Actinobacteria, designated RB20(T) and RB56(T), were determined using a polyphasic approach. Both were isolated from the fungus-farming … termite Macrotermes natalensis. Results of 16S rRNA gene sequence analysis revealed that both strains are members of the genus Nocardia with the closest phylogenetic neighbours Nocardia miyunensis JCM12860(T) (98.9 %) and Nocardia nova DSM44481(T) (98.5 %) for RB20(T) and Nocardia takedensis DSM 44801(T) (98.3 %), Nocardia pseudobrasiliensis DSM 44290(T) (98.3 %) and Nocardia rayongensis JCM 19832(T) (98.2 %) for RB56(T). Digital DNA-DNA hybridization (DDH) between RB20(T) and N. miyunensis JCM12860(T) and N. nova DSM 44481(T) resulted in similarity values of 33.9 and 22.0 %, respectively. DDH between RB56(T) and N. takedensis DSM44801(T) and N. pseudobrasiliensis DSM44290(T) showed similarity values of 20.7 and 22.3 %, respectively. In addition, wet-lab DDH between RB56(T) and N. rayongensis JCM19832(T) resulted in 10.2 % (14.5 %) similarity. Both strains showed morphological and chemotaxonomic features typical for the genus Nocardia, such as the presence of meso-diaminopimelic acid (A2pm) within the cell wall, arabinose and galactose as major sugar components within whole cell-wall hydrolysates, the presence of mycolic acids and major phospholipids (diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylinositol), and the predominant menaquinone MK-8 (H4, omega-cyclo). The main fatty acids for both strains were hexadecanoic acid (C16 : 0), 10-methyloctadecanoic acid (10-methyl C18 : 0) and cis-9-octadecenoic acid (C18 : 1 omega9c). We propose two novel species within the genus Nocardia: Nocardia macrotermitis sp. nov. with the type strain RB20(T) (=VKM Ac-2841(T)=NRRL B65541(T)) and Nocardia aurantia sp. nov. with the type strain RB56(T) (=VKM Ac-2842(T)=NRRL B65542(T)).

Authors: R. Benndorf, J. W. Schwitalla, K. Martin, Z. W. de Beer, J. Vollmers, A. K. Kaster, M. Poulsen, C. Beemelmanns

Date Published: 21st Aug 2020

Publication Type: Journal

Disease-free monoculture farming by fungus-growing termites.

Abstract (Expand)

Fungus-growing termites engage in an obligate mutualistic relationship with Termitomyces fungi, which they maintain in monocultures on specialised fungus comb structures, without apparent problems with … infectious diseases. While other fungi have been reported in the symbiosis, detailed comb fungal community analyses have been lacking. Here we use culture-dependent and -independent methods to characterise fungus comb mycobiotas from three fungus-growing termite species (two genera). Internal Transcribed Spacer (ITS) gene analyses using 454 pyrosequencing and Illumina MiSeq showed that non-Termitomyces fungi were essentially absent in fungus combs, and that Termitomyces fungal crops are maintained in monocultures as heterokaryons with two or three abundant ITS variants in a single fungal strain. To explore whether the essential absence of other fungi within fungus combs is potentially due to the production of antifungal metabolites by Termitomyces or comb bacteria, we performed in vitro assays and found that both Termitomyces and chemical extracts of fungus comb material can inhibit potential fungal antagonists. Chemical analyses of fungus comb material point to a highly complex metabolome, including compounds with the potential to play roles in mediating these contaminant-free farming conditions in the termite symbiosis.

Authors: S. Otani, V. L. Challinor, N. B. Kreuzenbeck, S. Kildgaard, S. Krath Christensen, L. L. M. Larsen, D. K. Aanen, S. A. Rasmussen, C. Beemelmanns, M. Poulsen

Date Published: 19th Jun 2019

Publication Type: Journal

Mechanistic characterization of three sesquiterpene synthases from the termite-associated fungus Termitomyces.

Abstract (Expand)

Three terpene synthases from the termite associated fungus Termitomyces were functionally characterized as (+)-intermedeol synthase, (-)-gamma-cadinene synthase and (+)-germacrene D-4-ol synthase, with … the germacrene D-4-ol synthase as the first reported enzyme that produces the (+)-enantiomer. The enzymatic mechanisms were thoroughly investigated by incubation with isotopically labeled precursors to follow the stereochemical courses of single reaction steps in catalysis. The role of putative active site residues was tested by site directed mutagenesis of a highly conserved tryptophan in all three enzymes and additional residues in (-)-gamma-cadinene synthase that were identified by homology model analysis.

Authors: I. Burkhardt, N. B. Kreuzenbeck, C. Beemelmanns, J. S. Dickschat

Date Published: 27th Mar 2019

Publication Type: Journal

Pseudoxylallemycins A-F, Cyclic Tetrapeptides with Rare Allenyl Modifications Isolated from Pseudoxylaria sp. X802: A Competitor of Fungus-Growing Termite Cultivars.

Abstract (Expand)

Based on fungus-fungus pairing assays and HRMS-based dereplication strategy, six new cyclic tetrapeptides, pseudoxylallemycins A-F (1-6), were isolated from the termite-associated fungus Pseudoxylaria … sp. X802. Structures were characterized using NMR spectroscopy, HRMS, and Marfey's reaction. Pseudoxylallemycins B-D (2-4) possess a rare and chemically accessible allene moiety amenable for synthetic modifications, and derivatives A-D showed antimicrobial activity against Gram-negative human-pathogenic Pseudomonas aeruginosa and antiproliferative activity against human umbilical vein endothelial cells and K-562 cell lines.

Authors: H. Guo, N. B. Kreuzenbeck, S. Otani, M. Garcia-Altares, H. M. Dahse, C. Weigel, D. K. Aanen, C. Hertweck, M. Poulsen, C. Beemelmanns

Date Published: 25th Jun 2016

Publication Type: Not specified

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