Plant biomass degrading ability of the coprophilic ascomycete fungus Podospora anserina

Couturier, Marie; Tangthirasunun, Narumon; Xie, Ning; Brun, Sylvain; Gautier, Valérie; Bennati-Granier, Chloé; Silar, Philippe; Berrin, Jean‐Guy

doi:10.1016/j.biotechadv.2016.05.010

Cited by 34 publications

(27 citation statements)

References 48 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…As expected from its wealth of carbohydrate-active enzymes [5], the fungus degraded the hemicellulosic carbohydrates with a clear preference. Still, though ligninolytic activity of P. anserina has previously been considered [13], this is the first evidence that the fungus is actually able to degrade and remove the aromatic biopolymer.…”

Section: Fate Of Carbohydrates and Lignin After Growth Of P Anserinamentioning

confidence: 77%

“…anserina on wheat straw lignin isolate and insoluble wheat glucoronoarabinoxylan. Total insoluble and water-soluble fractions based on compositional analysis by using quantitative 13 C-IS py-GC-MS (lignin) and constituent monosaccharide analysis after H 2 SO 4 hydrolysis (carbohydrates). Others represent residual dry matter.…”

Section: Structural Characterization Of Lignin After Growth Of P Ansmentioning

confidence: 99%

“…The fungus, furthermore, showed a dependency on catalases to grow on lignocellulose, which was related to the regulation of H 2 O 2 levels [12]. Considering the biotope, the fungus might besides its well-studied carbohydrate-degrading enzymatic arsenal also possess ligninolytic activity, which could broaden the scope of the exploitation of P. anserina in biomass upgrading approaches [13]. The suggestion of possible ligninolytic activity is based on the ability of the fungus to grow on a variety of lignocellulosic substrates, including nearly pure lignin (heavily pretreated, Kraft lignin), and its genome that encodes several putative lignin-active enzymes including laccases and H 2 O 2 -producing oxidoreductases [5,12,14].…”

mentioning

confidence: 99%

See 2 more Smart Citations

Evidence for ligninolytic activity of the ascomycete fungus Podospora anserina

Erven

Kleijn

Patyshakuliyeva

et al. 2020

Biotechnol Biofuels

View full text Add to dashboard Cite

Background: The ascomycete fungus Podospora anserina has been appreciated for its targeted carbohydrate-active enzymatic arsenal. As a late colonizer of herbivorous dung, the fungus acts specifically on the more recalcitrant fraction of lignocellulose and this lignin-rich biotope might have resulted in the evolution of ligninolytic activities. However, the lignin-degrading abilities of the fungus have not been demonstrated by chemical analyses at the molecular level and are, thus far, solely based on genome and secretome predictions. To evaluate whether P. anserina might provide a novel source of lignin-active enzymes to tap into for potential biotechnological applications, we comprehensively mapped wheat straw lignin during fungal growth and characterized the fungal secretome.Results: Quantitative 13 C lignin internal standard py-GC-MS analysis showed substantial lignin removal during the 7 days of fungal growth (24% w/w), though carbohydrates were preferably targeted (58% w/w removal). Structural characterization of residual lignin by using py-GC-MS and HSQC NMR analyses demonstrated that C α -oxidized substructures significantly increased through fungal action, while intact β-O-4′ aryl ether linkages, p-coumarate and ferulate moieties decreased, albeit to lesser extents than observed for the action of basidiomycetes. Proteomic analysis indicated that the presence of lignin induced considerable changes in the secretome of P. anserina. This was particularly reflected in a strong reduction of cellulases and galactomannanases, while H 2 O 2 -producing enzymes clearly increased. The latter enzymes, together with laccases, were likely involved in the observed ligninolysis. Conclusions:For the first time, we provide unambiguous evidence for the ligninolytic activity of the ascomycete fungus P. anserina and expand the view on its enzymatic repertoire beyond carbohydrate degradation. Our results can be of significance for the development of biological lignin conversion technologies by contributing to the quest for novel lignin-active enzymes and organisms.

show abstract

Section: Fate Of Carbohydrates and Lignin After Growth Of P Anserinamentioning

confidence: 77%

Section: Structural Characterization Of Lignin After Growth Of P Ansmentioning

confidence: 99%

mentioning

confidence: 99%

See 1 more Smart Citation

Evidence for ligninolytic activity of the ascomycete fungus Podospora anserina

Erven

Kleijn

Patyshakuliyeva

et al. 2020

Biotechnol Biofuels

View full text Add to dashboard Cite

show abstract

“…The coprophilous fungus Podospora anserina displays an impressive array of CAZymes [18, 19] with 189 glycoside hydrolases and 33 genes encoding AA9 LPMOs ( Pa LPMO9), of which seven have been characterized biochemically [15, 20]. These LMPOs are able to oxidatively cleave cellulose with different regioselectivity.…”

Section: Introductionmentioning

confidence: 99%

The Podospora anserina lytic polysaccharide monooxygenase PaLPMO9H catalyzes oxidative cleavage of diverse plant cell wall matrix glycans

