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Genome-wide transcriptomic analysis of a superior biomass-degrading strain of A. fumigatus revealed active lignocellulose-degrading genes.

Miao Y, Liu D, Li G, Li P, Xu Y, Shen Q, Zhang R - BMC Genomics (2015)

Bottom Line: It consists of complex carbohydrates and aromatic polymers found in the plant cell wall and thus in plant debris.Transcriptional responses of A. fumigatus Z5 induced by sucrose, oat spelt xylan, Avicel PH-101 and rice straw were compared.There were 444, 1711 and 1386 significantly differently expressed genes in xylan, cellulose and rice straw, respectively, when compared to sucrose as a control condition.

View Article: PubMed Central - PubMed

Affiliation: Jiangsu Key Lab and Engineering Center for Solid Organic Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Nanjing, 210095, P.R. China. 2011203046@njau.edu.cn.

ABSTRACT

Background: Various saprotrophic microorganisms, especially filamentous fungi, can efficiently degrade lignocellulose that is one of the most abundant natural materials on earth. It consists of complex carbohydrates and aromatic polymers found in the plant cell wall and thus in plant debris. Aspergillus fumigatus Z5 was isolated from compost heaps and showed highly efficient plant biomass-degradation capability.

Results: The 29-million base-pair genome of Z5 was sequenced and 9540 protein-coding genes were predicted and annotated. Genome analysis revealed an impressive array of genes encoding cellulases, hemicellulases and pectinases involved in lignocellulosic biomass degradation. Transcriptional responses of A. fumigatus Z5 induced by sucrose, oat spelt xylan, Avicel PH-101 and rice straw were compared. There were 444, 1711 and 1386 significantly differently expressed genes in xylan, cellulose and rice straw, respectively, when compared to sucrose as a control condition.

Conclusions: Combined analysis of the genomic and transcriptomic data provides a comprehensive understanding of the responding mechanisms to the most abundant natural polysaccharides in A. fumigatus. This study provides a basis for further analysis of genes shown to be highly induced in the presence of polysaccharide substrates and also the information which could prove useful for biomass degradation and heterologous protein expression.

No MeSH data available.


The conditions of degrading-enzyme gene expression. The whole histogram includes all genes in that group, and black indicates the genes that were significantly different in that treatment compared to sucrose. a CAZyme gene numbers with significantly different expression levels in xylan, rice straw and cellulose when compared to sucrose control. b Hydrolase genes with significantly different expression levels in xylan, rice straw and cellulose compared to sucrose
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Fig9: The conditions of degrading-enzyme gene expression. The whole histogram includes all genes in that group, and black indicates the genes that were significantly different in that treatment compared to sucrose. a CAZyme gene numbers with significantly different expression levels in xylan, rice straw and cellulose when compared to sucrose control. b Hydrolase genes with significantly different expression levels in xylan, rice straw and cellulose compared to sucrose

