From 13 C-lignin to 13 C-mycelium: Agaricus bisporus uses polymeric lignin as a carbon source

Author:

Duran Katharina1ORCID,Kohlstedt Michael2ORCID,van Erven Gijs13ORCID,Klostermann Cynthia E.14ORCID,America Antoine H. P.5ORCID,Bakx Edwin1ORCID,Baars Johan J. P.67ORCID,Gorissen Antonie8ORCID,de Visser Ries8ORCID,de Vries Ronald P.9ORCID,Wittmann Christoph2ORCID,Comans Rob N. J.10,Kuyper Thomas W.11ORCID,Kabel Mirjam A.1ORCID

Affiliation:

1. Laboratory of Food Chemistry, Wageningen University & Research, Bornse Weilanden 9, 6708 WG Wageningen, Netherlands.

2. Institute of Systems Biotechnology, Saarland University, Campus A 1.5, 66123 Saarbrücken, Germany.

3. Wageningen Food and Biobased Research, Wageningen University & Research, Bornse Weilanden 9, 6708 WG Wageningen, Netherlands.

4. Biobased Chemistry and Technology, Wageningen University & Research, Bornse Weilanden 9, 6708 WG Wageningen Netherlands.

5. Bioscience, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB Wageningen, Netherlands.

6. Plant Breeding, Wageningen University & Research, 6708 PB Wageningen, Netherlands.

7. CNC Grondstoffen, Driekronenstraat 6, 6596 MA Milsbeek, Netherlands.

8. IsoLife bv, Droevendaalsesteeg 1, 6708 PB Wageningen, Netherlands.

9. Fungal Physiology, Westerdijk Fungal Biodiversity Institute & Fungal Molecular Physiology, Utrecht University, Uppsalalaan 8, 3584 CT Utrecht, Netherlands.

10. Soil Chemistry and Chemical Soil Quality Group, Wageningen University & Research, Droevendaalsesteeg 3a, 6708 PB Wageningen, Netherlands.

11. Soil Biology Group, Wageningen University & Research, Droevendaalsesteeg 3a, 6708 PB Wageningen, Netherlands.

Abstract

Plant biomass conversion by saprotrophic fungi plays a pivotal role in terrestrial carbon (C) cycling. The general consensus is that fungi metabolize carbohydrates, while lignin is only degraded and mineralized to CO 2 . Recent research, however, demonstrated fungal conversion of 13 C-monoaromatic compounds into proteinogenic amino acids. To unambiguously prove that polymeric lignin is not merely degraded, but also metabolized, carefully isolated 13 C-labeled lignin served as substrate for Agaricus bisporus , the world’s most consumed mushroom. The fungus formed a dense mycelial network, secreted lignin-active enzymes, depolymerized, and removed lignin. With a lignin carbon use efficiency of 0.14 (g/g) and fungal biomass enrichment in 13 C, we demonstrate that A. bisporus assimilated and further metabolized lignin when offered as C-source. Amino acids were high in 13 C-enrichment, while fungal-derived carbohydrates, fatty acids, and ergosterol showed traces of 13 C. These results hint at lignin conversion via aromatic ring-cleaved intermediates to central metabolites, underlining lignin’s metabolic value for fungi.

Publisher

American Association for the Advancement of Science (AAAS)

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