Extracellular electron transfer systems fuel cellulose oxidative degradation

Kracher, Daniel; Scheiblbrandner, Stefan; Felice, Alfons K. G.; Breslmayr, Erik; Preims, Marita; Ludwicka, Karolina; Haltrich, Dietmar; Eijsink, Vincent G. H.; Ludwig, Roland

doi:10.1126/science.aaf3165

Cited by 345 publications

(489 citation statements)

References 111 publications

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“…Phylogenetic prediction of the function of this flavo-oxidase is hampered by the small number of characterized members of the AA3_2 subfamily (47). Our findings are in agreement with recent findings showing that AA3_2 GMC oxidoreductases can serve as extracellular electron sources for LPMOs (38,39), thus extending the array of fungal redox partners in filamentous fungi. Overall, the present data suggest that compensatory mechanisms indeed enable P. anserina to cope with lack of CDH for the most part.…”

Section: Resultssupporting

confidence: 81%

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

Tangthirasunun

Navarro

Garajová

et al. 2017

Appl Environ Microbiol

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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.

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Section: Resultssupporting

confidence: 81%

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

Tangthirasunun

Navarro

Garajová

et al. 2017

Appl Environ Microbiol

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“…These oxidative biocatalysts are activated in the presence of an electron donor molecule to facilitate cellulose degradation (2,3). Extensive studies have been performed to identify its potential redox partner, which led to the prediction of diverse exogenous (lignin, ascorbate or photosynthetic pigment) (4), and endogenous (dehydrogenases or oxidoreductases) (18,33) reductants.…”

Section: Discussionmentioning

confidence: 99%

“…Subsequent studies have also shown that a combination of AA9 protein and a co-secretory CDH (cellobiose dehydrogenase) could cleave pure cellulose (17). The identification of CDHs as redox partner for LPMO (18) was primarily dependant on (i) available secretome data which has given evidence about CDH as a LPMO co-secretory proteins and (ii) on theoretical understanding of the electron transport processes involved in LPMO activation (17,(19)(20)(21)(22). However, there are many filamentous fungi which do not secrete CDH (because of obvious lack of encoding gene) and in contrast many ascomycetes are known to encode multiple CDHs (20), suggesting that the choice of redox partner is very specific to type of LPMO and no general concept exist.…”

Section: Introductionmentioning

confidence: 99%

WITHDRAWN: Identification of an endogenous redox partner for lytic polysaccharide monooxygenase-based oxidative cleavage of polysaccharides

2017

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“…W hen microbial cells cannot import or are physically separated from metabolic electron donors or acceptors, diffusible compounds can act as electron carriers and support survival on these substrates (1,2). These conditions arise in the presence of poised-potential electrodes or insoluble minerals, such as iron oxides (3)(4)(5), and in multicellular communities (biofilms) where the formation of chemical gradients leads to oxidant limitation for cells at depth (6)(7)(8)(9).…”

mentioning

confidence: 99%

Electron-shuttling antibiotics structure bacterial communities by modulating cellular levels of c-di-GMP

Okegbe

Fields

Cole

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Diverse organisms secrete redox-active antibiotics, which can be used as extracellular electron shuttles by resistant microbes. Shuttlemediated metabolism can support survival when substrates are available not locally but rather at a distance. Such conditions arise in multicellular communities, where the formation of chemical gradients leads to resource limitation for cells at depth. In the pathogenic bacterium Pseudomonas aeruginosa PA14, antibiotics called phenazines act as oxidants to balance the intracellular redox state of cells in anoxic biofilm subzones. PA14 colony biofilms show a profound morphogenic response to phenazines resulting from electron acceptor-dependent inhibition of ECM production. This effect is reminiscent of the developmental responses of some eukaryotic systems to redox control, but for bacterial systems its mechanistic basis has not been well defined. Here, we identify the regulatory protein RmcA and show that it links redox conditions to PA14 colony morphogenesis by modulating levels of bis-(3′,5′)-cyclic-dimeric-guanosine (c-di-GMP), a second messenger that stimulates matrix production, in response to phenazine availability. RmcA contains four Per-Arnt-Sim (PAS) domains and domains with the potential to catalyze the synthesis and degradation of c-di-GMP. Our results suggest that phenazine production modulates RmcA activity such that the protein degrades c-di-GMP and thereby inhibits matrix production during oxidizing conditions. RmcA thus forms a mechanistic link between cellular redox sensing and community morphogenesis analogous to the functions performed by PAS-domain-containing regulatory proteins found in complex eukaryotes.W hen microbial cells cannot import or are physically separated from metabolic electron donors or acceptors, diffusible compounds can act as electron carriers and support survival on these substrates (1, 2). These conditions arise in the presence of poised-potential electrodes or insoluble minerals, such as iron oxides (3-5), and in multicellular communities (biofilms) where the formation of chemical gradients leads to oxidant limitation for cells at depth (6-9). Diverse microbes secrete redoxactive compounds with the capacity to function as electron shuttles (10-12). In the pathogenic bacterium Pseudomonas aeruginosa PA14, electron-shuttling antibiotics called phenazines support survival on poised-potential electrodes and balance the intracellular redox state of cells in anoxic biofilm subzones (1, 9).Similar to those formed by many species of microbes, colonies of PA14 develop intricate wrinkle structures on agar-solidified growth media (13). Phenazines profoundly alter PA14 colony morphogenesis, inhibiting the onset of wrinkle formation and changing the organization of wrinkles (12) (Fig. 1A). Modeling of resource availability within colonies suggests that the earlier increase in the colony surface area-to-volume ratio in phenazine-null (Δphz) mutants maximizes access to oxygen for cells that would otherwise become limited for oxidant (14). Measurements of...

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Extracellular electron transfer systems fuel cellulose oxidative degradation

Cited by 345 publications

References 111 publications

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

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

WITHDRAWN: Identification of an endogenous redox partner for lytic polysaccharide monooxygenase-based oxidative cleavage of polysaccharides

Electron-shuttling antibiotics structure bacterial communities by modulating cellular levels of c-di-GMP

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