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Complementary substrate-selectivity of metabolic adaptive convergence in the lignocellulolytic performance by Dichomitus squalens.

ABSTRACT: The lignocellulolytic platform of the wood-decaying organism Dichomitus squalens is important for production of biodegradable elements; however, the system has not yet been fully characterized. In this study, using statistical target optimization, we analysed substrate selectivity based on a variety of D.?squalens metabolic pathways using combined omics tools. As compared with the alkali-lignin (AL) programme, the rice straw (RS) programme has the advantage of multilayered signalling to regulate cellulolytic-related genes or to connect their pathways. The spontaneous instability of the AL programme was accelerated by harsh starvation as compared with that of the RS programme. Therefore, the AL programme converged on cellular maintenance much easier and more rapidly. However, regardless of external substrate/concentration type, the compensatory pattern of the major targets (especially peroxidases and growth regulators) was similar, functioning to maintain cellular homeostasis. Interestingly, ligninolytic-mediated targets under non-kaleidoscopic conditions were induced by a substrate-input-control, and especially this mechanism had an important effect on the early stages of the biodegradation process. This optimized target analysis could be used to understand lignocellulolytic network and to improve downstream efficiency.

SUBMITTER: Bak JS

PROVIDER: S-EPMC4229324 | biostudies-literature | 2014 Sep

REPOSITORIES: biostudies-literature

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Complementary substrate-selectivity of metabolic adaptive convergence in the lignocellulolytic performance by Dichomitus squalens.

Bak Jin Seop JS

Microbial biotechnology 20140603 5

The lignocellulolytic platform of the wood-decaying organism Dichomitus squalens is important for production of biodegradable elements; however, the system has not yet been fully characterized. In this study, using statistical target optimization, we analysed substrate selectivity based on a variety of D. squalens metabolic pathways using combined omics tools. As compared with the alkali-lignin (AL) programme, the rice straw (RS) programme has the advantage of multilayered signalling to regulate ...[more]

PMID: 24894915

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Project description:The extent of carbon catabolite repression (CCR) at a global level is unknown in wood-rotting fungi, which are critical to the carbon cycle and are a source of biotechnological enzymes. CCR occurs in the presence of sufficient concentrations of easily metabolizable carbon sources (e.g., glucose) and involves downregulation of the expression of genes encoding enzymes involved in the breakdown of complex carbon sources. We investigated this phenomenon in the white-rot fungus Dichomitus squalens using transcriptomics and exoproteomics. In D. squalens cultures, approximately 7% of genes were repressed in the presence of glucose compared to Avicel or xylan alone. The glucose-repressed genes included the essential components for utilization of plant biomass-carbohydrate-active enzyme (CAZyme) and carbon catabolic genes. The majority of polysaccharide-degrading CAZyme genes were repressed and included activities toward all major carbohydrate polymers present in plant cell walls, while repression of ligninolytic genes also occurred. The transcriptome-level repression of the CAZyme genes observed on the Avicel cultures was strongly supported by exoproteomics. Protease-encoding genes were generally not glucose repressed, indicating their likely dominant role in scavenging for nitrogen rather than carbon. The extent of CCR is surprising, given that D. squalens rarely experiences high free sugar concentrations in its woody environment, and it indicates that biotechnological use of D. squalens for modification of plant biomass would benefit from derepressed or constitutively CAZyme-expressing strains.IMPORTANCE White-rot fungi are critical to the carbon cycle because they can mineralize all wood components using enzymes that also have biotechnological potential. The occurrence of carbon catabolite repression (CCR) in white-rot fungi is poorly understood. Previously, CCR in wood-rotting fungi has only been demonstrated for a small number of genes. We demonstrated widespread glucose-mediated CCR of plant biomass utilization in the white-rot fungus Dichomitus squalens This indicates that the CCR mechanism has been largely retained even though wood-rotting fungi rarely experience commonly considered CCR conditions in their woody environment. The general lack of repression of genes encoding proteases along with the reduction in secreted CAZymes during CCR suggested that the retention of CCR may be connected with the need to conserve nitrogen use during growth on nitrogen-scarce wood. The widespread repression indicates that derepressed strains could be beneficial for enzyme production.

Project description:Lignocellulosic plant biomass is an important feedstock for bio-based economy. In particular, it is an abundant renewable source of aromatic compounds, which are present as part of lignin, as side-groups of xylan and pectin, and in other forms, such as tannins. As filamentous fungi are the main organisms that modify and degrade lignocellulose, they have developed a versatile metabolism to convert the aromatic compounds that are toxic at relatively low concentrations to less toxic ones. During this process, fungi form metabolites some of which represent high-value platform chemicals or important chemical building blocks, such as benzoic, vanillic, and protocatechuic acid. Especially basidiomycete white-rot fungi with unique ability to degrade the recalcitrant lignin polymer are expected to perform highly efficient enzymatic conversions of aromatic compounds, thus having huge potential for biotechnological exploitation. However, the aromatic metabolism of basidiomycete fungi is poorly studied and knowledge on them is based on the combined results of studies in variety of species, leaving the overall picture in each organism unclear. Dichomitus squalens is an efficiently wood-degrading white-rot basidiomycete that produces a diverse set of extracellular enzymes targeted for lignocellulose degradation, including oxidative enzymes that act on lignin. Our recent study showed that several intra- and extracellular aromatic compounds were produced when D. squalens was cultivated on spruce wood, indicating also versatile aromatic metabolic abilities for this species. In order to provide the first molecular level systematic insight into the conversion of plant biomass derived aromatic compounds by basidiomycete fungi, we analyzed the transcriptomes of D. squalens when grown with 10 different lignocellulose-related aromatic monomers. Significant differences for example with respect to the expression of lignocellulose degradation related genes, but also putative genes encoding transporters and catabolic pathway genes were observed between the cultivations supplemented with the different aromatic compounds. The results demonstrate that the transcriptional response of D. squalens is highly dependent on the specific aromatic compounds present suggesting that instead of a common regulatory system, fine-tuned regulation is needed for aromatic metabolism.

Dataset Information

Complementary substrate-selectivity of metabolic adaptive convergence in the lignocellulolytic performance by Dichomitus squalens.

Publications

Complementary substrate-selectivity of metabolic adaptive convergence in the lignocellulolytic performance by Dichomitus squalens.

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