A06

Overview

ISOLATION, CHARACTERIZATION AND FUNCTIONAL ANALYSIS OF NOVEL BIOMOLECULES FROM THE MUTUALISTIC FOOD FUNGUS AND ASSOCIATED MICROBES OF FUNGUS-GROWING TERMITES

SEEK ID: https://data.chembiosys.de/projects/25

Public web page: Not specified

Organisms: No Organisms specified

PALs: No PALs for this Project

Project start date: 1st Jun 2018

Related items

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The Termite Fungal Cultivar Termitomyces Combines Diverse Enzymes and Oxidative Reactions for Plant Biomass Conversion.
A06

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.
A06

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.
A06

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.
A06

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.
A06

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

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