Mentions: Genome analysis showed the potential of a wide spectrum of polysaccharide hydrolytic enzymes produced by A. fumigatus Z5. In order to determine which hydrolytic enzyme-encoding genes were induced by different substrates (sucrose, xylan, cellulose and rice straw), the transcriptional profiles of A. fumigatus Z5 under these conditions were determined. Xylan, as the major component of hemicellulose, was used as a sole carbon source to induce the expression of hemicellulase genes, while cellulose was used as the inducer of cellulases. Rice straw, which contains various polysaccharide components, was chosen as a carbon source to study the diversity of the degradation enzymes. A. fumigatus Z5 was grown on 2 % sucrose (used as control), and the mycelia were transferred to 1 % (w/v) xylan, cellulose or rice straw as the sole carbon source for 16 h. Gene expression patterns revealed that comparable genes were differentially expressed in each transcriptome, and many had similar patterns (Figs. 7 and 8). The xylan-induced gene expression pattern (XGEP) is relatively similar to the sucrose-induced gene expression pattern (SGEP), which may be due to the high efficiency of xylan degradation (data not shown) and xylose-induced carbon catabolite repression [41, 42]. However, the cellulose-induced gene expression pattern (CGEP) and the rice straw-induced gene expression pattern (RGEP) differ significantly from the SGEP (Fig. 7b, c). The main aim of this study was to focus on genes that have significantly different expression among the 4 different treatments. Four hundred and two genes were identified in cluster 3 and cluster 4, which showed higher expression levels in the XGEP, CGEP and RGEP than in the SGEP. These two clusters contained nearly all of the polysaccharides-degrading genes, including 14 cellulases (7 EGs: Y699_00150, Y699_02424, Y699_05430, Y699_06174, Y699_07518, Y699_08637 and Y699_08692; 2 CBHs: Y699_03865 and Y699_07898; 3 β-glucosidases: Y699_00561, Y699_01298 and Y699_08636), nine xylanases (5 endo-1,4-beta-xylanases: Y699_04481, Y699_06333, Y699_07611, Y699_07623 and Y699_09486; 4 β-xylosidases: Y699_04570, Y699_04662, Y699_05610 and Y699_07880), 2 alpha-L-arabinofuranosidases and 2 acetyl xylan esterases. Seven other cellulases (3 EGs: Y699_02044, Y699_04295 and Y699_05825; 4 β-glucosidases: Y699_00572, Y699_04562, Y699_06723 and Y699_09150) were found in cluster 6 and were expressed at higher levels in the CGEP and RGEP than in the SGEP and XGEP. Together, these results show that both cellulose and xylan can induce the expression of cellulase and xylanase genes, but xylan induces fewer cellulase genes (Fig. 9). Three cellobiose dehydrogenase (cdh) genes (Y699_02120, Y699_04685 and Y699_05507) were detected in the A. fumigatus Z5 genome. Consistent with a recent report that cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase can enhance cellulose degradation [43], we found that the cdh gene (Y699_02120) was induced by the substrates cellulose and rice straw. Gene Y699_04685 in cluster 2 only had a high expression level in RGEP compared to the three other patterns, suggested that this cellobiose dehydrogenase may not functional in the degradation of cellulose and xylan but may be useful for degradation of other components of plant biomass, such as pectin or other aromatic substrates. Interestingly, two endoglucanase genes (Y699_02418 and Y699_05110) were also located in cluster 2, which indicated that these two genes may not functional in the degradation of cellulose due to their low expressional levels in the CGEP.Fig. 7


Genome-wide transcriptomic analysis of a superior biomass-degrading strain of A. fumigatus revealed active lignocellulose-degrading genes.

Miao Y, Liu D, Li G, Li P, Xu Y, Shen Q, Zhang R - BMC Genomics (2015)

The conditions of degrading-enzyme gene expression. The whole histogram includes all genes in that group, and black indicates the genes that were significantly different in that treatment compared to sucrose. a CAZyme gene numbers with significantly different expression levels in xylan, rice straw and cellulose when compared to sucrose control. b Hydrolase genes with significantly different expression levels in xylan, rice straw and cellulose compared to sucrose
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4469458&req=5