Fanuel

Garajová

Ropartz

et al. 2017

Biotechnol Biofuels

Self Cite

View full text Add to dashboard Cite

BackgroundThe enzymatic conversion of plant biomass has been recently revolutionized by the discovery of lytic polysaccharide monooxygenases (LPMO) that catalyze oxidative cleavage of polysaccharides. These powerful enzymes are secreted by a large number of fungal saprotrophs and are important components of commercial enzyme cocktails used for industrial biomass conversion. Among the 33 AA9 LPMOs encoded by the genome of Podospora anserina, the PaLPMO9H enzyme catalyzes mixed C1/C4 oxidative cleavage of cellulose and cello-oligosaccharides. Activity of PaLPMO9H on several hemicelluloses has been suggested, but the regioselectivity of the cleavage remained to be determined.ResultsIn this study, we investigated the activity of PaLPMO9H on mixed-linkage glucans, xyloglucan and glucomannan using tandem mass spectrometry and ion mobility–mass spectrometry. Structural analysis of the released products revealed that PaLPMO9H catalyzes C4 oxidative cleavage of mixed-linkage glucans and mixed C1/C4 oxidative cleavage of glucomannan and xyloglucan. Gem-diols and ketones were produced at the non-reducing end, while aldonic acids were produced at the reducing extremity of the products.ConclusionThe ability of PaLPMO9H to target polysaccharides, differing from cellulose by their linkages, glycosidic composition and/or presence of sidechains, could be advantageous for this coprophilous fungus when catabolizing highly variable polysaccharides and for the development of optimized enzyme cocktails in biorefineries.Electronic supplementary materialThe online version of this article (doi:10.1186/s13068-017-0749-5) contains supplementary material, which is available to authorized users.

show abstract

“…To gain insight into the actual role of CDH, we performed a thorough analysis of the role of the three enzymes encoded by the genome of the filamentous ascomycete P. anserina. This filamentous fungus is easy to manipulate and is able to rapidly complete its life cycle with wood as the sole carbon source (29)(30)(31). Gene deletions and construction of multiple mutants can rapidly be achieved.…”

mentioning

confidence: 99%

Inactivation of Cellobiose Dehydrogenases Modifies the Cellulose Degradation Mechanism of Podospora anserina

Tangthirasunun

Navarro

Garajová

et al. 2017

Appl Environ Microbiol

Self Cite

View full text Add to dashboard Cite

Conversion of biomass into high-value products, including biofuels, is of great interest to developing sustainable biorefineries. Fungi are an inexhaustible source of enzymes to degrade plant biomass. Cellobiose dehydrogenases (CDHs) play an important role in the breakdown through synergistic action with fungal lytic polysaccharide monooxygenases (LPMOs). The three CDH genes of the model fungus Podospora anserina were inactivated, resulting in single and multiple CDH mutants. We detected almost no difference in growth and fertility of the mutants on various lignocellulose sources, except on crystalline cellulose, on which a 2-fold decrease in fertility of the mutants lacking P. anserina CDH1 (PaCDH1) and PaCDH2 was observed. A striking difference between wild-type and mutant secretomes was observed. The secretome of the mutant lacking all CDHs contained five beta-glucosidases, whereas the wild type had only one. P. anserina seems to compensate for the lack of CDH with secretion of beta-glucosidases. The addition of P. anserina LPMO to either the wild-type or mutant secretome resulted in improvement of cellulose degradation in both cases, suggesting that other redox partners present in the mutant secretome provided electrons to LPMOs. Overall, the data showed that oxidative degradation of cellulosic biomass relies on different types of mechanisms in fungi.IMPORTANCE Plant biomass degradation by fungi is a complex process involving dozens of enzymes. The roles of each enzyme or enzyme class are not fully understood, and utilization of a model amenable to genetic analysis should increase the comprehension of how fungi cope with highly recalcitrant biomass. Here, we report that the cellobiose dehydrogenases of the model fungus Podospora anserina enable it to consume crystalline cellulose yet seem to play a minor role on actual substrates, such as wood shavings or miscanthus. Analysis of secreted proteins suggests that Podospora anserina compensates for the lack of cellobiose dehydrogenase by increasing beta-glucosidase expression and using an alternate electron donor for LPMO.

show abstract

Plant biomass degrading ability of the coprophilic ascomycete fungus Podospora anserina

Cited by 34 publications

References 48 publications

Evidence for ligninolytic activity of the ascomycete fungus Podospora anserina

Evidence for ligninolytic activity of the ascomycete fungus Podospora anserina

The Podospora anserina lytic polysaccharide monooxygenase PaLPMO9H catalyzes oxidative cleavage of diverse plant cell wall matrix glycans

Inactivation of Cellobiose Dehydrogenases Modifies the Cellulose Degradation Mechanism of Podospora anserina

Contact Info

Product

Resources

About