Fig9: The conditions of degrading-enzyme gene expression. The whole histogram includes all genes in that group, and black indicates the genes that were significantly different in that treatment compared to sucrose. a CAZyme gene numbers with significantly different expression levels in xylan, rice straw and cellulose when compared to sucrose control. b Hydrolase genes with significantly different expression levels in xylan, rice straw and cellulose compared to sucrose
Mentions: Genome analysis showed the potential of a wide spectrum of polysaccharide hydrolytic enzymes produced by A. fumigatus Z5. In order to determine which hydrolytic enzyme-encoding genes were induced by different substrates (sucrose, xylan, cellulose and rice straw), the transcriptional profiles of A. fumigatus Z5 under these conditions were determined. Xylan, as the major component of hemicellulose, was used as a sole carbon source to induce the expression of hemicellulase genes, while cellulose was used as the inducer of cellulases. Rice straw, which contains various polysaccharide components, was chosen as a carbon source to study the diversity of the degradation enzymes. A. fumigatus Z5 was grown on 2 % sucrose (used as control), and the mycelia were transferred to 1 % (w/v) xylan, cellulose or rice straw as the sole carbon source for 16 h. Gene expression patterns revealed that comparable genes were differentially expressed in each transcriptome, and many had similar patterns (Figs. 7 and 8). The xylan-induced gene expression pattern (XGEP) is relatively similar to the sucrose-induced gene expression pattern (SGEP), which may be due to the high efficiency of xylan degradation (data not shown) and xylose-induced carbon catabolite repression [41, 42]. However, the cellulose-induced gene expression pattern (CGEP) and the rice straw-induced gene expression pattern (RGEP) differ significantly from the SGEP (Fig. 7b, c). The main aim of this study was to focus on genes that have significantly different expression among the 4 different treatments. Four hundred and two genes were identified in cluster 3 and cluster 4, which showed higher expression levels in the XGEP, CGEP and RGEP than in the SGEP. These two clusters contained nearly all of the polysaccharides-degrading genes, including 14 cellulases (7 EGs: Y699_00150, Y699_02424, Y699_05430, Y699_06174, Y699_07518, Y699_08637 and Y699_08692; 2 CBHs: Y699_03865 and Y699_07898; 3 β-glucosidases: Y699_00561, Y699_01298 and Y699_08636), nine xylanases (5 endo-1,4-beta-xylanases: Y699_04481, Y699_06333, Y699_07611, Y699_07623 and Y699_09486; 4 β-xylosidases: Y699_04570, Y699_04662, Y699_05610 and Y699_07880), 2 alpha-L-arabinofuranosidases and 2 acetyl xylan esterases. Seven other cellulases (3 EGs: Y699_02044, Y699_04295 and Y699_05825; 4 β-glucosidases: Y699_00572, Y699_04562, Y699_06723 and Y699_09150) were found in cluster 6 and were expressed at higher levels in the CGEP and RGEP than in the SGEP and XGEP. Together, these results show that both cellulose and xylan can induce the expression of cellulase and xylanase genes, but xylan induces fewer cellulase genes (Fig. 9). Three cellobiose dehydrogenase (cdh) genes (Y699_02120, Y699_04685 and Y699_05507) were detected in the A. fumigatus Z5 genome. Consistent with a recent report that cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase can enhance cellulose degradation [43], we found that the cdh gene (Y699_02120) was induced by the substrates cellulose and rice straw. Gene Y699_04685 in cluster 2 only had a high expression level in RGEP compared to the three other patterns, suggested that this cellobiose dehydrogenase may not functional in the degradation of cellulose and xylan but may be useful for degradation of other components of plant biomass, such as pectin or other aromatic substrates. Interestingly, two endoglucanase genes (Y699_02418 and Y699_05110) were also located in cluster 2, which indicated that these two genes may not functional in the degradation of cellulose due to their low expressional levels in the CGEP.Fig. 7

Bottom Line: It consists of complex carbohydrates and aromatic polymers found in the plant cell wall and thus in plant debris.Transcriptional responses of A. fumigatus Z5 induced by sucrose, oat spelt xylan, Avicel PH-101 and rice straw were compared.There were 444, 1711 and 1386 significantly differently expressed genes in xylan, cellulose and rice straw, respectively, when compared to sucrose as a control condition.

View Article: PubMed Central - PubMed

Affiliation: Jiangsu Key Lab and Engineering Center for Solid Organic Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Nanjing, 210095, P.R. China. 2011203046@njau.edu.cn.

ABSTRACT

Background: Various saprotrophic microorganisms, especially filamentous fungi, can efficiently degrade lignocellulose that is one of the most abundant natural materials on earth. It consists of complex carbohydrates and aromatic polymers found in the plant cell wall and thus in plant debris. Aspergillus fumigatus Z5 was isolated from compost heaps and showed highly efficient plant biomass-degradation capability.

Results: The 29-million base-pair genome of Z5 was sequenced and 9540 protein-coding genes were predicted and annotated. Genome analysis revealed an impressive array of genes encoding cellulases, hemicellulases and pectinases involved in lignocellulosic biomass degradation. Transcriptional responses of A. fumigatus Z5 induced by sucrose, oat spelt xylan, Avicel PH-101 and rice straw were compared. There were 444, 1711 and 1386 significantly differently expressed genes in xylan, cellulose and rice straw, respectively, when compared to sucrose as a control condition.

Conclusions: Combined analysis of the genomic and transcriptomic data provides a comprehensive understanding of the responding mechanisms to the most abundant natural polysaccharides in A. fumigatus. This study provides a basis for further analysis of genes shown to be highly induced in the presence of polysaccharide substrates and also the information which could prove useful for biomass degradation and heterologous protein expression.

No MeSH data available.